C H A P T E R

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Somatosensory SystemJon H. Kaas

Vanderbilt University, Nashville, Tennessee, USA

O U T L I N E

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Introduction 1075

Receptor Types and Afferent Pathways 1076

he Hu

Low-Threshold Mechanoreceptor Afferentsfrom the Hand 1077

man

The SA-I Afferent or the Non-Pacinian Iii

(NP Iii) Channel 1077

The RA-I Afferent or the Non-Pacinian I

(NPI) Channel 1078

The SA-II Afferent or Non-Pacinian II (NP II)

Channel 1078

The RA-II Afferent or Pacinian (PC) Channel 1079

Cutaneous Receptor Afferents of the Hairy Skin 1079

Deep Receptor Afferents 1080 C-Fiber and A-delta Afferents Mediating

Temperature, Itch, Pain, and Touch 1080

Afferent Pathways 1081 Terminations of Peripheral Nerve Afferents in the

Spinal Cord and Brainstem 1081

Ascending Spinal Cord Pathways 1082 The Dorsal (Posterior) Column System 1082 Second-Order Axons of the Dorsolateral

Spinal Cord (The Spinomedullothalamic System) 1083

The Spinothalamic Pathways 1084

Relay Nuclei of the Medulla and UpperSpinal Cord 1084

Dorsal ColumneTrigeminal Nuclear Complex 1084 Lateral Cervical Nucleus, Nuclei X and Z,

External Cuneate Nucleus, and Clarke’sColumn 1085

Lateral Cervical Nucleus 1085 Nuclei X and Z 1085 External Cuneate Nucleus 1085 Clarke’s Nucleus or Column 1085

Somatosensory Regions of the Midbrain 1085

Somatosensory Thalamus 1086

Ventroposterior Nucleus (VP) 1086

1074Nervous System, Third Edition DOI: 10.1016/B978-0-12-374236-0.10030-6

Ventroposterior Superior Nucleus 1088

Ventroposterior Inferior Nucleus 1088 The Posterior Group and the Posterior Ventromedial

Nucleus 1088

Anterior Pulvinar, Medial Pulvinar, and Lateral

Posterior Nucleus 1089

Anterior Parietal Cortex 1089

Anterior Parietal Cortex in Monkeys 1089

Area 3b 1090

Area 1 1090 Area 2 1091 Area 3a 1091 Subcortical Projections 1091

Anterior Parietal Cortex in Humans 1091

Architectonic Fields 1091 Maps in 3a, 3b, 1, and 2: Evidence from Scalp

and Brain Surface Recordings 1092

Sensory and Perceptual Impairments Following

Lesions 1094

Somatosensory Cortex of the Lateral (Sylvian)Sulcus Including Insula 1095

Organization of Cortex of the Lateral Sulcus in

Monkeys 1095

Lateral and Insular Parietal Cortex in Humans 1096

Posterior Parietal Cortex 1097

Posterior Parietal Cortex in Monkeys 1097

Area 5a (PE) 1097

Area 5b (PEc) 1098 Area 7b (PF and PFG) 1098 Area 7a (PG) 1098 Areas of the Intraparietal Sulcus: AIP, LIP,

CIP, VIP, MIP, and PIP 1098

Posterior Parietal Cortex Function in Humans 1100

Somatosensory Cortex of the Medial Wall: TheSupplementary Sensory Area and CingulateCortex 1101

Copyright � 2012 Elsevier Inc. All rights reserved.

INTRODUCTION 1075

INTRODUCTION

This chapter outlines the organization of the somato-sensory system of humans. The emphasis is on thecomponents of this system that are important in identi-fying objects and features of surfaces by touch. Eventhough small shapes can be perceived with informationsolely from tactile receptors, most discriminationsinvolve an active process of tactile exploration andmultiple contacts on the skin, and an integration of cuta-neous and proprioceptive information as well as efferentcontrol. Thus, this chapter concentrates on the pathwaysand neural centers for processing information from thelow-threshold mechanoreceptors of the skin thatprovide information about touch, and the deeper recep-tors in joints and muscles that provide informationabout position. Conclusions are based on both studiesin humans and studies in other primates, especiallythe frequently studied macaque monkeys. At least theearly stages of processing are likely to be similar inhumans and monkeys, but humans appear to havea more expanded cortical network for processingsomatosensory information. The important subsystemsdealing with afferents coding for pain and temperature

FIGURE 30. 1 The basic components of the somatosensory system shproject to the dorsal column nuclei or the trigeminal nuclei to form thbrainstem provide second-order afferents, representing the face, that jterminate in the contralateral ventroposterior complex of the thalamus. Twhere information is distributed to posterior and lateral parietal cortex.

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are only briefly mentioned here, as they are reviewedelsewhere (e.g., Chapter 32).

The basic parts and pathways of the somatosensorysystem of humans are shown in Figure 30.1. In brief,peripheral nerve afferents related to receptors in theskin, muscles, and joints course centrally past their cellbodies in the dorsal root and cranial nerve ganglia toenter the spinal cord and brainstem. These afferentssynapse on neurons in the dorsal horn of the spinalcord, or on equivalent neurons in the brainstem, andsend a collateral to the dorsal column–trigeminalnuclear complex. Most of the second-order neurons inthis complex have axons that cross to the contralaterallower brainstem to form the medial lemniscus columnof axons that ascend to the somatosensory thalamus.Second-order neurons representing the teeth and tongueproject both ipsilaterally and contralaterally to the thal-amus (see Chapter 32). Other second-order neuronsin the dorsal horn of the spinal cord and in the brainstemsend axons to the contralateral side to form theanterolateral spinothalamic ascending pathway (seeFigure 30.4). The low-threshold mechanoreceptor infor-mation from the skin and the information from musclespindle receptors and joints course in the mediallemniscus to terminate in nuclei of the ventroposterior

own on a posterolateral view of a human brain. Receptors in the skine dorsal column trigeminal complex. The trigeminal complex in theoin those from the dorsal column nuclei, representing the body, tohird-order neurons in the thalamus project to anterior parietal cortex,

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30. SOMATOSENSORY SYSTEM1076

thalamic complex. The spinothalamic pathway carriesinformation about pain, temperature, and touch to infe-rior and caudal parts of the ventroposterior complex.

The somatosensory thalamus has been subdivided invarious ways (e.g., Chapter 19; Hirai and Jones, 1989;Mai et al., 1997; Morel et al., 1997; Jones, 2007). Becausesome of the earlier parcellations of thalamic nuclei werebased solely in cytoarchitectonic and myeloarchitectoniccriteria (e.g., Hassler, 1959), and because they do notreflect the many recent advances in understandingbased on microelectrode recordings, studies of connec-tions, and chemoarchitecture, we use more recentlyproposed subdivisions stemming from studies largelyin monkeys (see Kaas, 2008 for review). Thus, the relayof afferents from the skin via the medial lemniscus isto the ventroposterior nucleus (VP), which has beentraditionally subdivided into a ventroposterior medialsubnucleus (VPM) representing the face and a ventro-posterior lateral subnucleus (VPL) representing thebody. The muscle spindle receptor inputs are relayedto a dorsal or superior part of the ventroposteriorcomplex that is often included in VPM and VPL. Wedistinguish this representation of deep body receptorsas the ventroposterior superior nucleus (VPS). Many ofthe spinothalamic afferents terminate in a ventroposte-rior inferior nucleus (VPI). Other spinothalamic affer-ents end in a caudal part of the VP complex that isoften included in VPI or end in the posterior group ofnuclei, part of which has been distinguished as a distinctrelay nucleus for pain and temperature, the ventrome-dial posterior nucleus (VMpo) (Dostrovsky and Craig,2008). The somatosensory thalamus also includes nucleiwithout ascending somatosensory inputs. The anteriorpulvinar (Pa) and the lateral posterior complex (LP)receive inputs from somatosensory cortex and projectback to somatosensory cortex.

The somatosensory cortex has also been variouslysubdivided into proposed subdivisions of functionalsignificance. Most investigators recognize four subdivi-sions of the cortex of the postcentral gyrus, areas 3a,3b, 1, and 2, stemming from the early architectonicstudies of Brodmann (1909) and the Vogts (Vogt andVogt, 1919, 1926). While all four areas were once consid-ered parts of a single functional area, primary somato-sensory cortex or S1, it has been clear for over 25 yearsthat each constitutes a separate representation of thebody. Area 3b corresponds to S1 of cats and rats (Kaas,1983). Areas 3b and 1 correspond to parallel somatotopicrepresentations of cutaneous inputs, while areas 3a and2 integrate cutaneous and deep receptor inputs. Yet, theterm “S1” is commonly used to refer to all four areas inmonkeys and humans. To avoid confusion, the architec-tonic terms for the four fields are used here. Thalamicprojections to areas 3b and 1 are largely from VP,while VPS provides driving inputs to areas 3a and 2.

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VPI and Pa project widely to areas of somatosensorycortex, and LP projects to posterior parietal cortex. Areas3b, l, and 2 form a hierarchical sequence of processing,while area 3a relates especially to motor cortex. Allfour areas project to somatosensory cortex of the lateralsulcus (lateral parietal cortex), especially the secondsomatosensory area, S2, and a more recently discoveredparietal ventral somatosensory area, PV (Krubitzer et al.,1995). These and other areas of the lateral sulcus relate tomotor areas of cortex to guide action, and to perirhinalcortex to engage the hippocampus in object recognitionand memory (Mishkin, 1979). Other connections of area2 and subdivisions of lateral parietal cortex are withsubdivisions of posterior parietal cortex that areinvolved with the early stages of forming movementintentions and sensory guidance for motor actions (Des-murget et al., 2009). Subdivisions of the posterior pari-etal cortex project to premotor and motor areas of thefrontal lobe (e.g., Tanne-Gariepy et al., 2002; Stepniew-ska et al., 2009b). Projections from the posterior parietalcortex also involve the medial limbic cortex of the pari-etal lobe in producing motivational and possiblyemotional states.

RECEPTOR TYPES AND AFFERENTPATHWAYS

In humans, the hand is the most important tactileorgan for object identification (Darian-Smith, 1984).Receptors in the hand must convey information abouttexture and shape. This is done primarily from the fingerpads during active exploration; consequently, fingerposition and temporal sequence are important. Theglabrous (hairless) skin of the hand has the highestinnervation density and tactile acuity of any bodysurface (Darian-Smith, 1984). Hairy skin is less impor-tant in object identification, and hairy skin is less sensi-tive to touch and vibration (Hamalainen and Jarvilehto,1981). However, the hairs themselves provide anincreased sensitivity to air movement and other stimulithat displace hairs (Hamalainen et al., 1985).

Psychophysical, physiological, and anatomicalstudies on humans and other primates support theview that sensations of touch from the glabrous skin ofthe hand are almost completely mediated by fourdifferent types of myelinated, rapidly conducting mech-anoreceptive afferents (Figure 30.2). The afferent classesfrom the glabrous skin include two types of slowlyadapting afferents and two types of rapidly adaptingafferents. All of these types have been extensivelystudied physiologically in monkeys and related toreceptor types. In addition, the response properties ofthese afferents have been characterized during record-ings in humans, and sensations have been evoked by

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FIGURE 30.2 Receptor types (right) and afferent classes (left) of the glabrous skin of humans. Four main classes of low-threshold, rapidlyconducting afferents have been described as slowly adapting type I (SA-I) and type II (SA-II), rapidly adapting type I (RA-I) and type II (RA-II) orPacinian corpuscle (PC). Each relates to a specialized receptor complex in the skin. Based on Johansson (1978), Johansson and Vallbo (1983), andVallbo et al. (1984). The ramp in the adaptation column marks a short period of skin indentation, and the vertical lines represent action potentialsrecorded during the indentation.

RECEPTOR TYPES AND AFFERENT PATHWAYS 1077

electrical stimulation of these afferents. Muscle spindlereceptors, perhaps aided by other deep receptors injoints and tendons and by receptors in the skin, playa significant role in the position sense of limbs andfingers. This sense is critical in the ability to recognizethe form of objects. Afferents that are thin and slowlyconducting relate to the sensations of cold, warm,pain, and crude touch. Other thin afferents are relatedto the sensations of itch and tickle (see Craig, 2002 forreview). This review concentrates on the afferents fromthe skin used in touch and the muscle spindle andskin receptors used in proprioception (kinaesthesia orposition sense).

Low-Threshold Mechanoreceptor Afferentsfrom the Hand

Four types of low-threshold mechanoreceptors arefound in the glabrous skin of primates, and afferentsfrom these four types have been studied electrophysio-logically in humans (Johansson, 1976, 1978; Jarvilehtoet al., 1981; Vallbo, 1981; Johansson et al., 1982;Johansson and Vallbo, 1983; Ochoa and Torebjork,1983; Torebjork et al., 1984; Vallbo et al., 1984; Westlingand Johansson, 1987; Edin and Abbs, 1991; Birzniekset al., 2009). These results, together with psychophysicalinformation on touch from humans, have led to a four-channel model of cutaneous mechanoreception(Bolanowski et al., 1994, 1988). Tactile experience,according to the model, depends on various combina-tions of neural activity in the four channels, with partic-ular channels providing the critical information for somesensations. Stimuli at threshold levels are signaled bythe channel that is most sensitive to these stimuli, but

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suprathreshold sensations are typically the result ofactivity in two or more channels.

The SA-I Afferent or the Non-Pacinian Iii (NP Iii)Channel

In the superficial glabrous skin, the type I class ofslowly adapting afferents (SA-I) is activated at receptorsites termed Merkel disks (see Rice and Albrecht,2008). Each receptor site includes a specialized Merkelcell that is distinct from adjacent skin cells and a numberof disk-like nerve terminals originating from a myelin-ated (7–12 mm diameter) afferent fiber. Merkel cellsappear to be essential for responses to light touch(Maricich et al., 2009). SA-I receptors are densely distrib-uted in the skin of the distal glabrous phalanges of thehuman hand, and they constitute about one-fourth ofthe 17 000 tactile units of the hand (Johansson andVallbo, 1979). Microelectrode recordings indicate thatthe SA-I afferents respond throughout a period ofa skin indentation, even when the indentation is sus-tained for many seconds. Thus, they are slowly adaptingto a maintained stimulus. Depending on the rate of theindentation, a large transient response also occursduring onset. The SA-I fibers have small, circumscribedreceptive fields and seem especially responsive whenthe edge of an object indents skin within the receptivefield. When stimulated by a train of electrical pulses,the single SA-I afferent signals the sensation of light,uniform pressure at a skin location corresponding tothe receptive field. Single electrical impulses are notfelt, and increases in stimulation frequency result in feel-ings of increased pressure. Thus, SA-I afferents arethought to be very important in mediating sensationsof static pressure and providing information about the

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FIGURE 30.3 Changes in the sensitivity to tactile stimuli withdistance across the receptive field for four classes of afferents from theglabrous skin of the human hand. Threshold levels on the verticalscale are arbitrary and do not indicate different thresholds. Therapidly adapting RA-I and the slowly adapting SA-I afferents havesmall receptive fields with sharp boundaries, while Pacinian (PC) orrapidly adapting RA-II and slowly adapting SA-II afferents have largereceptive fields with poorly defined boundaries and a gradual changein sensitivity across the skin. Based on Johansson (1978).

30. SOMATOSENSORY SYSTEM1078

locations of edges and textures of held objects. SA-Iafferents best preserve information about movingBraille-like dot patterns on the skin (Johnson andLamb, 1981). After correlating human discriminationof skin indentation with the response profiles of skinafferents in monkeys, Srinivasan and LaMotte (1987)concluded that static discriminations of shape are basedprimarily on the spatial configuration of the active andthe inactive SA-I afferents. In addition, under staticconditions, the SA-I afferents provide most of the inten-sity information. Form and surface texture perceptionappears to be dominated by the SA-I system (Johnsonand Hsiao, 1992; Hsiao and Bensmaia, 2008).

The RA-I Afferent or the Non-Pacinian I (NPI)Channel

The predominant receptor afferent of the digit skin isthe rapidly adapting RA-I fiber. Nearly half of the tactileafferents from the hand are of the RA-I type (Johanssonand Vallbo, 1983). RA-I afferents innervate Meissnercorpuscles, which are located in dermal papillaeprotruding into the epidermis. Meissner corpuscles areparticularly dense in the glabrous skin of the distalphalanges; they are less common on the palm and arerare in hairy skin, being replaced by RA-I afferentsrelated to hair shafts. The corpuscles consist of a coreof nerve terminal disks and lamellae of Schwann cellssurrounded by connective tissue extensions of the endo-neural sheath. Meissner corpuscles are elongated(100–500 mm) perpendicular to the skin, and the outercollagen fibers of the corpuscles are linked with fibrilsof adjacent epidermal cells, which allow skin deforma-tions to stretch the corpuscle. Most corpuscles are inner-vated by two to six myelinated axons, and each axoninnervates a tight group of corpuscles, providing a smallreceptive field of almost uniform sensitivity and sharpboundaries (Figure 30.3). RA-I afferents respond onlyto changes in skin indentation, and not to steady inden-tation. The RA-I afferents are thought to be responsiblefor the detection of low-frequency vibrations, movementbetween the skin and a surface, and surface texture(Johnson and Hsiao, 1992). They appear to detect micro-scopic slips between manipulated objects and skin toprovide signals for grip control. RA-I afferents arecapable of providing shape information during activetouch (see LaMotte and Srinivasan, 1987). Single electri-cal impulses on RA-I afferents from the human handoften result in the detectable sensation of a light tap ata location corresponding to the receptive field. Low-frequency stimulation produces a sensation of a seriesof taps; at higher frequencies the taps merge into a flut-tering sensation (Macefield et al., 1990). No increase inthe magnitude of the sensation follows increases in stim-ulation rate. These observations suggest that RA-I unitsare especially important in discriminations of textures

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moved across the skin, and of course in the sensation offlutter. Because RA-I afferents are frequently locatednear a joint on the back of the hand, and they respondto skin deformation during finger movements, theymay also have a role in kinesthesia (Edin andAbbs, 1991).

The SA-II Afferent or Non-Pacinian II (NP II)Channel

A second class of slowly adapting afferents, SA-II, arethought to innervate Ruffini-like endings that respondto tension in collagen fibers coursing in the skin. Inhumans, they are especially prevalent around the fingernails where they provide information about stress distri-bution across the finger tips (see Birznieks et al., 2009).Ruffini or Ruffini-like receptors are also found indeep tissues, including joint capsules, ligaments andtendons. Each Ruffini corpuscle contains an elongated(500–1000 mm� 200 mm) capsule of four to five layersof lamellar cells covered with a membrane, and a coreof nerve fiber branches and longitudinally alignedcollagen fibrils. Movement of the skin results instretching of the corpuscle because it is attached tosurrounding tissue. Such stretching results in deforma-tion and activation of the innervating axon. Each Ruffinicorpuscle is innervated by one A-beta myelinated fiber,which may also innervate several other adjacent corpus-cles. In the human hand, the SA-II class of afferents

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RECEPTOR TYPES AND AFFERENT PATHWAYS 1079

constitutes about one-fifth of the tactile units (Johanssonand Vallbo, 1979). SA-II fibers have large, poorly definedreceptive fields (Figure 30.3), often located near the nailbed or near skin folds on the digits or palm. These affer-ents are extremely sensitive to skin stretch, and oftenthey are sensitive to the direction of skin stretch. Normalmovements of digits and limbs are very effective in acti-vating these neurons. Electrical stimulation of single SA-II afferents may not be felt (Macefield et al., 1990), or isreported as producing a buzzing sensation (Bolanowskiet al., 1994), so uncertainty remains about the role of SA-II afferents in tactile perceptions. However, there ispsychophysical evidence that SA-II channels participatein the sense of touch (Bolanowski et al., 1988). In addi-tion, inputs from these skin stretch receptors maycombine with sensory inputs from muscles and jointsto provide limb and digit position and movementsignals (e.g., McCloskey, 1978; Edin and Abbs, 1991).These cutaneous mechanoreceptors appear to contributeto a movement sense but not to an awareness of thestatic-position of a joint (see Clark et al., 1986; Collinset al., 2005). Also, SA-II units are sensitive to skinshearing, and thus they might provide informationabout the weight of objects (McCloskey, 1974). Overall,SA-II afferents seemwell-suited for a role in motor guid-ance and control (Westling and Johansson, 1987). Theywould not be suitable for representing the details ofobjects, such as a Braille pattern (Phillips et al., 1992).

The RA-II Afferent or Pacinian (PC) Channel

Rapidly adapting RA-II afferents innervate Pacinian(PC) corpuscles (Bell et al., 1994). These corpuscles aremuch less common than other receptor endings in theskin of the hand (10–15%), and they are also found indeeper tissues (see Johansson and Vallbo, 1979; Darian-Smith, 1984). Only about 200 corpuscles may be found inthe human finger, where they are distributed withindeeper skin, subcutaneous fat, and tendonous attach-ments of the ventral but not the dorsal parts of the finger.The PC corpuscles are large (0.3–1.5 mm� 0.2–0.7 mm)ovoids consisting of a central nerve fiber surroundedby an inner core of 60 or so layers of concentrically wrap-ped lamellar cells, a space filled with fluid, and an outercapsule of up to 30 less densely packed lamellae. Thecorpuscle acts as a mechanical filter, relaying high-frequency and attenuating low-frequency componentsof skin compression to the axon terminal. The PC affer-ents allow the detection of distant events via the trans-mission of high-frequency vibrations through objectsand surfaces. PC afferents are extremely sensitive totransient indentations of the skin over large areas suchas a complete digit and part of the palm. Thus, informa-tion is transmitted in the tissue to the region of thereceptor. Sensitivity gradually decreases with distancefrom the receptor, and receptive field boundaries are

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not sharp (Figure 30.3). PC units typically can be acti-vated by gently blowing on the skin, and they respondto vibrations produced by tapping the table surface onwhich a skin surface rests. PC afferents, like RA-I fibers,respond to the indentation and release of the skinproduced by a probe (Figure 30.2), but fail to respondduring steady indentation. The responses of Pacinianafferents follow the cycle of a sinusoidal vibratory stim-ulus. However, unlike RA-I afferents that respond withlowest thresholds in the 30–40 Hz range, PC afferentshave lowest thresholds in the 250–350 Hz range. Thus,PC afferents appear to be the only afferents capable ofsubserving the sensation of high-frequency vibration.For most frequencies, PC and RA-I afferents bothcontribute to the perceived vibrotactile intensity(Hollins and Roy, 1996). Electrical stimulation of PCafferents in the human hand are not felt at low stimula-tion rates, but a sensation of vibration or tickle occurs athigh stimulation rates. Often, the sensation is restrictedto a part of the large, diffuse receptive field. PC afferentspoorly resolve moving texture patterns (Johnson andLamb, 1981), and they are apparently unimportant inobject identification. Therefore, their major role seemsto be detecting and roughly locating sudden skin defor-mations produced by ground and air vibrations, and byskin contact.

Cutaneous Receptor Afferents of the HairySkin

As in the glabrous skin, the hairy skin has SA-I, SAII,RA-I, and RA-II afferents. However, some modificationsin the receptor mechanisms exist. First, Merkel celldisks of the SA-I receptor are often aggregated in small(0.25–0.5 mm) diameter touch domes that are slightlyelevated from surrounding skin and can be visualizedwith a dissecting microscope. The Merkel touch spotor Haarscheibe is innervated by a single, large(7–12 mm) myelinated fiber that branches to terminatein a number of disks associated with Merkel cells. Iso-lated Merkel cells are rare. Second, some RA-I andSA-I afferents relate to the shafts of hairs. The SA-I affer-ents seem to be activated by Merkel-type endingsaround hair follicles, and the RA-I afferents may havethe equivalent of Meissner-type endings in glabrousskin. Third, the hairy skin does not have Paciniancorpuscles, but instead relies on a scattering of Paciniancorpuscles located in deep tissue around blood vesselsand muscles (Bolanowski et al., 1994). Thus, hairy skinis less sensitive to vibrations. Fourth, it is not yet clearhow or if the SA-I afferents in hairy skin contribute totactile sensation; in contrast, SA-II afferents maymediate sensations of pressure in hairy skin but not inglabrous skin (Bolanowski et al., 1994). The hairy skin

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30. SOMATOSENSORY SYSTEM1080

of humans also has C-mechanoreceptive afferents (seebelow).

Deep Receptor Afferents

As noted earlier, SA-II type afferents associated withRuffini-like endings are found not only in the skin,where they signal stretch, but also in deep tissues wherethey also signal stretch. The receptors are Ruffini corpus-cles and Golgi tendon organs. Deep SA-II afferentsprovide information about joint extension and tissuecompression. Joint afferents may have a role in theconscious awareness of joint movement (Macefieldet al., 1990). However, joint position sense survivesjoint removal and replacement (Cross and McCloskey,1973).

Other important deep receptors are the musclespindle receptors, which were once thought to partici-pate only in reflexes via spinal cord pathways andmotorcontrol via a relay to the cerebellum. Muscle spindleafferents are now known to also relay to the cortex

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(Figure 30.4), and to contribute to a sense of postureand movement (Goodwin et al., 1971; McCloskey, 1978;Burgess et al., 1982; Clark et al., 1986; Jones, 1994). Forstatic limb position, Clark et al. (1986), proposed thatthe nervous system computes joint angles and thuslimb position from muscle spindle information aboutthe lengths of the muscles that set the positions of joints.Muscle spindle afferents are activated when the musclesrelax due to the lengthening of the muscle whilemuscle contractions activate tendon afferents. Microsti-mulation of muscle spindle afferents rarely producesa perception of movement or joint position (Macefieldet al., 1990).

C-Fiber and A-delta Afferents MediatingTemperature, Itch, Pain, and Touch

Other afferents in the skin and deeper tissues relate tothe sensations of temperature, pain, itch, and crudetouch. These include several types of mechano-heatnociceptors, cold nociceptors, polymodal nociceptors

FIGURE 30.4 A more detailed overview of the basiccomponents of the human somatosensory system. Inputsfrom the four main classes of cutaneous receptors (seeFigure 30.2) enter the spinal cord branch and terminateon neurons in the dorsal brain of the spinal cord and inthe ipsilateral dorsal column nuclei of the lower brain-stem. Muscle spindle afferents branch in a similarmanner with the ascending branch coursing in the dorsalcolumns or more laterally to terminate in the gracile andcuneate subnuclei as well as the external cuneatenucleus. Other more slowly conducting afferents relatedto pain, touch, and temperature terminate on dorsal hornneurons that project contralaterally to form the spino-thalamic pathway. Afferents from the face enter thebrainstem to terminate in the principal trigeminal nucleifor cutaneous and muscle spindle afferents and thespinal trigeminal nuclei for pain, temperature, and touchafferents. The gracile nucleus represents the hindlimband lower body; the cuneate nucleus, the forelimb; andthe principal trigeminal nucleus, the face for cutaneousinputs. These inputs activate second-order neurons thatproject via the medial lemniscus to the contralateralthalamus. Nuclei in the thalamus include the ven-troposterior (VP) nucleus with ventroposterior medial(VPM) and ventroposterior lateral (VPL) subnuclei forthe face and body representations, respectively. Thecutaneous afferents from the foot, hand, and face arerepresented in a lateromedial sequence in VP. The ven-troposterior superior (VPS) nucleus represents musclespinal inputs in a similar somatotopic order, while theventroposterior inferior nucleus receives spinothalamicaxons. These nuclei project to subdivisions of anteriorparietal and lateral parietal cortex (see text). The secondsomatosensory area (S2), the parietal ventral area (PV),the parietal rostral area (PR) and caudal and rostraldivisions of the ventral somatosensory (VS) complex areindicated. Brodmann’s areas are numbered.

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RECEPTOR TYPES AND AFFERENT PATHWAYS 1081

(Mense, 2008) responsive to heat, pinch, and cooling(HPC), and the wide-dynamic range (WDR) afferents(Chapter 32; Willis and Coggeshall, 1991). Specific noci-ceptors conduct in the A-delta range and mediate prick-ing pain, while the multi-modal afferents conduct in theC range and mediate burning pain. A specific receptorand a C-fiber pathway for itch appears likely (Sunet al., 2009). Warm receptor afferents conduct in the Crange while responding at body temperatures andhigher, but not at noxious levels of heat.

One class of unmyelinated afferents from the skin(C-tactile) respond well to slow stroking of the hairyskin (Olausson et al., 2002, 2008; Bjornsdotter et al.,2009). Observations on a patient who lacks large myelin-ated afferents while having C-afferents intact indicatethat the C-tactile afferents allow a soft brush stimulusto be detected and localized to a body quadrant. Theseafferents are thought to signal pleasant touch, and servean affiliative function in social body contact. These andother slowly conducting afferents synapse on neuronsin the dorsal horn of the spinal cord that project contral-aterally to form the spinothalamic pathway.

Afferent Pathways

Afferents course from skin receptor and deepreceptor locations to combine in nerve fascicles thatjoin other fascicles to form the peripheral nerves. Theperipheral nerves branch and segregate into dorsalsensory roots and ventral motor–sensory roots. Theafferents that enter the dorsal roots terminate onneurons in the dorsal horn of the spinal cord. Onebranch of these afferents may ascend to terminate onneurons in the dorsal column nuclear complex at thejunction of the medulla and spinal cord (Figure 30.1;Chapters 7 and 8).

A number of investigators have attempted to deter-mine the skin regions subserved by the nerves in eachspinal root in humans and other mammals (see Dykesand Terzis, 1981 for review). Dissections have beenused to reveal the gross patterns of these dermatomaldistributions, but additional methods include usingthe zone of remaining sensibility after section of dorsalroots above and below the one studied, electricalrecording or stimulation, interruptions of functionproduced by ruptured disks, and data from herpes zos-ter eruptions. For humans, the extensive dermatomalmaps are those of Head (1920), based on skin regionsaffected by herpes zoster; Foerster (1933), from clinicalcases where spinal roots were sectioned for the reliefof pain; and Keegan (1943), from cases of local sensoryloss subsequent to ruptures of intervertebral disks.Dykes and Terzis (1981) point out that these threemaps of dermatomes differ considerably, and theysuggest that none is accurate. However, the maps in

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humans, together with the results from other primates,allow several conclusions: (1) the field of each root iscontinuous, and tends to form a strip perpendicular tothe spinal cord; (2) adjacent dorsal root distributionsoverlap extensively; (3) there is little overlap at theventral and dorsal body midlines; (4) there is consider-able variability across individuals.

Within dorsal roots, studies in monkeys indicate thatthere is some crude organization of afferent fibersaccording to skin location, with distal receptive fieldslocated caudal in the dorsal root, while fibers with prox-imal receptive fields tend to be rostral (Werner andWhitsel, 1967). These studies also indicate thatascending branches of axons entering the spinal cordin the dorsal columns (Figure 30.4) tend to preserve theirorder of entry so that axons from lower spinal roots aremedial to those from upper spinal roots (Whitsel et al.,1972). In monkeys, inputs from muscle spindles branchand join the cuneate fasciculus for the upper limb, butterminate in the spinal cord for the lower limb. Someafferent fibers with cell bodies in the dorsal root gangliaturn and enter the ventral root and then turn and retracea path back to the dorsal root, as if correcting an error(see Willis, 1985). These sensory fibers in the ventralroot are largely unmyelinated axons, and many arenociceptors.

Terminations of Peripheral Nerve Afferents inthe Spinal Cord and Brainstem

Afferent fibers entering the spinal cord either simplyterminate on neurons in the dorsal horn of the spinalcord or branch and send a collateral toward the brain-stem to terminate either in the dorsal horn at higherlevels or in the dorsal column–trigeminal nuclearcomplex of the lower brainstem. Figure 30.4 depictssensory terminations in the spinal cord and relays tothe medulla–spinal cord junction. Termination patternsof peripheral afferents have been investigated inmonkeys and other mammals (see Chapter 7), andsome rather consistent features can be assumed to applyto humans. First, the axons of specific types of afferentshave different characteristic termination patterns in thedorsal horn of the spinal cord. Second, afferents fromdifferent skin regions terminate to form a somatotopicmap in the spinal cord. Third, afferents ascending tothe dorsal column nuclei terminate somatotopically.

The termination patterns of individual axons thathave been physiologically identified and labeled withhorseradish peroxidase are known from studies oncats (see Brown, 1981). All four types of cutaneous affer-ents bifurcate as they enter the cord to send rostral andcaudal branches that further branch to form a sagittallyarranged series of terminal arbors in the dorsal horn.Individual RA-I collaterals form a separate arbor of

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about 500 mm in the sagittal plane and 50–300 mm in thetransverse plane in layers III and IV. Collaterals of PC orRA-II axons terminate in several sagittally elongatedarbors (400–750 mm) that extend vertically from layersIII and IV to layers V and VI. SA-I axon collaterals giverise to spherical arbors (250–700 mm) that distribute inlayers II, III, IV, and the dorsal margin of V. SA-II axoncollaterals terminate over layers III, IV, V, and part ofVI in rostrocaudally thin sheets (100–300 mm). While alltypes differ in the details of distribution, the results indi-cate that inputs from single receptive fields on the skinrelate to rostrocaudal rows of cells in the dorsal horn.How axons from specific skin regions terminate in thespinal cord is known for a range of mammals, includingmonkeys. Similarities across species suggest that thetermination pattern in humans is similar. Figure 30.5shows that the terminations from the skin of the digitsof the hand are arranged in a rostrocaudal row in themedial dorsal horn of the cervical spinal cord ofmacaque monkeys (see Florence et al., 1988, 1989).More proximal parts of the limb are represented morelaterally in the dorsal horn, and inputs from the footdemonstrate a similarly orderly arrangement. As forthe single axons, groups of axons from a limited skin

FIGURE 30.5 A section of the cervical spinal cord in a macaquemonkey (A). The rapidly conducting cutaneous afferents of peripheralnerves terminate in a somatotopic pattern in the dorsal horn of thespinal cord (B). Tracers were injected into the glabrous skin of digits 1,3, and 5 (D1, D3, D5). Although afferents from each digit typicallyenter the spinal cord over more than one cervical dorsal root (C5, 6, 7,and 8), the inputs terminate in an orderly pattern. Inputs from D1, D2,and D5 terminate in a rostrocaudal pattern (white) in the medialdorsal horn (black) with other digit inputs in between. The dorsalhand and palm are represented more laterally, and the forearm, inrostral and caudal bands. Based on Florence et al. (1988, 1989). The boxin (A) indicates the plane illustrated in (B).

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region terminate in rostrocaudally elongated zones.Thus, body parts are represented in rostrocaudal slabsof cells. While different classes of afferents activatedifferent groups of spinal cord cells, the single zonesof label for each digit indicate that the dorsal horn cellsactivated from a given skin region are grouped together.

Ascending Spinal Cord Pathways

Traditionally, the ascending somatosensory pathwaysfrom the spinal cord include the dorsal column pathwayand a ventrolateral pathway (Figure 30.4). The dorsalcolumn pathway includes the axons of first-order dorsalroot ganglion neurons coursing ipsilaterally to thedorsal column nuclei. The ventrolateral pathway (seebelow) originates from second-order neurons of thedorsal horn, crosses to the opposite ventrolateral whitematter of the spinal cord, and ascends to brainstemand thalamic targets, including the ventroposterior infe-rior nucleus of the thalamus. The ipsilateral dorsalcolumn system is thought to largely deal with epicriticfunctions such as position sense and light touch,while the crossed spinothalamic system is thought tomediate protopathic sensibilities of crude touch, pain,and temperature. More recent research has complicatedthis story by indicating that (1) second-order neuronsalso contribute to the ipsilateral dorsal columns; (2)additional ipsilateral pathways from second-orderneurons exist, including a spinocervical system that isreduced in primates; (3) pathways from the upper andlower limbs differ; (4) crossed spinothalamic pathwaysvary in location; and (5) descending axons are mixedwith ascending axons. Of course, these conclusions arebased on anatomical studies in non-human primatesand other mammals, but findings are general enoughthat they are likely to apply to humans.

The Dorsal (Posterior) Column System

The extremely large dorsal column afferent pathwayin humans occupies over a third of the spinal cord athigh cervical levels (Wall, 1970). The twomajor divisionsare the more medial gracile tract subserving the trunkand lower limb and the cuneate tract for the upperlimb and associated trunk and neck. Inputs from theface and head via the trigeminal system form an analo-gous tract in the brainstem (see Chapter 31). The axonsin the dorsal columns are large, myelinated dorsal rootfibers that branch to ascend to the dorsal column nuclei,send descending collaterals for several segments in thedorsal columns, and emit a number of local collateralsto terminate on neurons in the dorsal horn. Other axonsoriginate from spinal cord neurons and ascend overseveral segments to terminate in the spinal cord on localcircuit neurons or on neurons that project to the

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brainstem. Some of these secondary sensory neuronsproject via the dorsal columns to the dorsal columnnuclei. Thus, both first- and higher-order axons are foundin the dorsal column pathway (Rustioni et al., 1979;Cliffer and Willis, 1994; Al-Chaer et al., 1999). A fewdescending fibers may also travel in the dorsal columns.Entering fibers from each dorsal root form a narrowlayer at the lateral margin of fibers from lower levels,but some mixing of levels occurs as the axons ascend.

Most of what is known about the types of informationconveyed by the dorsal columns comes from microelec-trode recordings in monkeys (Whitsel et al., 1969),although limited recordings in humans revealed nervefibers activated by pressure and limb movement (Pulettiand Blomquist, 1967). The gracile and cuneate tractsdiffer at high spinal cord levels in the classes of axonsthey contain. The gracile tract at lower levels containsa mixture of cutaneous afferents, largely rapidly adapt-ing afferents (probably RA-I), and muscle afferentsthat leave to terminate in Clarke’s nucleus, whichprojects in turn to the cerebellum and other structuresvia the dorsal spinocerebellar tract. At higher levels,the remaining axons that travel to nucleus gracilis arealmost completely RA cutaneous afferents. The cuneatetract contains a mixture of RA cutaneous and muscleafferents, but the cutaneous inputs terminate in thecuneate nucleus, and the muscle afferents separate toinnervate the external cuneate nucleus. Thus, lesions ofthe dorsal columns deactivate RA neurons, regardless ofthe level of the lesion, but muscle afferents from thelower body terminate on neurons that project outsideof the gracile tract. Presumably, the dorsal columns ofmonkeys and humans also contain SA-I, SA-II, and PCafferents, as in other mammals (see Willis and Cogge-shall, 1991).

Lesions of the dorsal columns in humans have littleeffect on many simple tactile abilities, but major defectsoccur in the abilities to detect the speed and direction ofmoving stimuli and to identify figures drawn on the skin(Nathan et al., 1986; see Mountcastle, 1975, andWall andNoordenhos, 1977, for reviews). These changes obvi-ously can be attributed to the loss of inputs from RAcutaneous afferents. Other defects in the control of fore-limb movements (Beck, 1976) may relate to disruption ofproprioceptive afferents. The sensory changes followingdorsal column lesions in monkeys are similar, wherethey have been extensively studied (see Vierck andCooper, 1998; Mountcastle, 2005, for review). Disrup-tions occur in the ability to discriminate the frequencyof stimulation, the spatiotemporal sequence of tactilestimuli, the directions of moving stimuli and changesin texture. The results of such lesion studies should beinterpreted with caution as a small number of afferentssurviving a lesion can mediate the recovery of lost abil-ities (Darian-Smith and Ciferri, 2005).

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The dorsal columns apparently carry all of the inputsfrom the body that activate anterior parietal cortex. Aftercomplete lesions of the dorsal columns at a high cervicallevel in monkeys, neurons throughout the forelimb andadjacent trunk representations in areas 3a, 3b, l, and 2totally fail to respond to somatosensory stimuli (Jainet al., 1997, 2008). Given the distribution of informationfrom anterior parietal cortex to areas of posterior pari-etal and lateral parietal cortex (Figure 30.4), the impacton somatosensory processing at the cortical level ismajor. However, the effects of dorsal column lesionson behavior have been difficult to study because thesomatosensory system of adult primates has a greatcapacity for plasticity, and the survival of only a fewdorsal column axons can have a substantial impact oncortical neurons (Jain et al., 1997, 2008). As expected,humans (Nathan et al., 1986) and monkeys (e.g., Vierckand Cooper, 1998) with dorsal column lesions at thelevel of the cervical spinal cord are greatly impaired inforelimb and hand use compared to leg and foot use,because some of the proprioceptive afferents from theleg travel outside the dorsal columns. The somatosen-sory abilities that remain demonstrate the importanceof the spinal cord connections and other ascending path-ways, especially the spinothalamic pathway, althoughthe role of the spinothalamic pathway in touch seemslimited (Bjornsdotter et al., 2009).

Primary afferents from oral and facial structurestravel in the trigeminal (fifth) nerve and enter the brain-stem to branch and terminate in the principal trigeminalnucleus and subdivisions of the spinal trigeminalcomplex (May and Porter, 1998; see Chapter 31). Theaxon branches terminating in the principal nucleus arelargely of the low-threshold SA and RA classes, andthey constitute the equivalent of the dorsal columnpathway. Terminations in the subdivisions of the spinaltrigeminal complex correspond to those from the bodythat terminate in the dorsal horn of the spinal cord.

Second-Order Axons of the Dorsolateral SpinalCord (The Spinomedullothalamic System)

In monkeys, all the muscle afferents for the lowerbody apparently leave the gracile column and synapseon neurons that send axons in the dorsolateral (postero-lateral) spinal cord to the dorsal column nuclearcomplex (Whitsel et al., 1972). In humans, lesions ofboth the dorsal columns and the dorsolateral spinalcord result in severe defects in proprioception, but it isnot certain that all proprioceptive axons from the lowerlimbs are in the dorsolateral pathway rather than thedorsal column pathway (Nathan et al., 1986).

Many or all mammals have other inputs to the dorso-lateral pathway, including a spinocervical pathway fromsecond-order neurons in the dorsal horn that project

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ipsilaterally to the lateral cervical nucleus. A compara-tively reduced lateral cervical nucleus has beendescribed for humans (Truex et al., 1970), but the typesof inputs activating this nucleus are known only fromstudies on other mammals, particularly cats (see Willisand Coggeshall, 1991, for review). Neurons projectinginto the spinocervical tract have receptive fields onboth the hairy and glabrous skin in monkeys (Bryanet al., 1974). Peripheral inputs activating these neuronsare cutaneous rapidly adapting afferents, and there isan apparent lack of slowly adapting cutaneous anddeep receptor influences.

The Spinothalamic Pathways

Many second-order somatosensory neurons in thedorsal horn of the spinal cord have axons that cross inthe spinal cord to ascend in the ventrolateral or dorsolat-eral white matter. Many axons in these pathways termi-nate before reaching the thalamus, but others branch toreach several thalamic nuclei. In Old World monkeys,a dorsolateral spinothalamic tract consists of locallycrossing axons of lamina I cells of the dorsal horn, whilethe ventrolateral spinothalamic tract contains locallycrossing axons of laminae I-X cells (Apkarian andHodge, 1989a). In monkeys, spinothalamic tract neuronshave been found to respond to tactile stimuli and move-ment of hairs, stimuli ranging from tactile to noxious(wide dynamic range neurons), noxious stimuli, andtemperature (see Willis and Coggeshall, 1991; Craig,2003). In humans, some capacity for mechanoreceptivesensibility remains after large lesions of other ascendingpathways (Bjornsdotter et al., 2009). Electrical stimula-tion of the ventral quadrants of the spinal cord hasproduced sensations of pain and temperature (Sweetet al., 1950; Tasker et al., 1976).

RELAY NUCLEI OF THE MEDULLA ANDUPPER SPINAL CORD

Several groups of neurons in the spinal cord andmedulla are important in relaying information to higherbrain centers. These include the dorsal column nuclearcomplex, the dorsal nucleus of the spinal cord (Clarke’snucleus or column), and the lateral cervical nucleus. Thetrigeminal nuclear complex adds analogous pathwaysfor information from the head.

Dorsal Column–Trigeminal Nuclear Complex

The dorsal column–trigeminal nuclear complexconsists of groups of cells in the lower brainstem andupper spinal cord that receive inputs from ipsilaterallow-threshold mechanoreceptors and project to the

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ventroposterior complex of the thalamus (Figure 30.4).The part of the system originating in dorsal root gangliaand coursing in the dorsal columns terminates in thegracile nucleus for the lower body and the cuneatenucleus for the upper body. The trigeminal complexreceives inputs from cutaneous mechanoreceptors inthe face and mouth. The gracile, cuneate, and trigeminal“nuclei” form a somatotopic map from hindlimb to headin a mediolateral sequence in the lower medulla (Xu andWall, 1996, 1999). The gracile and cuneate nuclei areelongated in the rostrocaudal dimension (Figure 30.4).The overall appearance of the nuclei in humans (seeChapter 8) is quite similar to that observed in macaquemonkeys and other primates (Florence et al., 1988, 1989;Strata et al., 2003; Qi and Kaas, 2006). In both, the middleregions contain discrete clusters of neurons outlined bymyelinated fibers. Stains for the mitochondrial enzymecytochrome oxidase (CO) show that the cell clustershave more of the enzyme and, presumably, higher meta-bolic activity than the surrounding fiber regions. Thedetails of the parcellation pattern of these nuclei inhumans and monkeys are quite comparable (Florenceet al., 1989), suggesting the significance of the parcella-tion is the same. Afferents from individual digits andother body parts terminate in specific cell clusters, andthus, the parcellation reflects the somatotopic organiza-tion of the gracile and cuneate nuclei. The rostral andcaudal poles of the cuneate nucleus have more conver-gent terminations from afferents of the digits. Thus,the nucleus appears to segregate inputs into a discretesomatotopic map in the central part of the nucleus andinto less precise maps in the rostral and the caudal polesof the nucleus in monkeys, and probably in humans.

The projection neurons of the dorsal column nucleisend axons into the contralateral medial lemniscus,where they course to the ventroposterior complex (seeKaas, 2008). In humans, as in other mammals, someaxons probably send collaterals to the inferior olive,which projects to the cerebellum (see Schroeder andJane, 1976; Molinari et al., 1996). In monkeys and othermammals, the dorsal column nuclei, especially therostral poles, receive inputs from the contralateralsomatosensory and motor cortex (areas 4, 3a, 3b, l,and 2) that may modulate the relay of sensory informa-tion (e.g., Cheema et al., 1985; Bentivoglio and Rustioni,1986; see Marino et al., 1999, for a review).

The trigeminal complex includes the principal (Pr 5)or main sensory nucleus and three spinal trigeminalsub-nuclei (Chapter 31). The principal nucleus isthought to be analogous to the cuneate and gracilenuclei, and the three together form a systematic repre-sentation of cutaneous receptors of the body (Noriegaand Wall, 1991; Xu and Wall, 1996). The principalnucleus projects via the medial lemniscus to themedial subnucleus of the contralateral ventroposterior

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complex (VPM). The spinal trigeminal sub-nuclei (Sp 5)correspond to part of the dorsal horn of the spinal cord.As in the spinal cord, a marginal zone receives pain andtemperature afferents (Craig et al., 1999) and deeperneurons are activated by cutaneous other afferents(e.g., Price et al., 1976). Second-order neurons in thespinal trigeminal nucleus form a relay that joins thecontralateral spinothalamic tract to terminate in theventroposterior inferior nucleus and other nuclei (seeBurton and Craig, 1979). The mesencephalic trigeminalnucleus consists of the cell bodies of peripheral nerveafferents subserving proprioception. They relay to Pr5.

Lateral Cervical Nucleus, Nuclei X and Z,External Cuneate Nucleus, and Clarke’sColumn

Second- and third-order relay neurons are found inseveral structures in addition to the dorsal column–trigeminal complex and the dorsal horn of the spinalcord (for the human brainstem, see Paxinos and Huang,1995; Chapter 8).

Lateral Cervical Nucleus

The lateral cervical nucleus consists of a longcolumn of neurons outside the gray matter proper ofthe dorsal horn of the spinal cord that extends fromC4 to the caudal part of the medulla. Rapidly adaptingafferent fibers serving hairs and other tactile afferentsenter the dorsal horn to relay on neurons forming thespinocervical tract in the dorsolateral white matter.These second-order neurons terminate on neurons inthe ipsilateral lateral cervical nucleus. A subset ofmultimodal neurons with a convergence of nociceptiveafferent inputs has been reported in the lateral cervicalnucleus as well (see Boivie, 1978, for a review). Thelateral cervical nucleus appears to relay touch, pres-sure, and vibration information, largely from the hairyskin, to the contralateral thalamus, inferior olive, andmidbrain. In humans, the lateral cervical nucleus maybe a rudimentary structure because it is only welldefined in some individuals (Truex et al., 1970). Insuch humans, the nucleus contains up to 4000 neurons,while nearly double that number may exist in cats(Boivie, 1983).

Nuclei X and Z

Other second-order axons of the dorsolateral fascic-ulus, possibly collaterals of spinocerebellar axons, termi-nate in two small medullary nuclei, termed X and Z byPompeiano and Brodal (1957). Muscle spindle afferentsfor the hindlimb relay via the dorsolateral fasciculus tonucleus Z, located just rostral to the gracile nucleus.Nucleus Z, which has been identified in the human

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brainstem (Sadjadpour and Brodal, 1968; see Chapter 8),projects to the contralateral ventroposterior complex inthe thalamus. In monkeys, muscle spindle receptor affer-ents related to the forelimb relay over neurons projectingwithin the dorsal columns (Dreyer et al., 1974). This prob-ably also occurs in humans, since lesions of the dorsalcolumns impair motor control for the upper limbs(Nathan et al., 1986). A separate nucleus X, not clearlypresent in humans, forms a second group of neuronsreceiving mostly second-order muscle spindle afferentsrelated to the lower limbs.

External Cuneate Nucleus

The muscle spindle afferents of the upper limbs andbody course in the cuneate fasciculus to terminate inthe external cuneate nucleus (Hummelsheim et al.,1985). Like nucleus X, the external cuneate nucleusrelays to the contralateral ventroposterior complex ofthe thalamus, and to the cerebellum.

Clarke’s Nucleus or Column

A long column of cells called Clarke’s column islocated just dorsolateral to the central canal in themedial part of the spinal cord of T1–L4 levels. Inputsare largely from muscle spindles. Clarke’s columnprojects to nucleus Z and, via the dorsal spinocerebellartract, to the cerebellum (for reviews, see Mann, 1973;Willis and Coggeshall, 1991).

SOMATOSENSORY REGIONS OF THEMIDBRAIN

Studies in non-human mammals implicate severalmidbrain structures in somatosensory functions, butevidence for similar roles in humans is presently lack-ing. Thus, neurons in the external nucleus of the inferiorcolliculus respond to somatosensory stimuli and receiveinputs from the dorsal column nuclei. The pericentralnucleus may have spinal cord inputs as well. Schroederand Jane (1976) speculate that auditory and somatosen-sory systems interrelate in these structures in the detec-tion of low-frequency vibratory stimuli. In addition, thedeeper layers of the superior colliculus contain neuronsactivated by somatosensory stimuli via inputs from thespinal trigeminal nucleus, the spinal cord, the lateralcervical nucleus, and the dorsal column nuclei (seeHuerta and Harting, 1984, for a review). The somatosen-sory inputs form a representation that is matched ingeneral spatial location with visual and auditory maps,and the presumed role of the matched maps is to func-tion together in directing eye and head movementstoward sounds, touches, and images of interest (seeStein et al., 2004).

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SOMATOSENSORY THALAMUS

Various proposals have been made for how to subdi-vide the human thalamus (see Chapter 19), as thalamicstructures related to somatosensory abilities have beengiven various names or have not been identified withcomplete certainty. In macaques and several families ofNew World monkeys, where considerable experimentalevidence is available (e.g., Krubitzer and Kaas, 1992), wesubdivided the somatosensory thalamus into a largeventroposterior nucleus, a ventroposterior superiornucleus (VPS), and a ventroposterior inferior nucleus(Figure 30.4; see Kaas, 2008 for review). The VP is theprincipal relay of information from rapidly adaptingand slowly adapting cutaneous receptors to anteriorparietal cortex, the VPS relays information from deepreceptors in muscle and joints, while the significanceof the VPI with spinothalamic inputs is less certain.Just caudal to VPI, a ventromedial posterior nucleusappears to receive spinothalamic inputs mediatingpain and temperature (Craig et al., 1994). In addition,related nuclei of the posterior complex (Po) appear tohave somatosensory functions. Other nuclei, notablythe medial and anterior divisions of the pulvinarcomplex and the lateral posterior nucleus, are knownto have connections with parietal cortex and therebyare implicated in somatosensory functions. However,these nuclei do not appear to have a role in relayingsensory information. The somatosensory nuclei are dis-cussed and related to proposed subdivisions of thehuman thalamus below.

Ventroposterior Nucleus (VP)

The VP is a basic subdivision of the mammalian thal-amus (Welker, 1974; Jones, 2007; Kaas, 2008) that is char-acterized by (1) densely packed and darkly stainedneurons; (2) a systematic representation of cutaneousreceptors; (3) inputs from the dorsal column nuclei, thespinothalamic tract, and the trigeminal system; and (4)projections to “primary” somatosensory cortex. Thenucleus has subnuclei of dense aggregates of neuronspartially separated by cell-poor fiber bands, the mostconspicuous of which is the arcuate lamina that separatesthe part of VP representing the face, the ventroposteriormedial “nucleus” (VPM), from the portion representingthe rest of the body, the ventroposterior lateral “nucleus”(VPL). Another notable fiber band separates the repre-sentations of the hand and foot in VPL.

In macaque monkeys, the dorsal boundaries of VP arenot very distinct from the region we now identify as VPS(see Paxinos et al., 2000). The VP of some investigatorsincludes VPS, although this region has also been distin-guished as the VP “shell” (Jones, 2007). Olszewski’s(1952) popular atlas of the thalamus of macaque

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monkeys includes additional parts of the thalamusrelated to motor cortex within an oral division of VPL(VPLo). This use of terminology is not consistent withthat used in other mammals.

In the human thalamus, the region identified as the“ventrocaudalis group” or Vc (see Chapter 19) corre-sponds closely to our VP in monkeys. Using the termi-nology of Hassler (1982), VPL is Vce (the externalsegment) and VPM is Vci (the internal segment of Vc).VP is composed of a range of neuron sizes that generallystain densely for Nissl substance. The dorsal border ofthe nucleus is described as indistinct, but medial borderswith the anterior pulvinar and ventral borders with theVPI are distinct. Recent atlases of the human brain usethe terms VPL and VPM (Mai et al., 1997; Morel et al.,1997).

The VP contains a systematic representation of cuta-neous receptors. Each location on the body surface acti-vates a small volume of tissue or cluster of neurons inVP, and these clusters of neurons are arranged to forma somatotopic representation. The general form of thesomatotopic organization in mammals has beenreviewed by Welker (1974), and described in detail forsquirrel monkeys by Kaas et al. (1984) (Figure 30.6; seeRausell and Jones, 1991; Padberg et al., 2009 for VP ofmacaque monkeys). In all primates, including humans,we expect the tactile receptors of the tongue, teeth, andoral cavity to be represented medial to the lips andupper face in VPM. Because some of the inputs fromthe principal trigeminal nucleus are ipsilateral as wellas contralateral, both the ipsilateral and contralateralteeth and tongue are represented in each VPM. Moremedially, a gustatory nucleus, VPM parvocellular(VPMpc), is part of the system for taste (see Chapter 33).The medial portion of VPL contains a mediolateralsequential representation of the digits of the hand fromthumb to little finger. The lateral portion of VPL isdevoted to the foot, while dorsal portions of the nucleusrelate to the proximal leg, the trunk, and the proximalarm in a lateromedial sequence. This arrangement,found in monkeys and in other mammals, is basicallythe order described for the human VP. Recordingsand electrical stimulation with microelectrodes in VPof the human thalamus (Emmers and Tasker, 1975;Lenz et al., 1988; Davis et al., 1996; Patel et al., 2006)indicate that the mouth and tongue relate to ventrome-dial portions of VPM, the hand and foot are inventrorostral VPL, and the back and neck are in dorso-caudal VPL. Furthermore, the fingers activate a largeportion of medial VPL and the lips and tongue relateto a large part of VPM. In addition, often groups ofneurons extending in the parasagittal plane areactivated by the same restricted skin surface, indicatingthat lines of isorepresentation are largely in the para-sagittal direction.

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FIGURE 30.6 The somatotopic organizationof the ventroposterior (VP) nucleus of squirrelmonkeys. A similar organization, except fora lateral representation of the tail, exists in VP ofhumans (Lenz et al., 1988). VP is subdivided intoventroposterior lateral (VPL) for the body andventroposterior medial (VPM) for the face. VPLhas further subnuclei for the hand and foot. Thehand subnucleus is shaded. Digits of the handand foot are represented in mediolateralsequences with the tips ventral in VP. Neurons inVP are activated by slowly and rapidly adaptingafferents. Neurons activated by each class formsmall clusters with VP. Adapted from Kaas et al.(1984).

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As in monkeys (e.g., Dykes et al., 1981), most neuronsin VP of humans are activated by RA-I or SA inputs,with local clusters of cells related to one or the otherclass of inputs (Lenz et al., 1988). Thus, there are twofragmented, intermixed representations of the skin inVP, one fragmented representation of RA-I afferentsand one fragmented representation of SA afferents.The SA inputs could be SA-I or both SA-I and SA-II.There is little evidence for Pacinian (RA-II) inputs, butthey likely add to the complexity of the nucleus. A fewneurons respond with an increasing frequency as lighttactile stimuli become more intense and extend intothe painful range (the wide-dynamic-range neurons);these neurons may have a role in pain perception (seeKenshalo et al., 1980) or in signaling the intensity ofstimuli. In humans, electrical stimulation of peripheralnerves results in evoked potentials in the contralateralVP with a latency of 14–17ms (Fukushima et al., 1976;Celesia, 1979). Electrical stimulation at sites in VP or ofinput fibers in the medial lemniscus generally resultsin sharply localized sensations of numbness or tingling(paresthesia) rather than light touch (Tasker et al.,1972; Emmers and Tasker, 1975; Davis et al., 1996; Lenzet al., 1998, 1988; Patel et al., 2006). However, sensationsof touch and vibration are also reported (Ohara et al.,2004). Localized lesions of VP are followed by a persis-tent numbness in a restricted skin region correspondingto the body surface map in VP (Garcin and LaPresle,1960; Domino et al., 1965; Van Buren et al., 1976).

The sources of ascending inputs to VP (Figure 30.4)have been studied in many mammals, includingmacaque monkeys. The dense inputs are from the dorsalcolumn nuclei via the medial lemniscus and the main

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sensory trigeminal nucleus via the trigeminal lemniscus.Less-dense, unevenly distributed inputs are from thespinothalamic tract and the lateral cervical nucleus(Berkley, 1980; Apkarian and Hodge, 1989b; Craig,2006). The spinothalamic inputs appear to relate tosmall-cell regions of VP that express calbindin (possiblyextensions of VPI) that project to superficial layers ofareas 3b and 1 (Rausell and Jones, 1991). Thus, this relaylikely has a modulatory role in somatosensory cortex. Inhumans, degenerating spinothalamic terminations havebeen reported in VP after spinal cord damage (Mehler,1966; see Bowsher, 1957, for a review of classical reports)and, evoked potentials have been recorded in VP afterelectrical stimulation of the dorsal columns (Gildenbergand Murthy, 1980).

The outputs of the ventroposterior nucleus have beenstudied extensively in primates and other mammals (seeKaas and Pons, 1988; Darian-Smith et al., 1990; Krubitzerand Kaas, 1992; Kaas, 2008; Padberg et al., 2009). In allmammals studied, VP projects to area 3b or its non-primate homolog S1. In most mammals, other projec-tions are to the second somatosensory area (S2) andpossibly other fields, but in monkeys, and probablyhumans, projections to S2 are a trivial component ofthe output. In monkeys, VP also projects over thinneraxons and in a less-dense manner to area 1, and, inmacaque monkeys, a sparse input exists to part of area2 related to the hand and even a specialized part ofarea 5 (Pons and Kaas, 1986; Padberg et al., 2009). Inhumans, lesions of anterior parietal cortex includingareas 3b and 1 cause retrograde degeneration and cellloss in VP (Van Buren and Borke, 1972), supporting theconclusion that the output patterns in humans and

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monkeys are similar. Furthermore, recordings from thesurface of somatosensory cortex indicate that potentialsevoked by median nerve stimulation are reduced orabolished by lesions of VP (Domino et al., 1965).

Ventroposterior Superior Nucleus

There has been long-standing recognition that inputsfrom receptors in deep tissues are at least partially segre-gated from inputs from cutaneous receptors in theventroposterior thalamus of primates (see Poggio andMountcastle, 1963) and perhaps other mammals. Thezone of activation by deep receptors is dorsal to thatrelated to cutaneous receptors in monkeys, and thedeep receptor zone is further distinguished by itspattern of cortical connections and architecture. Wehave termed the deep receptor zone the ventroposteriorsuperior nucleus (VPS; see Kaas and Pons, 1988; Kaas,2008). Early investigators included the zone of activationby deep receptors in VP, and several recent researcherssimply designate the deep receptor zone as the VP“shell.” Others conclude that the deep receptor zoneincludes two nuclei, a VPS and a “ventroposteriororal” nucleus (see Dykes, 1983), but the evidence forsuch a subdivision in primates is inconclusive. Someterm the VPS region VPO (see Chapter 19) as it is asmuch oral (anterior) as superior in some primates.Finally, the medial posterior nucleus of some investiga-tors (see Krubitzer and Kaas, 1987, for a review) maybe a non-primate homolog of VPS.

In monkeys, VPS contains a representation of deepreceptors for proprioception, principally muscle spindlereceptors (see Wiesendanger and Miles, 1982; Kaas andPons, 1988). The representation parallels that in VP sothat the face, hand, and foot activate the medial, middle,and lateral portions of VPS in sequence (Kaas et al.,1984). The major input appears to be from the externalcuneate nucleus (Boivie and Boman, 1981), and theoutput is largely to area 3a, area 2, and part of area 5(Padberg et al., 2009). Many of the same neurons inVPS appear to project to both area 3a and area 2 viacollaterals (Cusick et al., 1985).

Evidence is less complete for VPS of humans. Deepreceptors are represented in an orderly manner in partof the thalamus just rostrodorsal to the cutaneous repre-sentation in VP (Lenz et al., 1990; Ohye et al., 1993; Seike,1993). The mediolateral progression in the representa-tion corresponds to that in VPS with the jaw medial tofingers, followed by wrist, elbow, shoulder, and leg.VPS is probably within VP or a VL-VP “transition”zone identified as Vcae or Vim by Hassler (1959) andVPLa in more recent studies (Hirai and Jones, 1989;Morel et al., 1997). Microstimulation of neurons in theVPS region of humans can elicit sensations of movementand deep pressure (Ohara et al., 2004).

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Ventroposterior Inferior Nucleus

In all primates, including humans (e.g., Morel et al.,1997), VPI is recognized as a narrow region just ventralto VP that is composed of small, pale-staining neurons.VPI is densely myelinated and reacts lightly to cyto-chrome oxidase. Narrow parts of VPI appear to extenddorsally into the cell-poor regions that separate face,hand, and foot subnuclei of VP (Krubitzer and Kaas,1992). Because of this dorsal finger-like extension ofparts of VPI, and its caudal extension into thalamicregions of similar appearance and perhaps function(see following discussion), some of the boundaries ofVPI have been uncertain. As a result, the major inputsto VPI from the spinothalamic and caudal trigeminotha-lamic afferents have been variously described asincluding not only VPI but also VP as well as morecaudal nuclei (see Apkarian and Hodge, 1989b). Never-theless, VPI “proper” receives a mixture of inputs fromlamina I nociceptive neurons and lamina V wide-dynamic-range neurons of the contralateral spinal cord(Craig, 2006b). The inputs to VPI reveal a somatotopicpattern with the hindlimb inputs most lateral and theforelimb and face inputs more medial (Gingold et al.,1991). Outputs to cortex also reflect this overall somato-topic pattern of organization (Cusick and Gould, 1990).Neurons in the VPI region of both monkeys (Apkarianand Shi, 1994) and humans (Lenz et al., 1993) are respon-sive to noxious stimulation. In monkeys, VPI projectsdensely to areas S2 and PV of lateral parietal cortexand less densely and more superficially to areas of ante-rior parietal cortex (Friedman and Murray, 1986; Cusickand Gould, 1990; Krubitzer and Kaas, 1992). AlthoughVPI relays spinothalamic tract information, and VPIincludes neurons responsive to noxious stimuli, it seemslikely that the role of VPI projections to cortex are largelymodulatory. They may have a role in experience-relatedplasticity of somatosensory cortex (see Kaas andFlorence, 2000), or in signaling stimulus intensitywithout the emotional component of pain (e.g., Brooksand Tracey, 2005).

The Posterior Group and the PosteriorVentromedial Nucleus

Apoorly defined group of nuclei with somatosensory,auditory, and multimodal functions, located just caudalto the ventroposterior complex, has been referred to asthe posterior group or complex (Jones, 2007). Thecomplex is commonly divided into separate limitans,suprageniculate, and posterior nuclei. The posterior“nucleus” is often subdivided into medial, lateral, andeven intermediate nuclei. The medial posterior nucleus(Pom) is composed of small cells that seem to mergewith caudal VPI. There is some evidence that neurons

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with large cutaneous receptive fields and multimodalresponses in the lateral cervical nucleus relay to Pom(see Metherate et al., 1987, for a review). Cortical projec-tions of the posterior complex appear to be to cortex ofthe lateral fissure near S2.

Recently, a part of the posterior group has beendistinguished in monkeys and humans as posteriorventromedial nucleus, VMpo (Craig et al., 1994; Daviset al., 1999; Blomquist et al., 2000). The nucleus receivessomatotopically organized nociceptive and thermore-ceptive spinothalamic inputs from layer I of the contra-lateral dorsal horn of the spinal cord via thespinothalamic tract (Craig, 2006a). VMpo projects tocortex in the lateral fissure in the region of the dorsalposterior insula. This pathway appears to be importantin mediating sensations of pain and temperature (seePerl, 1998).

Anterior Pulvinar, Medial Pulvinar, and LateralPosterior Nucleus

Other thalamic structures without direct inputs fromsecond-order somatic afferents can be considered partof the somatosensory system on the basis of connec-tions with somatosensory cortex. These include theanterior (oral) pulvinar with widespread projectionsto anterior parietal cortex, posterior parietal cortex,and somatosensory cortex of the lateral fissure (Cusickand Gould, 1990; Krubitzer and Kaas, 1992; Padberget al., 2009); the medial pulvinar with connectionswith posterior parietal cortex and the temporal lobe(e.g., Gutierrez et al., 2000) and the lateral posteriornucleus (LP) with projections to posterior parietalcortex (Cappe et al., 2007). In humans, degenerationhas been noted in the anterior pulvinar after damageto parietal cortex of the lateral fissure, while LP degen-erates after lesions of posterior parietal cortex (VanBuren and Borke, 1972). The roles of these nuclei inthe processing of somatosensory information areunknown, but the lack of direct sensory input and thewidespread cortical connections suggest modulatoryand integrative functions.

ANTERIOR PARIETAL CORTEX

The anterior parietal cortex was first considered asseveral separate fields in early architectonic studies(e.g., Brodmann, 1909), then as a single primary somato-sensory field or S-I on the basis of electrophysiologicalstudies in monkeys (see Marshall et al., 1937), andmore recently as several fields again, as the validity ofearly subdivisions as functionally distinct areas hasbeen experimentally supported (see Qi et al., 2008).

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Early attempts to subdivide anterior parietal cortexresulted in the differing conclusions of Campbell(1905), Smith (1907), Brodmann (1909), Vogt and Vogt(1919), and von Economo and Koskinas (1925). Thesubdivisions made by Campbell and Smith fell intodisuse, but the proposals of Brodmann, Vogt and Vogt,and von Economo are in use today (see Chapter 23).In brief, Brodmann distinguished a mediolateral stripof cortex in the caudal bank of the central (Rolandic)fissure as area 3, an immediately superficial and caudalstrip on the caudal lip of the sulcus as area 1, and a morecaudal strip on the surface of the postcentral gyrus asarea 2. Area 3 was described as a field with denselypacked small granular cells in layer IV, as is character-istic of sensory fields, while areas 1 and 2 had less domi-nant sensory features. Brodmann further describeda “transitional” field (deep in the central fissure) in ante-rior area 3 with both prominent sensory (layer IVgranule cells) and motor (layer V pyramidal cells)features. Vogt and Vogt (1919) added to this proposalby stressing the distinctiveness of anterior area 3, andsubdivided area 3 into two fields, area 3a and area 3b(see Jones and Porter, 1980, for a review). These fourarchitectonically defined subdivisions of postcentralsomatosensory cortex are in common use for humanand other anthropoid primates today (Qi et al., 2008).However, some investigators use the terms of vonEconomo (1929) for these subdivisions. Rather thannumber cortical fields, von Economo used two lettersto denote fields, with the first letter indicating thelobe of the brain for the field, and the second letterindicating the order in which fields were described inthe lobe, typically starting with fields of obvioussensory nature. In general, Brodmann (1909) and vonEconomo (1929) divided the human brain in differentways, but the proposed subdivisions of anterior pari-etal cortex are quite similar, the agreement suggestingthe validity of the divisions. Von Economo’s most ante-rior field, deep in the central sulcus, is area PA, equiv-alent to area 3a. The adjacent field, area PB, was notedas sensory “koniocortex” as a result of the powder-likeappearance of the small granule cells in layer IV ofwhat clearly corresponds to area 3b. Area PC, charac-terized by a less distinct laminar structure, is equiva-lent to area 1. A more caudal strip of cortex witha more distinct layer IV and layer VI, is area PD, closelycorresponds to area 2.

Anterior Parietal Cortex in Monkeys

Over the last few years, research on monkeys hasgreatly clarified the significance of the four architectonicstrips. Conclusions based on an extensive number ofanatomical and electrophysiological studies are brieflysummarized next.

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Area 3b

We have termed area 3b “S-I proper” because itappears to be the homolog of the primary somatosen-sory area, S-I, in non-primates (Kaas, 1983). Area 3bcontains a separate, complete map of the cutaneousreceptors of the body (Nelson et al., 1980). The represen-tation proceeds from the foot in medial cortex to the faceand tongue in lateral cortex, with the digits of the footand hand pointing “rostrally” (or more precisely, deeperin the central sulcus), and the pads of the palm and soleof the foot caudal in 3b near the area 1 border. Subdivi-sions of area 3b related to body parts can be seen in brainsections cut parallel to the surface as myelin-dense ovalsseparated by myelin-light septa (Jain et al., 1998, 2001;Iyengar et al., 2007). The most conspicuous septum tran-sects lateral area 3b where it separates the more medialhand representation from the more lateral face represen-tation. In the hand representation, a narrow strip ofcortex for each digit is bounded on each side by septa(Qi and Kaas, 2004). The hand representation isbordered laterally by a caudorostral series of threemyelin-dense ovals, first for the upper face, next forthe upper lip, and then for the lower lip and chin.Next, a succession of four ovals represent the contralat-eral teeth, the contralateral tongue, the ipsilateral teeth,and the ipsilateral tongue. Except for the rostrolateralrepresentations of the ipsilateral tongue and teeth (alsosee Manger et al., 1996), the area 3b representation,like other representations in anterior parietal cortex, isalmost exclusively of the contralateral body surface.The septa-distinguishing body parts in area 3b usefullyserve as an anatomical guide for other types of experi-ments. They have not been described in area 3b ofhumans, but they may be present (see Mountcastle,2005).

The activation of area 3b neurons is from RA-I and SA(I and possibly II) afferents relayed from the ventropos-terior nucleus. RA-I and SA inputs appear to be segre-gated into bands (columns) in layer IV (Sur et al.,1984). Microstimulation of neurons in the RA modulesof area 3b in monkeys provided psychophysical datathat suggest that this stimulus can be perceived as flutteron the fingers (Romo et al., 2000). Most of the large relayneurons in VP project to layer 4 of area 3b via thickrapidly conducting afferents. Smaller neurons in thesepta of VP and in VPI project to the superficial layers(Rausell and Jones, 1991). Major outputs in area 3b areto area 1, area 2, and S2 and the parietal ventral area,PV, and these fields provide feedback inputs (Krubitzerand Kaas, 1990; Burton et al., 1995; Romo et al., 2000).Area 3b is callosally interconnected with areas 3b, 1,and 2, and S2 of the opposite hemisphere. The callosalconnections are unevenly distributed, with the largerepresentations of the glabrous hand in area 3b having

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few connections (Killackey et al., 1983). Neurons inarea 3b have small receptive fields with excitatory andinhibitory subregions (Sripati et al., 2006). These smallexcitatory receptive fields do not reflect the callosalconnections, which may contribute to surroundsuppression or enhancement, but instead are confinedto locations on the contralateral body surface. Yet,neuron responses are often reduced or increased bystimuli on the hand but outside the receptive field, andeven on the other hand (Reed et al., 2008). In monkeys,inactivation or lesions of area 3b or area 3b togetherwith areas 1 and 2, result in impairments in all but thecrudest of tactile discriminations involving texture andshape (Randolph and Semmes, 1974; Hikosaka et al.,1985; Zanios et al., 1997; Brochier et al., 1999). Smallobjects might be unrecognized by touch and ignored,and coordination during grasping is impaired.

Area 1

Like area 3b, area 1 contains a systematic representa-tion of the body surface. The representation parallelsand also roughly mirrors that in area 3b. Thus, the foot,leg, trunk, forelimb, and face are represented in a medio-lateral cortical sequence (as in area 3b), but the digit tipsare represented caudally near the area 2 border ratherthan rostrally near the area 3b border. Most neurons inarea 1 are rapidly adapting and respond as if theywere related to RA-I cutaneous receptors. A smallportion of neurons, perhaps 5%, respond as if activatedby RA-II (Pacinian) afferents. The results of opticalimaging experiments suggest that small regions ofdomains of neurons in area 1 are selectively dominatedby SA, RA-I, and RA-II (PC) inputs (Friedman et al.,2004). Neurons in area 1 tend to have larger and morecomplex receptive fields (Iwamura et al., 1993),including stronger suppressive or inhibitory surrounds,than area 3b neurons (Sur, 1980; Sur et al., 1985). Someneurons code for the direction of movement on theskin (Hyvarinen and Poranen, 1978; Bensmaia et al.,2008). More neurons in area 1 than in area 3b are sensi-tive to stimulus orientation (Bensmaia et al., 2008). Theactivity patterns of most area 1 neurons, but not area3b neurons, are modified according to what motorbehavior will follow the stimulus (Nelson, 1984). Area1 receives strong inputs from both area 3b and the ven-troposterior nucleus. The VP inputs are partly fromcollaterals of neurons projecting to area 3b (Cusicket al., 1985), and the terminations are largely of thinneraxons than those of area 3b. As the inputs from area 3bare to layer 4 and those from VP are to layer 3 (Jones,1975), the area 3b inputs appear to provide the majoractivation. Thus, lesions of areas 3a and 3b inactivateneurons in area 1 (Garraghty et al., 1990a). Feedforwardcortical outputs are predominantly to area 2, PV, and S2,and feedback inputs are from these fields. Callosal

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connections are more evenly distributed than for area 3b,but connections in the hand, foot, and parts of the faceregions remain sparse (Killackey et al., 1983). The callosalconnections largely modulate neurons with receptivefields on the contralateral body surface, but someneurons with ipsilateral or bilateral body midline recep-tive fields occur (Taoka et al., 1998). In monkeys, lesionsof area 1 impair discriminations of texture rather thanshape (Randolph and Semmes, 1974; Carlson, 1981).

Area 2

Area 2 contains a complex representation of bothcutaneous and non-cutaneous receptors. Neuronsappear to be influenced by cutaneous receptors, deepreceptors, or both. The portions of area 2 related to thehand and face are most responsive to cutaneous stimu-lation. The representation is in parallel with those inareas 3b and 1 so that the foot, trunk, hand, and faceform a mediolateral cortical sequence. A mirror reversalorganization of that in area 1 is apparent for parts of area2 near the area 1 border. However, the overall organiza-tion is more complex than in areas 3b and 1, and somebody parts are represented more than once in area 2(Pons et al., 1985). Receptive fields for neurons in area2 are typically, but not always, larger than those forneurons in areas 3b and 1, and receptive field propertiesappear to be complex (Iwamura et al., 1993). Manyneurons are best activated by stimuli of certain shapesor directions of movement. Some neurons respondduring both passive and active movements and othersonly during active movements (Prud’Homme andKalaska, 1994). The inputs from deep receptors arelargely those related to muscle spindles, suggestingthat area 2 combines information about limb and digitposition with tactile information during active touch.The major thalamic input to area 2 is from VPS(Figure 30.4), but a sparse input to the hand region ofarea 2 originates in VP (Pons and Kaas, 1985; Padberget al., 2009). Major cortical inputs are from areas 1, 3b,and 3a (Pons and Kaas, 1986). There also appear to besparse inputs from the motor cortex and to S2. Callosalconnections are fairly evenly distributed and includethe hand representation (Killackey et al., 1983). Neurons,however, have excitatory receptive fields mainly on thecontralateral body, but bilateral receptive fields arecommon (Iwamura et al., 2001). Lesions of area 2 inmonkeys impair finger coordination (Hikosaka et al.,1985) and discriminations of shape and size (Carlson,1981).

Area 3a

Area 3, in the depth of the central sulcus, forms thefourth systematic representation of the body in anteriorparietal cortex. Area 3a is largely activated by musclespindle and other deep receptors, but some cutaneous

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activation is also apparent, especially in the portiondevoted to the hand. The representation parallels thatin area 3b (Krubitzer et al., 2004). Neurons in area 3aare responsive during movements and are influencedby behavioral intentions (“motor-set,” see Nelson,1984). The major input is from VPS and roughly halfof the VPS relay neurons project to both area 3a andarea 2, thus providing the same information (Cusicket al., 1985). Area 3a projects to area 2, motor cortex,S2, and other fields (Huerta and Pons, 1990; Huffmanand Krubitzer, 2001). Callosal connections are uneven,but the hand region has somewhat more densecallosal connections than the hand representation inarea 3b.

Subcortical Projections

All four fields project to a number of subcortical fieldsincluding feedback to the thalamic relay nuclei, the basalganglia, the anterior pulvinar, the pons, the dorsalcolumn nuclei, and the spinal cord (see Kaas and Pons,1988). These projections presumably function in modi-fying motor behavior and sensory afferent flow. Theprojections to the pons are to neurons that relay to thecerebellum (Vallbo et al., 1999) where they may modifymotor responses.

Anterior Parietal Cortex in Humans

Several types of evidence support the conclusion thatthe organization and functions of anterior parietal cortexin humans are similar to those in monkeys.

Architectonic Fields

As in monkeys, four architectonic fields can be iden-tified in the anterior parietal cortex of humans – areas3a, 3b, 1, and 2 (see Chapter 23). In early studies, thepresumed boundaries of these fields varied somewhat,and other terminologies were sometimes used.Recently, a number of studies have reconsidered theissue of how anterior parietal cortex is divided intofields with the benefit of new chemoarchitectonicmethods (Zilles et al., 1995; White et al., 1997; Geyeret al., 1999; Qi et al., 2008). Area 3b is the most obviousfield, and investigators closely agree on boundaries.Area 3a is also easily recognized as distinct from 3band area 4 (motor cortex), although area 3a appearsto have rostral and caudal subdivisions. The area 1border with area 2 is also reasonably distinct, whilethe area 2 border with posterior parietal cortex (area 5)is the least obvious, as in monkeys. Detailed compar-ison of the architecture of these fields in monkeys(where somatotopy and connections have beenstudied), chimpanzees, and humans (Qi et al., 2008)perhaps provides the most compelling evidence forfunctionally significant boundaries. Overall, as in

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monkeys, areas 3a and 3b have chemoarchitectonicfeatures that are characteristic of primary sensory areas,while areas 1 and 2 resemble secondary areas (see Eske-nasy and Clarke, 2000), supporting the conclusion thatareas 3b, 1, and 2 constitute a processing hierarchy inhumans as in monkeys.

As in macaque monkeys, area 3a of humans occupiesthe depths of the central sulcus, where it extends some-what from the posterior to the anterior bank. In area 3a,layers IVand VI are less pronounced than in area 3b, andlayer V pyramidal cells are more obvious. Area 3boccupies roughly the middle half or more of the poste-rior bank of the central sulcus. The field appears onthe surface as the central sulcus ends near the medialwall, and the field extends into the medial wall. Area3b is easily distinguished over most of its extent by thedense packing of small cells in layer IV, and the rela-tively dense packing of cells in layer VI. The small cellshave led to the terms “koniocellular cortex” and “parvi-cellular core” (see Chapter 23). Most investigators showarea 3b as ending with the lateral extent of the centralsulcus, but area 3b extends anteriorly past the end ofthe sulcus in monkeys, where it represents the mouthand tongue. However, these body parts may be repre-sented more medially in humans (see following discus-sion). Area 1 occupies the anterior lip of the postcentralgyrus where it borders area 3b on the posterior bank ofthe central sulcus and extends over the anterior third ofthe postcentral gyrus. Layers IV and VI are less denselypacked with cells in area 1 than in area 3b, so the overallappearance is of less conspicuous lamination. Area 1would roughly correspond to the posterior half of thepostcentral area of Campbell (1905), and the full extentof area 1 of Brodmann. Area 1 is unlikely to be as wideas area PC of von Economo and Koskinas (1925), area1 of Sarkossov and co-workers (see Braak, 1980), or themedial half of the paragranulous belt of Braak (1980).Area 2 is characterized by a denser layer IV than isfound in area 1. The caudal border is difficult to delimitin monkeys even with the aid of electrophysiologicaldata, and the precise location of this border remainssomewhat uncertain in humans (however, see Qi et al.,2008). However, the expected width of area 2 wouldapproximate that of area 1.

Maps in 3a, 3b, 1, and 2: Evidence from Scalp andBrain Surface Recordings

As part of efforts to localize abnormal tissue and forother clinical reasons, recordings have been made fromthe scalp, from the surface of anterior parietal cortex,and from depth probes in the cortex of 3b of patients.In addition, neuromagnetic recordings and scalp-evoked potentials have been recorded from healthyvolunteers. Such recordings support the conclusion

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that separate representations with different functionsexist in areas 3a, 3b, 1, and 2. The hand representationin area 3b appears to correspond to a bulge in the centralsulcus (Sastre-Janer et al., 1998).

1. Electrical stimulation of cutaneous afferents in themedian nerve of the hand results in a focus of evokedpotentials after 20–30ms in area 3b of the caudal bankof the central sulcus and a second focus after25–30 ms in area 1 of the dorsolateral surface ofpostcentral cortex (see Allison et al., 1988; Ploneret al., 2000). The two foci support the view that area3b and area 1 have separate maps of the body surface.The area 1 potentials are caudal to the area 3bpotentials, indicating parallel maps, although a slightmedial shift of the area 1 focus suggests a smalldisplacement of one map relative to the other. As inmonkeys, activity was generated only fromstimulating contralaterally.

2. Stimulation of muscle afferents from the human handresults in a focus of activity that is caudal to that forcutaneous afferents (Gandevia et al., 1984). Areasonable interpretation of this result is that themuscle afferents activate area 2, which is caudal to theactivity produced in areas 1 and 3b by cutaneousafferents. More recently, evoked potentials to jointmovement in the fingers has been attributed to area 2activation (Desmedt and Ozaki, 1991), suggestingthat joint receptor afferents as well as muscle spindleafferents activate area 2.

3. Another focus of activity produced by deep receptoror muscle spindle afferents is deep to foci related tocutaneous stimulation. Using neuromagneticrecordings, Kaukoranta et al. (1986) found that mixednerve stimulation resulted in a deeper focus ofactivity in the central sulcus than cutaneous nervestimulation. The results were interpreted as evidencefor muscle spindle receptor input to area 3a andcutaneous receptor input to area 3b. Similar resultshave been obtained with fMRI (Moore et al., 2000;also see Mima et al., 1996, 1997).

4. More recently, non-invasive imaging techniques havebeen used to explore the organization of anteriorparietal cortex in awake humans. While positronemission tomography (PET) has been useful for grosslocalization of sites of induced activity (see Burtonet al., 1993, 1999), functional magnetic resonanceimaging (fMRI) has provided more resolution. Mostnotably, vibratory and other stimuli applied todifferent finger tips provided evidence for separaterepresentations in areas 3a, 3b, 1, and 2 (Lin et al.,1996; Gelnar et al., 1998; Francis et al., 2000;Blankenburg et al., 2003). Functional magneticresonance imaging has also demonstrated therepresentation of thumb to little finger in

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a lateromedial sequence in area 3b, area 1, and area 2(Kurth et al., 1998, 2000; Francis et al., 2000), andshow that the tongue, fingers, and toes arerepresented in a lateromedial sequence (Sakai et al.,1995). Hoshiyama et al. (1996) located therepresentation of the lower lip lateral (inferior) to thatof the upper lip, as in monkeys (Jain et al., 2001).Teeth are represented next to the lip followed by thetongue (Miyamoto et al., 2005), as in monkeys.

5. Recordings of scalp-recorded evoked potentials inhumans also support the conclusion that the maps ofreceptor surfaces in anterior parietal cortex areorganized much as they are in monkeys. Thus,electrical stimulation of the little finger activatescortex 1–2 cm medial to that activated by stimulatingthe thumb (see Hari and Kaukoranta, 1985), andactivity evoked in cortex by tapping the tongue islateral to that produced by tapping the finger (Ishikoet al., 1980). Measurements of magnetic fields,thought to be generated in the depths of the centralsulcus in area 3b, indicated that the thumb, indexfinger, and ankle are represented at successively moremedial position (Okada et al., 1984). These methodshave now been used to show that the tongue, lowerlip, upper lip, thumb through little finger, palm,forearm, elbow, upper arm, chest, thigh, ankle, andtoes are represented in a lateromedial order(Nakamura et al., 1998; Figure 30.7).

FIGURE 30.7 The somatotopic organization of the anteriorsomatosensory cortex according to results obtained from the non-invasive recording of sensory-evoked magnetic fields (Nakamuraet al., 1998). The center of activity for the different body parts is shownon the lip of the central sulcus, but the regions generating themagnetic fields were judged to be along the posterior bank of thecentral sulcus, most likely reflecting activity in area 3b and part of area1. This map does not address the issue of separate representations ineach of area 3a, 3b, 1, and 2. In addition, centers of activity for ankleand toes were likely generated from cortex on the medial wall.

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6. Extensive observations on the somatotopy ofpostcentral cortex in humans come from recordingsof evoked slow waves from the brain surface duringneurosurgery (Woolsey et al., 1979). In a sequence ofrecording sites along the posterior lip of the centralsulcus, from near the medial wall to over two-thirdsof the distance to the lateral (Sylvian) sulcus,potentials were evoked from foot, leg, thigh, trunk,and hand. In individual patients, there was somenotable variability in organization so that the legrepresentation extended from the medial wall ontothe dorsolateral surface in some but not other cases.By electrically stimulating the dorsal nerve of thepenis and recording evoked potentials from anteriorparietal cortex of humans during surgery, Bradleyet al. (1998) provided evidence that the penis isrepresented in cortex near the representation of thelower abdomen and lateral to that of the foot (also seeRothemund et al., 2002). Similar results have nowbeen obtained with fMRI (Kell et al., 2005).

7. More details about the sequence of representation ofbody parts in postcentral cortex have been obtainedby electrically stimulating the brain in patients. Usinghigher levels of stimulating current than used formotor cortex, Foerster (1931, 1936a) was able toproduce a postcentral motor map that roughlymatched the precentral motor map in themediolateral cortical order of leg, hand, and face(Figure 30.8). Penfield and Rasmussen (1950) alsoreported evoked movements for postcentralstimulation sites, with the postcentral motor maproughly paralleling the precentral motor map inmediolateral organization. More precise information

FIGURE 30.8 The order of representation in human postcentralcortex according to Foerster (1931). The summary was based onsensations reported when the surface of cortex was electrically stim-ulated. Most stimulation sites were in area 1 or area 2, as area 3b islargely in the central sulcus. No distinctions between the separaterepresentations in areas 3a, 3b, 1, and 2 were made. Similar but moredetailed maps were later produced by Penfield and Jasper (1954).Their maps placed the foot in the cortex of the medial wall andincluded the back of the head in center medial to the armrepresentation.

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about the somatotopic organization of postcentralcortex has been obtained by noting where sensationsare located during electrical stimulation of corticalsites. As one might expect, sensations evoked fromstimulating the cortex match in somatotopic locationthe source of afferents related to the stimulation sites.Thus, stimulating cortex where evoked responseswere obtained to ulnar nerve stimulation resulted insensations largely confined to the ulnar hand (Jasperet al., 1960). The extensive report of Penfield andBoldrey (1937) summarizes the results fromstimulating precentral and postcentral cortex in 163patients. Stimulation sites resulting in sensationswere scattered over the precentral and postcentralgyri, and even a few more posterior or more anteriorsites were effective. However, the vast majority ofsites were along the posterior lip of the central sulcusand were probably evoking sensations by activatingneurons in area 1. The evoked sensations were not oflight touch, but were described as a localizednumbness, tingling, or, infrequently, the feeling ofmovement. Sensations were evoked from the cortexextending from the medial wall, where the foot isrepresented, to the lateral fissure, where the mouth isrepresented. In general, the sensory ordercorresponds to the detailed maps compiled formonkeys (e.g., Nelson et al., 1980). Cortex devoted tothe foot and toes was most ventral on the medial wall.The back of the head and the neck were in medialcortex with the trunk representation, while the facewas in lateral cortex separated from the head by thecortex devoted to the arm and hand. The digits wererepresented from little finger to thumb ina mediolateral sequence. As for the area 1representation in macaque monkeys, the orbital skinand the nose were represented just lateral to thethumb in humans. In monkeys and humans, thetongue and mouth are most lateral in the responsivecortex. Thus, the mediolateral sequence ofrepresentation in the region of anterior area 1 appearsto be quite similar in humans (Penfield and Boldrey,1937; note more detail and some differences insummaries in Figures 30.7 and 30.8) and monkeys(Nelson et al., 1980). Little can be said aboutsequences of change in the rostrocaudal direction,however, because only microelectrode maps providemuch detail about this direction in monkeys, and thesurface stimulation and recordings in humans mayinvolve amounts of tissue that are large relative to thenarrow widths of the representations in areas 3b, 1,and 2.

8. Some aspects of somatosensory organization havelong been known from the order of progressions ofsensations or movements (“the Jacksonian march”)during epileptic seizures. Because the seizure starts

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from a focus and spreads to more distant tissue, theorder of sensations reflects the order ofrepresentation. Typical cases are described byFoerster (1936b) and Penfield and Jasper (1954). Theorders of these sensory marches correspond to theevoked sensation map (Figure 30.8). For example,a sensation of tingling or numbness in the thumbmaybe followed by tingling in the face, or a tingling thatpasses from thumb to fingers, to arm. Sensations arecontralateral to the postcentral focus, and theyseldom spread over many body parts (Mauguiereand Courjon, 1978).

Sensory and Perceptual Impairments FollowingLesions

Damage to postcentral cortex, if extensive, causessevere and lasting impairments in pressure sensitivity,two-point discrimination, point localization, anddiscrimination of object shape, size, and texture(Head and Holmes, 1911; Semmes et al., 1960; Corkinet al., 1970; Roland, 1987a; Taylor and Jones, 1997).The spatial accuracy of motor movements is alsoimpaired by the reduced sensory control (Agliotiet al., 1996). However, the detection and crude locali-zation of tactile stimuli remains intact. Roland(1987a) reported that lesions of the deep and anteriorpart of the hand region of postcentral cortex, presum-ably including much but not all of the area 3b repre-sentation and probably the area 1 representation,abolished the ability to discriminate edges fromrounded surfaces, while lesions of the surface, appar-ently involving areas 1 and 2, left the ability to distin-guish edges from rounded surfaces, but removed theability to discriminate shapes and curvatures. Thisdifference is similar to that reported for monkeyswhere lesions of areas 3b, 1, and 2 permanently abol-ished the ability to distinguish the speed of movingtactile stimuli (Zainos et al., 1997), lesions of area 1impaired texture discriminations, and area 2 lesionsaltered discrimination of shape (Randolph andSemmes, 1974; Carlson, 1981; also see LaMotte andMountcastle, 1979). Inactivation of the finger represen-tations in area 2 of monkeys led to a major deficit infinger coordination while small food pieces were oftenignored after contact with inactivation of area 3b(Hikosaka et al., 1985). Remarkably, small lesions ofpart of the hand representation result in no obviousimpairment in humans (Evans, 1935; Roland, 1987a,1987b). Roland (1987a) estimated that a notableimpairment resulted only after lesions involvingthree-fourths or more of the hand region of anteriorparietal cortex. Furthermore, the larger the lesion ofthe region, the greater the impairment (Roland,1987b). The preservation of abilities after lesions to

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parts of somatotopically organized representationscould be the result of cortical reorganizations thatresult in the recovery of lost parts of representations.Removing part of a representation or deactivatingpart of a representation in monkeys can be followedby cortical reorganization, even in adults, so thatremaining cortex is activated by skin formerly relatedto the damaged area, and deactivated cortex becomesresponsive to alternative inputs (see Kaas andFlorence, 2000, for a review).

FIGURE 30. 9 A dorsolateral view of the brain showing proposedsubdivisions of posterior parietal cortex in macaque monkeys. Areas5a, 5b, 7a, and 7b are traditional subdivisions from Brodmann (1909)and Vogt and Vogt (1919). The ventral intraparietal region (VIP) andthe lateral intraparietal region (LIP) are subdivisions that have beendistinguished by visual and visuomotor connections (Maunsell andVan Essen, 1983; Anderson et al., 1985). Other recently proposed fieldsinclude the medial (MIP) and the anterior (AIP) intraparietal region.The MIP region and adjoining cortex is also known as the parietalregion (PRR). Alternative terms (e.g., PE for 5b) for posterior parietaland frontal motor cortex, based in part on von Economo (1929) arefrom Rizzolatti and Matelli (2003). Frontal motor fields include thesupplementary motor area (SMA), dorsal (PMd) and ventral (PMv)premotor areas, and primary motor cortex (M1). See text for otherareas.

SOMATOSENSORY CORTEX OF THELATERAL (SYLVIAN) SULCUS

INCLUDING INSULA

Much of the cortex of the upper bank of the lateralsulcus and some of the cortex of the insula are somato-sensory in function. Because of the general inaccessi-bility of this region in monkeys and humans, therehave been relatively few attempts to reveal aspects offunctional organization by stimulation or recording.However, there is clear evidence for the existence ofseveral functionally distinct areas from fMRI studies(Eickhoff et al., 2008) that correspond to separate archi-tectonic fields (Eickhoff et al., 2007). The lateral somato-sensory cortex may be part of a critical corticolimbicpathway for the identification of objects by touch (seeFriedman et al., 1986), as monkeys have severe deficitsin tactile memory after combined removal of the amyg-dala and hippocampus (Murray and Mishkin, 1984a).The pathways for inputs to these limbic structuresinvolve convergent inputs from areas 3a, 3b, 1, and 2to areas of the upper bank of the lateral sulcus (Cusicket al., 1989), and a relay from these areas over morerostral subdivisions of the somatosensory cortex in thelateral sulcus (Figure 30.9). Because this lateral pathwayis best understood in macaque monkeys, the organiza-tion of lateral somatosensory cortex in these primatesis briefly reviewed.

Organization of Cortex of the Lateral Sulcus inMonkeys

Much progress has been made in recent years inunderstanding the traditional “SII” region (see below)of the lateral somatosensory cortex in monkeys. The large“SII” region has now been divided into several areas. Onesubdivision that has been repeatedly described is thesecond somatosensory area (S2), named because it wasthe second representation after S1 discovered in catsand later in other mammals. S2 appears to border thelateral extension of areas 3b and/or areas 1 and 2 inmonkeys, according to species (see Pons et al., 1987;Cusick et al., 1989; Krubitzer and Kaas, 1990; Burton

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et al., 1995; Krubitzer et al., 1995; Disbrow et al., 2000).S2 forms a systematic representation of the contralateralbody surface on the upper bank of the lateral sulcuswith the face represented along the outer lip, the handdeeper in the sulcus, and the foot near the fundus. A pari-etal ventral area (PV) forms a second representation ofthe contralateral body surface just rostral to S2 (see Dis-brow et al., 2000, for review). S2 and PV adjoin alongrepresentations of the hand, and they form mirror-imagerepresentations of each other. PV and S2 are bordered inthe fundus of the lateral sulcus by a ventral somatosen-sory area (VS), which extends somewhat onto the lowerbank of the central sulcus and insula to border secondaryauditory fields (Cusick et al., 1989; Krubitzer et al., 1995).More recent evidence suggests that VS actually includesseparate rostral, VSr, VSc, and caudal representations,one bordering PV and the other S2 (Qi et al., 2002; Coqet al., 2004).

S2 and PV receive feedforward inputs from all fourareas of anterior parietal cortex (Krubitzer and Kaas,1990; Burton et al., 1995; Qi et al., 2002; Disbrow et al.,2003; Coq et al., 2004). Removing these areas deactivatesS2 and PV (Pons et al., 1987; Burton et al., 1990;Garraghty et al., 1990b). Major inputs to S2 and PVfrom the ventroposterior inferior nucleus (Disbrow

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et al., 2002) do not seem to be capable of independentlyactivating neurons in these areas. Neurons in both S2and PV respond to cutaneous stimulation within recep-tive fields that are generally larger than those in area3b or area 1. Inputs to S2 and PV from areas 3a and 2undoubtedly provide some activation from deep recep-tors. Proprioceptive neurons seem to be concentratedanteriorly in PV and posteriorly in S2, away from cuta-neous representations of digit tips (Fitzgerald et al.,2004). Callosal connections from S2 and PVof the oppo-site hemisphere are particularly dense (Disbrow et al.,2003), and some bilateral receptive fields have beenreported, although ipsilateral stimuli largely modulateactivity based on contralateral receptive fields. Neuronsin S2 and PVappear to code for stimulus features such asroughness (Pruett et al., 2000) and the orientation ofedges (Fitzgerald et al., 2006). S2 and PV may beinvolved in determinations of the sizes and shapes ofobjects (Fitzgerald et al., 2006). Lesions of the PV-S2region greatly impair the abilities of monkeys to maketactile discriminations and identifications (Murray andMishkin, 1984b). Ipsilateral cortical projections of PVand S2 include PR, insular cortex, premotor cortex,and posterior parietal cortex (Disbrow et al., 2003).Inputs to adjoining areas of lateral somatosensory cortexare relayed to perirhinal and entorhinal cortex(Friedman et al., 1986). The processing series from ante-rior parietal to lateral parietal to perirhinal cortex andthen to the hippocampus constitutes a proposed lateralhierarchy of areas involved in the recognition andmemory of objects by touch (Mishkin, 1979; Murrayand Mishkin, 1984a; Friedman et al., 1986).

Cortex caudal to S2 includes part of 7B that extendsinto the lateral sulcus, and the retroinsular area (Ri).Neurons in both lateral 7B and Ri are responsive to cuta-neous stimuli (Krubitzer et al., 1995). Cortex caudal toVS on the lower bank of the lateral sulcus has neuronsresponsive to vision and somatosensory stimuli (Krubit-zer et al., 1995). Cortex rostral to PVreceives inputs fromPV and S2 and has been called the parietal rostral area,PR (Krubitzer and Kaas, 1990; Krubitzer et al., 1995).Cortex along VS on the lower bank of the lateral sulcuscontains primary auditory area and the medial belt ofsecondary auditory areas, including the caudal medialarea, CM, where neurons respond to both auditoryand somatosensory stimuli, with somatosensory inputscoming from retroinsular (Ri) granular insular regions(Smiley et al., 2007). The more posterior portion of theinsula in monkeys is a region of thalamocortical inputsfrom VMpo relaying information concerned with pain,temperature, and the well-being of the internal organs(Craig et al., 2000; Craig, 2002). Part of the posteriorinsula and the retrosplenial region (Ri) receives vestib-ular information from the thalamus (Guldin et al.,1992; Guldin and Grusser, 1998). Insular cortex also

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receives inputs from cutaneous receptors. The anteriorinsula includes a gustatory area or areas (Augustine,1996; Kaas et al., 2006). Thus, the cortex of the lateralsulcus, including the insula, has a number of somatosen-sory and multisensory areas.

Lateral and Insular Parietal Cortex in Humans

There is increasing evidence that at least some of thecortex in the lateral fissure of humans is organizedmuchas in monkeys. An fMRI study using tactile stimuliapplied to various body parts provides clear evidencefor both S2 and PV in humans. PV and S2 are organizedas mirror-reversal images of each other, both proceedingfrom face to forelimb to hindlimb from near the lip of theupper bank to the depths of the lateral fissure (Disbrowet al., 2000). Both S2 and PV demonstrate some increasedactivity with ipsilateral stimulation and more activitywith bilateral stimulation (Disbrow et al., 2001; Eickhoffet al., 2008).

Studies of the somatosensory cortex of the lateralsulcus in humans traditionally refer to a large “SII”region that includes S2, PV, and other areas. The termS2 is used here to refer to a particular somatosensoryarea with a somatotopy corresponding to that of SII ofearly descriptions for a range of mammals. In humans,the SII region has been divided into four architectonicfields, parietal operculum (OP) areas 1, 2, 3, and 4(Eickhoff et al., 2006c, 2007). OP4 is thought to be coex-tensive with PV, OP1 with S2, and OP3 with much ofVS. As VS in monkeys appears to be a composite oftwo somatotopically organized areas, a more rostralarea, VSr and a more caudal area VSc (Coq et al.,2004). OP3 may correspond to VSr and OP2 to VSc(see Eickhoff et al., 2006a; Burton et al., 2008). All fourfields are activated by tactile stimulation, and differ-ences in activation occurred with the task (Eickhoffet al., 2006a; Burton et al., 2008), but differences in thefunctional roles of the four areas are not well establishedfor humans or monkeys. In monkeys and humans, theparietal rostroventral area, PR, just anterior to PV, is acti-vated during body movements (Hinkley et al., 2007),suggesting a role in manual exploration during objectdiscrimination. Alternatively, cortex in the PR regionmay be responsive to visceral stimulation (Eickhoffet al., 2006b), and PR is in the region of the proposedgustatory cortex. Cortex caudal to S2 in area 7b isanother region responsive in humans to tactile stimula-tion of the hand.

The insula of the cortex of the lateral sulcus is a large,multisensory region of the human brain that has longbeen divided into a posterior granular region, witha well-developed layer 4 of granule cells, a more anteriordysgranular region, and an anterior agranular region(Augustine, 1996). Each of these regions is likely to

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contain several functional areas. The posterior insula hasbeen shown to be responsive to painful stimuli, temper-ature, auditory, and vestibular stimuli. Painful sensa-tions have been evoked by electrical stimulations fromthe upper, posterior insula (Ostrowsky et al., 2002; Afifet al., 2008; also see Chapter 32). The posterior insulaconstitutes a multisensory region (Mazzola et al., 2006)that possibly codes the magnitudes of sensory inputs(Baliki et al., 2009). The anterior insula appears to bemore involved with motor functions via connectionswith frontal cortex. One proposed function is to allocateattention and help select appropriate behaviors out ofalternatives (Eckert et al., 2009).

POSTERIOR PARIETAL CORTEX

The posterior parietal region is an arbitrary subdivi-sion of the brain that includes most of the parietal lobecaudal to area 2 but excludes the cortex of the lateral(Sylvian) fissure and the supplementary sensory areaof the medial wall (Figure 30.10). Current investigatorscommonly refer to the architectonic subdivisions ofBrodmann (1909) or von Economo (1929), and bothsystems are in use. However, research on monkeyssuggests that the proposed fields (areas 5a, 5b, 7a, and7b or areas PE, PF, and PG) have little validity otherthan denoting general regions of the lobe. Other subdivi-sions have been suggested by patterns of connectionsand the response characteristics of neuronal popula-tions, but the organization of posterior parietal cortexis not well understood. Electrical stimulation in humansseldom produces any sensations or motor responses(Penfield and Rasmussen, 1950), although Foerster

FIGURE 30.10 Posterior parietal and lateral cortex of humans.The posterior parietal cortex has been variously subdivided by earlyinvestigators (for example, see Campbell, 1905; Smith, 1907;Brodmann, 1909; Vogt and Vogt, 1919, 1926; von Economo andKoskinas, 1925). The subdivisions shown here reflect those of Vogtand Vogt, with the second somatosensory area (S2) and the parietalventral area (PV) of the lateral sulcus added. Much of the regiondenoted here as 7b would be in Brodmann’s area 40.

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(1931, 1936a) was able to produce hand movementsand leg movements on occasion with high levels ofstimulating current. Posterior parietal cortex has beenimplicated in both somatosensory and visual functionsas well as in premotor planning, but lesions do notproduce simple sensory impairments. Rather, largelesions produce a variety of complex symptoms, manyincluded within the general category of contralateralsensory neglect or inattention. In monkeys, impairmentsare basically the same regardless of the hemisphere ofthe lesion, but in humans, lesions of the right or “minor”hemisphere produce a much more profound defect.Major reviews of posterior parietal cortex organizationand function in monkeys and humans include those ofMountcastle (1975), Lynch (1980), Hyvarinen (1982),Yin and Medjbeur (1988), Andersen et al. (1997), Colbyand Goldberg (1999), Fogassi and Luppino (2005) andGardner (2008). Also, see Chapter 27 for connections ofsubdivisions of posterior parietal cortex with motorareas of the frontal lobe.

Posterior Parietal Cortex in Monkeys

Since posterior parietal cortex of all primates is a placewhere somatosensory information is combined withvisual and auditory inputs in order to guide reaching,grasping, looking, and other behaviors via connectionswith premotor and motor cortex (for review see Cohenand Andersen, 2002; Jeannerod and Farne, 2003), andposterior parietal cortex in macaque monkeys hasmany features of functional organization in commonwith posterior parietal cortex in humans, a brief reviewof the results and conclusions from current studies ofconnections, neuron properties, and functional subdivi-sions in monkeys is useful.

One current scheme for subdividing posterior pari-etal cortex in macaque monkeys is shown in Figure 30.9(also see Preuss and Goldman Rakic, 1991; for an alter-native proposal see Seltzer and Pandya, 1980; Pandyaand Seltzer, 1982). The scheme includes the traditionalsubdivisions of areas 5a, 5b, 7a, and 7b as introducedby Brodmann and the Vogts, with the addition ofrecently defined intraparietal areas.

Area 5a (PE)

Area 5a is not uniform in histological structure,connections, and neuron types, but functional subdivi-sions have not yet been established. Subdivisions ofanterior parietal cortex, especially area 2, provide directsomatosensory inputs from both deep and cutaneousreceptors (Pons and Kaas, 1986). Major thalamic inputsare from the anterior pulvinar and the lateral posteriornucleus (see Yeterian and Pandya, 1985), nuclei withoutsignificant sensory inputs from the brainstem or spinalcord. However, a lateral portion of area 5 receives

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some input from the ventroposterior nucleus (Pons andKaas, 1985). Cortical projections include those to area 7,S2, motor and premotor cortex, limbic cortex, and partsof the superior temporal gyrus; callosal connectionsare largely between matched regions of area 5 (seeHyvarinen, 1982). Subcortical projections includethalamic nuclei, the basal ganglia, the pontine nuclei,and the spinal cord through the pyramidal tract. Neuronproperties include those related to both cutaneous anddeep receptors and to passive and especially activelimb movement (Iwamura and Tanaka, 1996). Neuronsare preferentially activated during graspingmovements.Receptive fields for neurons in area 5a are generallymuch larger than those in areas 1 and 2. Specific combi-nations of positions in several joints may be the mosteffective stimulus for many neurons (Hyvarinen, 1982).Many neurons in area 5a respond to ipsilateral as wellas contralateral stimulation, with receptive fields thatinclude the digits of both hands, and sometimes extendup onto the arm and even the trunk (Taoka et al., 1998).Some neurons have both somatosensory and visualreceptive fields (Iriki et al., 1996), and visual stimulimay modulate proprioceptive activity. Some neuronsin area 5a that were responsive to arm position whenthe arm was covered from view responded better toseeing the arm or even a fake arm in the correct position,but not better to a fake arm in the wrong position(Graziano et al., 2000). Finally, ablation of cortex of theintraparietal sulcus including area 5a interferes withthe ability to orient the hand correctly in grasping(Denny-Brown and Chambers, 1958). Overall, the resultssuggest that area 5a is involved in providing a mentalmodel of what the body is doing, and thereby guidingrelevant behavior such as reaching for objects.

Area 5b (PEc)

Area 5b appears to be largely somatosensory in func-tion, despite its position near the visual cortex. Majorcortical inputs are from area 5a, while outputs includeadjoining parietal cortex of the medial wall and partsof 7b as well as cortex caudal to S2 in the lateral fissure,and dorsal premotor cortex (Pandya and Seltzer, 1982;Marconi et al., 2001).

Area 7b (PF and PFG)

Area 7b also appears to be involved in the higher-order processing of somatosensory information(Andersen et al., 1997). Somatosensory inputs includethose from the anterior parietal cortex (Pons and Kaas,1986), secondary somatosensory areas (Disbrow et al.,2003) and other parts of posterior parietal cortex.Thalamic connections include the ventral lateral nucleusand the anterior pulvinar. Cortical projections includepre-motor and prefrontal areas of the frontal lobe,more caudal regions in posterior parietal cortex, and

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the superior temporal sulcus (Cavada and Goldman-Rakic, 1989; Lewis and Van Essen, 2000a). More recently,Gregoriou et al. (2006) provided further architectonicevidence for dividing 7b into an anterior half (PF) anda posterior half (PFG), and provided evidence that PFprojects densely to dorsal premotor cortex while PFGalso projects to the frontal eye field. Neurons respondto touching the skin, particularly on the head and facein anterior 7b and the hand and arm in posterior 7b (Lei-nonen, 1984; Krubitzer et al., 1995).

Area 7a (PG)

Area 7a is related to visual and visuomotor activities.The visual functions are reflected in both connectionpatterns and neuron properties. Visual inputs includethose from superior temporal cortex involved in pro-cessing visual motion information (see Maunsell andVan Essen, 1983). Other visual inputs are from adjacentdorsal portions of the pre-lunate gyrus (May andAndersen, 1986). Connections also include the cortexof the intraparietal sulcus, cortex of the medial wall,prefrontal cortex, multimodal and visual areas of thesuperior temporal sulcus, cortex of the lateral sulcusand especially dorsal premotor cortex (Cavada andGoldman-Rakic, 1989; Andersen et al., 1990; Gregoriouet al., 2006). The cortical region just caudal to 7a (PG)is even more involved in visual processing, and itprojects to cortex just anterior to dorsal premotor cortex.Other connections are with the medial pulvinar. Severalclasses of visual and visuomotor neurons have beendescribed (see Hyvarinen, 1982). Visual trackingneurons respond during the visual pursuit of targets.Another class of neurons is activated during fixationon a moving or stationary visual target. Some neuronsseem to be important to the visual guidance of reachingmovements with the hand. Many neurons respond tovisual stimuli, but these neurons respond poorly tovisual stimuli when monkeys are not attending andvisual responses are suppressed when gaze and atten-tion are directed to the stimulus (Steinmetz et al.,1994). The presence of neurons responding both tovisual stimuli and to visuomotor and reaching behaviorimplicates areas 7a in guiding eye and handmovements.

Areas of the Intraparietal Sulcus: AIP, LIP, CIP,VIP, MIP, and PIP

Cortex of the intraparietal sulcus is highly involved insensorimotor functions. Specifically, this cortex isinvolved in forming of intentions and cognitive plansfor specific types of movements (Andersen and Buneo,2002). Different subregions or areas of the intraparietalsulcus are involved in the planning of eye movements,grasping movements, reaching, and defensive forelimband head movements. Sensory guidance is based onsomatosensory, visual, and, to a lesser extent, auditory

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inputs. Important outputs are to motor and premotorareas of the frontal lobe. The cortex of the intraparietalsulcus of macaque monkeys has been divided intoa number of areas (Figure 30.9). Along the lateral(caudal) bank of the sulcus, the anterior intraparietalarea, AIP (Sakata and Taira, 1994), the lateral intraparie-tal area, LIP (Andersen et al., 1985), and the caudal inter-parietal area, CIP (Sakata and Taira, 1994) forma rostrocaudal sequence, with more rostral areas moredominated by somatosensory inputs, and more caudalareas by more direct visual inputs (see Stepniewskaet al., 2005). The fundus of the sulcus contains theventral intraparietal area, VIP (Maunsel and Van Essen,1983). The medial (rostral) back of the sulcus starts withpart of area 5a anteriorally, followed by the medial intra-parietal area, MIP (Eskandar and Assad, 1999), and theposterior parietal area, PIP (Sakata et al., 1998). TheMIP and PIP regions have been combined into a poste-rior parietal reach region, PPR, by Cohen and Andersen(2002).

AIP, the most anterior area of the lateral bank of theintraparietal sulcus, is important in planning and orga-nizing grasping movements of the hand (Gallese et al.,1994; Rizzolatti et al., 1997). The area is adjacent topart of area 5a on the medial bank of the sulcus that isalso involved in grasping (Iwamura and Tanaka, 1996;Padberg et al., 2007). More lateral cortex in area 7b isalso involved in grasping (Cohen and Andersen, 2002).A region similar to AIP in relative location, wheregrasping movements of the contralateral hand can beevoked by electrical stimulation with microelectrodes,has been identified in prosimian primates and NewWorld monkeys (Stepniewska et al., 2009a). AIP hasconnections with adjoining areas of cortex, includingarea 5a, area 2, S2, and PV of the lateral sulcus. Visualinputs include those from LIP, CIP, dorsal visual cortex,and inferior temporal cortex (Nakamura et al., 2001;Borra et al., 2008). Important outputs are to ventral pre-motor cortex, a motor area also important in handmove-ment control (Luppino et al., 1999). Neurons in AIPappear to code for hand movements that are specific tothe perceived task (Baumann et al., 2009). Graspingbehavior is abnormal after the inactivation of AIP(Gallese et al., 1994). Overall, AIP and adjoining regionsof cortex are involved in grasping and manipulatingobjects with the hand, and likely tool use in humans(Frey, 2008).

LIP, just caudal to AIP (Figure 30.9), is an areaprimarily devoted to the planning of eye movements(Andersen and Buneo, 2002), as well as a major sourceof visual information about object shape and positionto AIP (Janssen et al., 2008). Most neurons in LIPrespond to visual stimuli signaling an eye movement,and just before spontaneous eye movements to locationswithin the neuron’s receptive field (Shandlen and

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Newsome, 1996). Eye movements are evoked by electri-cal stimulation of neurons in LIP (Thier and Andersen,1998). Major projections are to the frontal eye fields,which are also concerned with eye movements (Huertaet al., 1987; Bullier et al., 1996). Somatosensory inputsto LIP come from other areas of posterior parietal cortexsuch as AIP. Responses to auditory signals for eye move-ments are found in some neurons (Grunewald et al.,1999). Visual inputs come from the middle temporalvisual area, MT, and other visual areas (Blatt et al.,1990). Overall, LIP has been implicated in the planningof saccadic eye movements, spatial attention, decisionmaking, and reward expectation (see Janssen et al.,2008).

VIP, in the depths of the intraparietal sulcus, adjoinsLIP. Most neurons respond to either visual stimuli orlight touch (Duhamel et al., 1998). The area seems tocontain matched representations of the body surfaceand visual space. Small foveal visual receptive fieldsrelated to neurons with small tactile receptive fields onthe muzzle and larger peripheral visual receptive fieldswere determined for neurons with larger receptive fieldson the side of the head. VIP may have a crude somato-topic organization with nearly all of the area devotedto the head. Somatosensory inputs arise from areas 1and 2, 5 and 7b, and S2 and nearby areas of the lateralsulcus (Lewis and Van Essen, 2000b). There also maybe inputs from vestibular cortex and auditory areas.Visual inputs are from visual areas of the dorsal stream(especially the middle temporal visual area) and LIP.Outputs include projections to the frontal eye field andadjoining portions of the frontal lobe, as well as theventral premotor area. Complex defensive movements,including eye closure, facial grimacing, and movementof the hand to protect the head, can be evoked by electri-cally stimulating neurons in VIP with microelectrodes(Cooke et al., 2003). VIP has been implicated in cross-modal (sensory) attention, but a major role appears tobe in the use of sensory information to form a motorplan to avoid harm via defensive movements.

MIP and PIP function together as a larger posteriorparietal reach (PPR) region dedicated to the planningof reaching movements (Andersen and Buneo, 2002).This cortex receives inputs from dorsal stream visualareas and other parts of posterior parietal cortex,and projects especially to dorsal premotor cortex(Blatt et al., 1990; Caminiti et al., 1998). Recentevidence suggests that neurons in PPR are not onlyinvolved in forming plans for reaching, but also inmonitoring the course of the movement in order tocorrect errors and perform a successful reach(Mulliken et al., 2008).

Finally, CIP, on the caudal part of the lateral bank ofthe intraparietal sulcus, appears to be largely involvedin higher-order visual processing, and not in

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somatosensory processing (see Tsutsui et al., 2003 forreview). CIP receives visual inputs from dorsal andventral stream visual areas, has connections with otherparts of posterior parietal cortex, and with prefrontalcortex. Neurons are sensitive to object texture, orienta-tion, and distance, and thus provide information thatcould guide various motor behaviors via interactionswith other areas of posterior parietal cortex.

Posterior Parietal Cortex Function in Humans

Concepts of posterior parietal cortex function inhumans are largely derived from the much discussedbehavioral changes that typically follow large lesions(for reviews, see Critchley, 1949; Denney-Brown andChambers, 1958; Mesulam, 1981, 1983; DeRenzi, 1982:Hyvarinen, 1982; see Chapter 28 for architecture). Inbrief, patients with posterior parietal lobe injury tendto neglect visual and tactile information coming fromvisual space or the body surface opposite the lesion(see Moscovitch and Behrmann, 1994; Pouget andDriver, 2000). The defect is most severe after lesions ofthe right hemisphere that is non-dominant for language.The defect may be profound, leading to bizarre symp-toms, or it may be quite mild, resulting in little notablechange in spontaneous behavior. Mild defects are typi-cally revealed by bilateral stimulation. The expectedresult is that the ipsilateral stimulus is preferentiallyattended, either immediately or after a series of trials.In more dramatic cases, there is a denial of the existenceof the contralateral (typically left) side of the body and ofobjects in the left side of the visual space. Patients mayfail to shave or dress the neglected side, and food onthe contralateral side of the plate may be uneaten. Thedefect can be characterized as a change in attention,because it is clearly not a result of a sensory impairment.More specifically, a unique aspect of the impairmentseems to be a difficulty in the ability to disengage atten-tion from a current focus and move that attention toa new focus in the contralateral world (Posner et al.,1984). Right-hemisphere damage produces a reluctanceor inability to redirect attention from the right visualfield to the left visual field, as well as a reluctance to shiftattention within the left visual field (Baynes et al., 1986).Other defects also occur (see Sirigu et al., 1996).

1. Errors may exist in localizing objects so that accuratepointing does not occur. Right and left may beconfused, and the patient may have difficulty inmoving from place to place.

2. Eye movement patterns are altered, and a reductionin spontaneous eye movements and trackingmovements may occur.

3. Errors in reaching into the contralateral hemifield arecommon. Targets may be missed by several inches. In

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addition, corrections of reach to displaced targetsduring reach are impaired during posterior parietalcortex inactivation with transcranial magneticstimulation (Desmarget et al., 1999).

4. Lesions of the right orminor hemisphere may producea defect in drawing even simple objects, such asa house, and in constructing simple models.Furthermore,during constructional tasks, bloodflow isincreased in posterior parietal cortex (Roland et al.,1980). Blood flow also increases in the superior parietalcortex and intraparietal sulcus of humans performingmental rotations of the hand (Bonda et al., 1995, 1996b).

5. Lesions, especially those involving the anterior half ofposterior parietal cortex, may producesomatosensory deficits. Reported changes includeimpairment in length discrimination, weightjudgment, shape discrimination, and limb positionsense (see Hyvarinen, 1982).

6. Difficulties may exist in performing symbolicgestures and pantomimes. This is attributed to aninability to access or store representations ofmovements adequately.

Even though posterior parietal cortex is not uniformin function, much of the region appears to relate to pre-motor planning in relation to eye movements and reach.Clearly, the anterior part of posterior parietal cortex ismore related to the somatosensory system, and theposterior part is more related to the visual system. Theconnections of posterior parietal cortex suggest thata motivational component depends on relationshipswith limbic cortex of the medial wall and perhaps theventral temporal lobe (see Mesulam, 1981). Connectionswith the frontal lobe and connections with subcorticalmotor structures such as the superior colliculus andbasal ganglia undoubtedly are important in initiatingbehavior. More specifically, Mountcastle (1975) hypothe-sized that posterior parietal cortex functions asa “command” center for body movements. Finally, thefunctional asymmetry of posterior parietal cortex inhumans can be explained if the right hemispherecontains the neural substrate for attending to both sidesof space, though predominantly contralateral space,while the left hemisphere is almost exclusively con-cerned with contralateral space (Mesulam, 1981). Thus,unilateral lesions of the left hemisphere are partiallycompensated by the functions of the right hemisphere,but the reverse does not hold. This difference may relateto the specialization of the left hemisphere for language.As posterior parietal cortex is a large region, even inproportion to the rest of the brain, in humans, it isunlikely that all functional subdivisions found inhumans are also present in monkeys. Comparativestudies suggest that at least some of the intraparietalareas of monkeys have been retained in humans, likely

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including LIP, AIP, VIP, PPR, and CIP, but other func-tionally defined regions that are not present in monkeysappear to be present in humans (Orban et al., 2006).

Although the pathways are not known, primaryvisual cortex appears to be involved in tactile discrimi-nations, such as Braille reading, in humans (e.g., Sadatoet al., 1996; Zangaladze et al., 1999; Merabet et al., 2004).Other visual areas may also be involved in somatosen-sory discrimination. Multisynaptic pathways likelyinvolve posterior parietal cortex.

SOMATOSENSORY CORTEX OF THEMEDIAL WALL: THE SUPPLEMENTARY

SENSORY AREA AND CINGULATECORTEX

The organization of the medial parietal cortex is notwell understood. Penfield and Jasper (1954) postulatedthe existence of a supplementary sensory area, as ananalogy to the supplementary motor area, on the medialwall of the cerebral hemisphere where electrical stimula-tion evoked sensations from the contralateral leg, arm,and face. Later, Woolsey et al. (1979) reported in a singlepatient that sensations were obtained from the arm orleg after electrical stimulation of sites on the medialwall. There have been only a few experimental studiesin monkeys that relate to the existence or organizationof a supplementary sensory area, SSA (see Murray andCoulter, 1982, for review). In macaque monkeys,neurons on the medial wall respond to somatosensorystimuli, and there is some suggestion of anterior sitesrelating to the lower body and posterior sites relatingto the upper body. These neurons have large receptivefields and appear to have inputs related to both skinand deep receptors. Major connections of the SSA regioninclude those with area 2, the S2 and PVregions, parts ofthe insula, parts of area 7 and 5, cingulate cortex, anddorsal premotor and prefrontal areas (Morecraft et al.,2004). Other connections of medial parietal cortex arewith the lateral posterior nucleus of the thalamus. Thereis also evidence for projections to the spinal cord andeven sparse projections to primary motor cortex (seeWu et al., 2000). The connections of posterior parietalcortex of the medial wall to adjoining sensory and motorregions of cingulate cortex may function to providemotivation and attention to behavioral plans (Mesulam,1981; Chapter 25).

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