Cortical fields participating in spatial frequency and orientation discrimination: Functinal anatomy by positron emission tomography

Human Brain Mapping 3:133-152(1995)

Cortical Fields Participating in Spatial Frequency and Orientation Discrimination: Functional Anatomy by Positron Emission Tomography

Balizs Gulyis and Per E. Roland

Division of Human Brain Research, Department of Neuroscience, Karolinska Institute, S-171 77 Stockholm, Sweden

Abstract: With the purpose of localising those anatomical structures participating in the discrimination of spatial frequencies and orientations of gratings, we measured regional cerebral blood flow (rCBF) changes with positron emission tomography (PET) and 150-butanol as tracer in ten healthy young male volunteers. The subjects performed two-alternative forced-choice discriminations of pairs of squarewave gratings regarding their spatial frequencies or orientations (spatial frequency and orientation tasks) or pairs of a grating and a two-dimensional random noise pattern regarding the presence or absence of grating pattern (reference task). In both the spatial frequency and orientation discrimination tasks a widely distributed network of functional fields is activated in the occipital, temporal, parietal, and frontal cortices and in the cerebellum. Spatial frequency discrimination required the activation of more cortical fields than orientation discrimination, and whereas the total volume of activated fields in the temporal and frontal lobes were similar in the two tasks, the volumes of activated fields in the occipital lobes as well as in the parietal lobes were about two and a half times larger in spatial frequency discrimination than in orientation discrimination. The two networks of cortical fields were partially overlapping in the two tasks. The findings indicate that the discrimination of spatial frequency and orientation signals engages functional networks of cortical fields widely distributed in the human brain. Whereas both the occipito-temporal and occipito-parietal visual pathways are involved in both tasks, the processing and analysis of spatial frequency information activates occipital and parietal lobe regions more extensively than those of orientation information. o 1995 wiley-Liss, Inc.

Key words: human brain, vision, regional cerebral blood flow (rCBF), visual cues, discrimination, cortical networks

INTRODUCTION

Single unit studies in cats and monkeys have dem- onstrated that cells in early levels of the visual pathways exhibit varying sensitivity for different visual

Received for publication June 20, 1994; revision accepted July 19, 1995. Address reprint requests to Balazs Gulyas M.D., Ph.D., Division of Human Brain Research, Department of Neuroscience, Karolinska Institute, S-171 77 Stockholm, Sweden.

cues, such as colour, motion, or disparity {Van Essen and Maunsell, 1983; Burkhalter and Van Essen, 1986; Maunsell and Newsome, 1987; Livingstone and Hubel, 1987; De Yoe and Van Essen, 2988; Zelu and Shipp, 1988; Felleman and Van Essen, 19911. Orientation and spatial frequency are fundamental cues for encoding visual images {De Valois and De Valois, 19881, and both are among those visual features for which cells are tuned in the primary visual cortical area and its neighbouring extrastriate cortex.

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In cats and monkeys, orientation and spatial frequency sensitivity are well-known characteristics of single cells at already low levels of the visual pathways. Cells in the lateral geniculate nucleus (LGN) display clear sensitivity for spatial frequencies [Wiesel and Hubel, 1966; Dreher et al., 1976; Derrington and Lennie, 1982,1984; Shapley and Lennie, 19851 though with some conspicious exceptions they are not sensitive for different stimulus orientations. In the striate cortex [Hubel and Wiesel, 1977; Hammond, 1978; De Valois et al., 1979, 1982; Dow and Gouras, 1974; Albrecht et al., 1981; Campbell et al., 19691 as well as in the early extrastriate visual cortical areas [Baizer, 1982; Burkhalter et al., 1986; Tootell et al., 1981, 1988; Baizer et al., 1977; Albright, 1984; Felleman and Van Essen, 1987; Gizzi et al., 1983; Motter, 19921, most cells show orientation sensitivity and spatial frequency sensitivity. Lesions in early levels of the visual cortical pathways may cause severe deficits in orientation discrimination [Crook and Eysel, 19921 as well as in spatial acuity measurements [Orban et al., 1990; Pasternak and Maunsell, 19921.

Similarly to cats and monkeys, human observers are also able to discriminate even very small differences in spatial frequency [Burbeck and Regan, 19831 or orientation [Orban et al., 1984; Lindblom and Westheimer, 1992). The ability to discriminate spatial frequency and orientation differences is assumed to be based on the spatial frequency and orientation tuning characteristics of populations of single cells in the visual system [Vogels, 19901. Nevertheless, as most single cells in the primary and secondary visual areas are tuned to a narrow range of orientation or spatial frequency, the computation of differences in orientation or spatial frequency requires a number of connections between the tuned units, and therefore it is reasonable to assume that the discrimination of differences either is a computation at the neuronal population level which requires a relatively large number of neuronal assem- blies and robust interconnections between them or it takes place at higher levels in the visual system (remote computation fields) than the detection of orientations or spatial frequencies itself.

Furthermore, the orientation of gratings with different spatial frequencies can be discriminated as accurately as that of gratings with fixed spatial frequency. On the other hand, the spatial frequency discrimination of gratings with various orientations can be done as accurately as the spatial frequency discrimination of gratings with fixed orientation [Burbeck and Regan, 19831. These observations would entail the conclusion that the generation of orientation-invariant spatial frequency signals requires the activity of numerous

cells sensitive to different spatial frequencies at various orientations, and, conversely, the generation of spatial frequency-invariant orientation signals requires single cells tuned for various orientations at a large number different spatial frequencies [Vogels et al., 19881. This reasoning, consequently, entails that cue-invariant discrimination of a given visual signal takes place at a higher level than the operations directly related to the detection of the given visual signal. These arguments lead to a working hypothesis related to the discrimination of spatial frequencies and orientations, namely, that different functional networks of activated cortical fields underlie the discrimination of spatial frequency and orientation signals.

Keeping in mind these considerations, we set out to map in the human brain those regions selectively activated during the discrimination of orientations and spatial frequencies of grating stimuli. As cerebral blood flow is known to be a faithful indicator of cerebral metabolism, we used positron emission tomography (PET) measurements with a freely diffusible flow tracer, 150-butanol, to measure regional cerebral blood flow (rCBF) changes in the human brain in normal volunteers while the subjects were performing three two-alternative forced-choice visual discrimination tasks.

MATERIALS AND METHODS

Subjects

Ten healthy male volunteers (aged 2446 years) participated in the present study. The subjects were fully informed about the objectives, details, and risks of the experiment and they gave a written consent, in agreement with the Helsinki Declaration and the OPRR [1989] reports. All the volunteers were psycho- physically naive subjects. Although they were informed about the main purpose and detailed technical aspects of the experiment weeks before it, they were not given a description of the psychophysical tasks until an hour prior to the experiment. The study was approved by the Ethical, Radiation Safety, and Mag- netic Resonance Imaging Committees of the Karolin- ska Hospital. All subjects were right-handed, accord- ing to the Edinburgh Handedness Inventory [Oldfield, 19711. The subjects denied any previous medical, neurological or psychiatric history and all had normal or corrected-to-normal visual acuity. None of them had any manifest or hidden colour vision and visual field deficit. Electro-oculographic (EOG), electroen- cephalographic (EEG), and electromyelographic (EMG) measurements (movements of the right thumb), as

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well as the arterial PaOz and PaCOz levels were regularly monitored during the experiments.

Brain scanning procedures

Each subject was given an individually moulded plastic head fixation helmet [Greitz et al., 1980; Berg- strom et al., 19811 which held the head in an identical position during the magnetic resonance imaging (MRI) and PET scanning procedures. In the first step, the subjects underwent a high-resolution (1 Tesla) MRI (Siemens Magnetom), resulting in 19 transaxial, 3 parasagittal, and 3 coronal slices (both proton- enhanced and TZweighted images; spatial resolution, 0.5 mm; slice thickness, 4 mm; inter-slice distance, 6.50 mm; spin echo, TR 2,300 msec, TE 25 msec, and 90 msec). The MR images were used to guide the head positioning in the PET scanner. With the help of a computerised brain atlas system, the MRI and PET slices were placed in register and the MR images were used to standardise individual brains, as well as to localise anatomical structures underlying functional changes in the individual brains (see later).

The method of measuring rCBF with PET was described in great detail in a recent publication [Ro- land et al., 19931; therefore only a short description is needed here. In brief, the PET measurements were made in wobbling mode on a Scanditronix 2048-15B positron camera with 4.5 mm in-plane resolution and 6.5 mm inter-slice distance [Litton et al., 1990; Evans et al., 19911. The effective image resolution in the final statistical images was 3.8 mm along the x axis and 4.5 mm along the y axis [Roland et al., 19931. The camera produced 15 transaxial slices of the brain. 150-butanol was used as tracer [Berridge et al., 1990,19911, which was given in a bolus injection [65 k 5 mCi dissolved in 7 ml solution of physiological saline (90 volume %) and ethanol (10 volume %)] before each test in the right cubital vein. In the emission scans, data were obtained for a total of 100 sec in 20 sequential scans, each lasting for 5 sec, but only the first 80 sec was used for the actual computation of rCBF. Data acquisition and stimulus presentation started simultaneously.

Under local anaesthesia, the left brachial artery was cannulated and the arterial radiotracer concentration was continuously monitored during the PET measurements with an automatic sampling device [Eriksson et al., 19881. The sampling velocity was 2.5 ml/min. The time shift between the arterial radiotracer concentration and the global uptake curve from the positron camera was calculated as described earlier [Roland et al., 19871. Arterial PaOz and PaC02 concentrations were measured regularly (30 sec and 180 sec after the

tracer injection). Differences in rCBF between PET measurements of test and reference tasks due to differences in PaCOz were corrected to the level of the reference condition [Olesen et al., 1971; Roland et al., 19871. In each experiment, due to the perfect head fixation, only one transmission scan was obtained in the same image planes as those of the emission scans, and it was used to correct for attenuation in each emission scan. The reconstruction filter in both the transmission and emission scans was a 4 mm Hanning- filter [Roland et al., 19931. Images of rCBF (ml/min/100 g brain tissue) were calculated [Koeppe et al., 1985; Roland et al., 19871.

Electrophysiological measurements

The EEG was recorded with a Siemens Mingograph using 100 x amplification. Needle electrodes were placed in the scalp at five standard positions: F3, F4, P3, P4, and Cz. In addition, one ground electrode was fixed above the left clavicula. The recordings were analysed off-line for the proportion of different frequency domains during the PET measurements.

For the recording of the EOG, two monitoring channels of the same instrument was used. Two-two skm electrodes were located above the lateral and inferior edges of the orbita on both sides. As measured in preliminary tests, the recordings give information about the frequency, amplitude, and movement trajec- tory of saccadic eye movements equal to or larger than 2" in amplitude. Fine eye movements smaller than 2" in amplitude cannot be monitored with precision with the present method.

The EMG was recorded with two skin electrodes placed above the right m. extensor pollicis in order to monitor thumb movements. For the recording, the same EEG apparatus was used.

Visual stimulation

PET measurements were taken while the subjects performed a reference task and two visual discrimination tasks: an orientation and a spatial frequency discrimination task. The tasks were randomly inter- leaved with each other in the various subjects. During the investigations, the subjects were comfortably placed in a supine position on the camera bed. The ears were covered by the helmet. With the exception of the ambient noise of the mechanical parts of the projectors, the EEG and the arterial pump, there was no noise in the room. The room temperature was kept at 23°C. The investigation was not disturbed by any movements or speech by the personnel; all control activities of the experiment took place outside the

4 Gulyas and Roland 4

Stimulus 1 Interval 1 Stimulus 2 Interval 2 Signal Response interval

120 msec 720 msec 120 msec 720 msec 100 msec 2000 msec

Reference

Orientation

Spatial frequency

Figure I . Stimulus paradigms used in the three tests.

camera room in a control room. The subjects were not allowed to move or activate their muscles, to say anything, or to change the respiratory rhythms after the injection, except raising their right thumbs as an indica- tion of their responses. The rest of the visual field outside the projection screen was obscured by black drapes.

The stimulus patterns were projected by a computer- controlled projector system (Simda projectors) onto a double-polarised projection screen facing the subjects at a distance of 86 cm from their eyes (1" = 1.5 cm). The stimulus patterns were circular and 10" in diameter. The average luminance value on the screen during stimulus presentation and during the interstimulus interval was 13.5 cd/m2. The stimulus presentation format was identical in the tasks: the stimuli, which were presented for 120 msec, came in pairs, with a 720 msec inter-stimulus interval in between. The second stimulus was followed by a 720 msec interval, then a 100 msec long response signal (an illuminated circle of 1" diameter), and, finally, a 2,000 msec long response interval (Fig. 1). In the reference task a stimulus pair was

composed of a random dot pattern and a grating. The spatial frequency of the random dot pattern and the grating, as well as the orientation of the grating pattern were different in each stimulus pair. The subject had to indicate after the response signal if the first member of the stimulus pair was the grating. In the orientation task a pair of two gratings were presented. The gratings were of the same spatial frequencies but of different orientations. The subject had to indicate if the orientation of the first grating in the stimulus pair was closer to the vertical meridian. In the spatial frequency task again two gratings were presented. The orientation of the gratings was identical, whereas their spatial frequencies differed. The subject had to indicate if the spatial frequency of the first pattern was higher than that of the second one.

Visual stimuli

The stimuli were computer-generated random dot patterns or rectangular grating patterns. The spatial

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frequencies for both the random dot and grating patterns ranged between 0.42 and 4.6 cycldegree in equal steps on a log scale; the orientations of the grating patterns covered 0"-360" in 15" steps. Against their fundamentally different appearance, the physical characteristics of the gratings and random dot patterns, important for psychophysical testing, were closely matched. All stimulus patterns (1) had the very same geometrical complexity measures (Euler num- bers); (2) contained the same amount of light and dark surfaces; (3) had the same average luminance value (13.5 cd/m2); 4) had the same internal luminance contrast [Michaelson contrast, c = ([Imax - Iminl/ [I,,, + I X 100) = 82 +- 21; (5) had the same edge- lengths (in relative terms: 1.00:0.97, gratings:random dot patterns of identical spatial frequencies, respectively); (6) had the same stimulus energies [Roland and Mortensen, 19871; and (7) practically contained all orientations (though this latter condition was not fulfilled ideally: within one stimulus pair the random dot pattern contained all possible orientations whereas the grating had only one orientation; however, since the orientation of the individual gratings varied between 0" and 180", during the whole stimulation period practically all orientations were presented).

Logic of functional subtractions

As the above task design focused on the most elementary discrimination processes involved in the processing and analysis of spatial frequencies and orientations, the tasks clearly involved different specific components and did not necessarily involve the very same aspecific components (see Discussion). Op- timising a task design is always a trade-off, which puts more emphasis on certain aspects of the task and less on other aspects. In the present case, the role of the reference task was double: to engage the brain with a simple and fundamental grating versus non-grating discrimination task (discrimination component), while at the same time to stimulate neuronal populations in the brain involved in the processing of spatial frequency and orientation information (spatial frequency and orientation components). Because during the stimulation the correct answer had to be kept in mind until the response signal was shown, it also contained a short-term (verbal non-visual memory) component, as well as a memory component related to the task instructions, just as the other two tasks did. As the cue physical characteristics of all stimuli were closely matched, during the orientation and spatial frequency discrimination tasks those neuronal populations processing the elementary aspects of the stimuli were

expected to be annulled after the "specific task- reference task" subtractions, and the specific aspects (spatial frequency discrimination, orientation discrimination) were expected to be highlighted. However, there was a clear difference with respect to a visual short-term memory component between the reference task and the other two tasks: whereas the reference task could be solved by looking at the first member of the stimulus pair, the spatial frequency and orientation tasks could only be solved by keeping in shorf- term visual memory the appearance of the first member of the stimulus pair at least until the onset of the second member of the pair, when the discrimination could have been made, i.e., in addition to the discrimination components, a visual short-term memory component was also present in the orientation and spatial frequency tasks (see Discussion).

Data processing and analysis

All individual MR and rCBF images were processed in the computerised human brain atlas (HBA) system of our group [Roland et al., 1994; Roland and Zilles, 19941. First the individual MR images were adjusted in both size and shape to the standard HBA brain contours, affine and non-affine non-linear operations. As the PET images do not g v e us precise anatomical information on the individual brains, and as the corresponding MR and PET images were put in register, the standardisation parameters of the corresponding MR images were used in standardising the individual PET images. By using the HBA procedures, standardised individual rCBF images and, by means of pixel-by-pixel subtractions, ArCBF (difference between a specific task and its reference task) images were created. The voxel size was 1 x 1 x 1 mm. The accuracy and precision of the HBA have been vali- dated earlier [Roland et al., 19941. The position of the original 15 image slices in relation to the cardinal AC-PC plane and the contours of the brain is shown in Figure 2.

The anatomically standardised pictures were analysed for local field activations occurring in the brain as clusters of voxels having a high signal-to-noise ratio. Statistical analysis of the cluster detection was described extensively in a recent report [Roland et al., 19931; therefore only a brief description is needed here. From the individual ArCBF images, mean ArCBF images (ArCBFAVE = CArCBF/number of subjects) as well as variance images and descriptive Student's t images (ArCBFAVE/dvariance/dnumber of subjects) were calculated. Voxels in the image (volume, 1 mm3) having t-values 2 2.22 were considered to be clustered

137 4


7 2 0

Figure 2.

-1 03

Positioning of the original 15 image slices obtained by the PET camera with respect to the Talairach proportional co-ordinate system [Talairach and Tournoux, 19881. AC, anterior cornmissure; PC, posterior commissure. The horizontal line intersecting the anterior and posterior comrnissures is the AC-PC line, the main reference axis of the Talairach coordinate system. The retroflexion of the image plane is 8.5" with respect to the AC-PC line. The image planes of the PET scans are drawn as oblique solid lines. The

if they were attached by side, edge, or corner. On the basis of an analysis of false-positive clusters with high t-values [Roland et al., 19931, it was decided to reject the hypothesis that all clusters of size 350 and above belong to the distribution of false positives. The probability of finding one false positive cluster of size 350 and above in the whole brain is ~ 0 . 0 6 , whereas the probability of finding two or three false positive clusters is i 0.01. The descriptive f-image was thresh- olded to comprise only clusters of voxel size 350 or more with voxel values f 2 2.22. The remaining voxel values were set to zero. The resulting image is called a cluster image. In this image all clusters of size 350 and above are shown as regions of significantly changed rCBF. In Tables 111 and IV the volumes of regions (together with levels of activation inside the region) are shown.

The activation fields in which there were significant changes in rCBF were localised in relation to the sulci and gyri of the computerised brain atlas as well as those of the reformatted mean MRI. The relationship between the stereotactic coordinates of our HBA and the Talairach and Tournoux [1988] atlas is very close,

most caudal slice is numbered I , and the top slice is the 15th. The orientation of the image planes of the MR scans is identical with that of the PET scans; however, the spacing of the MR image planes is different (I mm inter-slice distance, covering 128 rnrn). The figures on the left and lower sides of the Talairach grid indicate the distances in rnrn from the AC-PC line and the AC in the standard brain of the Human Brain Atlas [Roland et at., 19941; lettering along the upper and right sides represents labels of the proportional grid,

as has been evaluated in an earlier study [Roland et al., 19941. The mean rCBF change (m1/100 g/min) and the mean volume of rCBF change (mm3) were calculated by voxel-by-voxel analysis of regions in the mean subtraction CBF images, which had been identified from corresponding regions of significant change in cluster images. Since all cluster images were in the same standard anatomical format, if we multiplied one image by another image we could demonstrate if fields of activation present during orientation and

u

spatial frequency discrimination overlapped in 1 brain.

RESULTS

Physiological and response parameters during stimulation

Physiological parameters measured during the tac " including the mean degree of a-blockade in the EEG, eye movement frequencies, arterial PaOz and PaCO, levels, and global CBF values are displayed in Table I. All the tasks were accompanied by about the same

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TABLE I. Physiological parameters measured during the tasks

Eye Mean degree movement PaCOz P a 0 of a-blockade frequency level level gCBF

Task (%I ( H 4 W a f (kPa) (rn1/100 g/min)

Reference 93.2 f 1.4 0.46 * 0.06 5.77 f 0.45 12.29 2 1.74 48.86 ? 3.45 Orientation 95.3 + 2.3 0.45 2 0.03 5.77 ? 0.41 12.49 + 1.97 47.74 f 4.67 Spatial frequency 91.9 ? 2.4 0.46 * 0.04 5.76 + 0.37 12.10 f 1.27 49.14 f 4.46

-

percentage of a-blockade in all leads in the EEG and the same amount of eye movements. Amplitude analysis of the EOG signals indicated that the distribution of saccadic and pursuit eye movements was not different between the tasks. There was no significant difference between the EEG measurements and the eye movement frequencies during the different tasks. Similarly, there was no significant difference between the tasks with respect to PaC0, and PaO, levels, nor was there a significant difference in the gCBF values between the tasks. Performance levels and response latencies were closely matched, and there were no significant differences between them (t-test, two-tailed, P I 0.05). It is, however, worth noting here that, due to the task design, there was a faultless performance in the reference task, whereas it was not so in the other two tasks (Table 11).

rCBF measurements and localisation of activity

Using the criteria described in Materials and Meth- ods, regions of activity were determined in the brain during the different tasks. In the subtraction, the reference task was subtracted from the spatial frequency and orientation tasks to yield subtraction images exhibiting pure modality-specific regions of activation. The delineated regions, their location in the standard stereotactic Talairach space, their volume, the mean t-value, and rCBF changes within the volumes (in absolute values of blood flow as well as in

percentage of changes with respect to the reference state) are displayed in Tables I11 and IV.

Regions involved in spatial frequency

Regions activated by the discrimination of spatial frequencies of gratings were relatively more widespread in the cortex than those activated by orientation discrimination (Table 111). In this case, compared with orientation discrimination, more activated fields were present in the occipital lobe. The activated fields were located in the right cuneus, in the superior and inferior occipital gyri in both sides, and in the fundus of the right occipito-temporal sulcus. The total volume of occipital fields activated during orientation discrimination occupied was less than those activated during spatial frequency discrimination. Fields in the temporal lobe were present in the right superior temporal gyrus, the left middle temporal gyrus, the right inferior temporal gyrus, the right fusiform gyrus, and the right hippocampus. Fields in the parietal lobe were numerous and widespread; they were present bilaterally in the inferior parietal lobules, the postcentral gyri, and the precuneus, as well as in the left cingulate gyrus, the left angular gyrus, and the medial bank of the right intraparietal sulcus. There was a relatively large number of fields (eight) present in the frontal lobes, predominantly in the left side (superior frontal

TABLE II. Performance levels and response latencies between the tasks [Performance levels in Yo (k I SD), latencies in msec ( 2 I SD)]

Overall Correct False Correct performance Response

Task hit Miss alarm rejection level latency

Reference 100 0 0 100 100 616 2 228 Spatial frequency 97 f 5 3 f 5 4 +- 7 96 ? 7 96 2 6 664 & 183 Orientation 9 3 + 9 7 + 9 1 2 2 6 8 8 k 6 91 2 8 602 2 184

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TABLE 111. Activated fields during spatial frequency discrimination

HBA coordinates”

% change (mm) Volume Mean ArCBFAVE Region x y z (mm3) t-value (ml/100 g/min) (test-reference)

Occipital Calcarine sulcus

and cuneus R Superior

occipital gyrus R

occipital gyrus L

Inferior occipital gyrus R

Inferior occipital gyrus L

Occipito-temporal sulcus (fundus) R

Superior

Parietal Postcentral

gyrus L Postcentral

gyrus R Precuneus R Precuneus R Cingulate gyrus

(mid) L Cingulate gyrus

(mid) L Angular gyrus L Intraparietal

sulcus (medial bank) R

Posterior inferior parietal lobule R

Posterior inferior parietal lobule R

Posterior inferior parietal lobule L

7

31

- 29

28

-31

41

- 32

54 1

12

-1

-4 - 59

23

45

54

- 44

- 82

67

- 68

- 87

-81

- 67

- 31

-15 - 67 -56

- 30

-19 - 38

- 57

- 56

- 38

- 44

-1

28

40

12

-9

-9

49

15 35 24

33

50 26

39

43

41

48

837

368

401

359

460

828

377

454 474 646

362

703 368

368

651

71 1

992

2.92

3.11

2.70

3.34

2.96

3.19

2.85

2.93 2.87 2.86

2.68

2.65 2.91

3.05

3.08

3.09

3.08

9.23

8.71

8.63

9.89

9.72

10.22

6.98

10.09 10.16 9.23

8.31

7.99 7.05

7.63

7.23

8.72

8.38

16.89

17.84

17.94

22.76

21.81

23.17

16.61

16.85 16.49 17.54

12.79

14.22 11.77

20.33

14.21

17.07

16.80

gyri, middle frontal gyri, precentral gyrus), whereas only two fields were found in the right prefrontal cortex (orbitofrontal part of the superior frontal gyrus, and anterior part of the cingulate gyrus). Activations were also present in the left insula, right caudate nucleus, left thalamus, and cerebellum (left hemisphere) (Figure 3.)

Regions involved in orientation discrimination

During orientation discrimination only three fields were present in the occipital lobe, and there was no activation in the striate cortex (as defined by another PET study in our laboratory [Roland and Gulyas, 1995]), indicating that by way of subtracting the

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TABLE 111. Activated fields during spatial frequency discrimination (continued)

HBA coordinatesa

(mm) Volume Mean ArCBFAVE % change Region x y z (mm3) t-value (m1/100 g/min) (test-reference)

Temporal Superior tem-

poral gyrus R Middle tem-

poral gyrus L Middle tem-

poral gyrus L Inferior tem-

poral gyms R Fusifonn gyrus R Hippocampus R

Superior frontal

Superior frontal

Superior frontal gyrus (orbitofrontal part) R

gyrus L

gyrus L

Frontal

gyrus L

gyms L

Middle frontal

Middle frontal

Middle frontal

Cingulate gyrus (ant.) R

Precentral gyrus L

gyrus L

Insula Insula L

Cerebellum Cerebellum L

Subcortical Thalamus L Caudate

nucleus R

57 -47 17 427 2.91 9.80 18.07

-51 -41 -14 518 2.96 8.64 21.31

- 59 -23 -6 1234 3.42 10.20 21.64

52 35 22

-20 -17 1284 2.99 -42 -12 658 3.05 -36 -6 497 3.31

8.18 7.58

10.10

18.86 20.96 23.29

- 14

- 10

1 58 413 3.21

26 54 526 3.37

7.12

7.26

14.57

15.91

28

- 25

-26

-40

7

-39

38 -7 398 2.94

27 -8 507 2.72

56 1 1544 3.06

39 21 1650 3.00

50 -5 907 3.21

-6 56 423 3.08

9.75

9.15

9.34

9.78

9.10

7.92

23.16

20.10

24.05

19.26

22.19

14.02

- 36 8 8 605 2.77 12.20 19.60

-8 -49 -4 350 2.66 10.82 26.73

-15

12

-15 14 358 2.77

18 5 388 2.86

11.63

9.21

22.37

18.07

a About the relationship between HBA coordinates and Talairach coordinates, see last paragraph in Materials and Methods.

orientation and reference tasks the striate cortex activations annulled each other. The activated fields were present in the right lingual gyrus as well as in the left inferior and lateral occipital gyri. There were six fields activated in the temporal lobes: bilaterally in the inferior and middle temporal gyri and in the right fusiform gyrus. Activation in the parietal lobe was

restricted to two fields in the left hemisphere (angular gyrus and the medial bank of the intraparietal sulcus) and two fields in the right hemisphere (inferior parietal lobule and posterior superior parietal lobule). The prefrontal activations included two symmetrically located fields in the inferior frontal gyri, fields in both superior and inferior frontal gyri, a field in the left

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TABLE IV. Activated fields during orientation discrimination

HBA coordinatesa

Volume Mean ArCBFAVE % change (mm)

Region x y z (mm3) t-value (m1/100 g/min) (test-reference)

Occipital Lateral occipital

gyrus L -26 -82 11 440 3.03 8.45 22.28 Inferior occipital

gyrus L -18 -84 -11 352 2.82 9.65 18.79 LingualgyrusR 30 -52 -19 517 3.08 10.92 21.59

Inferior tem- poralgyrusL -52 -17 -18 359 2.64 10.51 25.75

Inferior tem- poralgyrusR 46 -63 -12 898 2.87 9.81 21.72

Middle tem- poralgyrusL -63 -25 -7 1066 2.92 11.01 26.71

Middle tem- poralgyrusL -52 -42 -15 480 2.73 9.84 23.41

Middle tem- poralgyrus R 55 -44 4 541 3.06 9.06 18.86

FusiformgymsR 39 -42 -15 488 2.64 10.65 29.06

AngulargyrusR 53 -41 27 630 2.92 8.83 16.30 Intraparietal

Temporal

Parietal

sulcus (medial bank) R 26 -62 37 402 3.03 8.57 18.29

Posterior inferior parietal lobule L -43 -41 45 473 2.83 8.65 16.87

Posterior superior parietal lobule L -37 -61 40 879 3.14 8.97 18.33

"bout the relationship between HBA coordinates and Talairach coordinates, see last paragraph in Materials and Methods.

cingulate gyrus, and one in the right precentral sulcus. Finally, activation was also present in the left cerebellar hemisphere. (Table 4 and Figure 3.)

Distribution of fields in the brain

In Tables I11 and IV fields of ddferent sizes are listed. The probabdity that these are false-positive activations declines rapidly with field size. For example, a field of 400 rnm3 will have a P < 0.2 of being false positive, whereas a field of size 500 mm3 will have a P < 0.01 of being false positive [Roland et al., 19931. If all listed fields in Tables I11 and IV are regarded as activations, we can calculate their number and the total volume of cortex activated for the spatial frequency and orientation discrimination tasks. Thus, the risk of including one small field of 350 m3 having a probability of 0.5 of being a false-positive activa-

tion will only marginally affect the estimate of the total volume of cortex activated during the tasks.

Keeping in mind these assumptions, we made an attempt to estimate the relative size of the activated cortical fields in terms of cortical grey matter in various parts of the cortex. Assuming an average brain surface (cerebral cortex, 1.680 cm2; cerebellar cortex, 450 cm2) and average thickness of cortex (cerebral cortex, 2.2 mm; cerebellar cortex, 0.7 mm) [Blinkov and Glezer, 19671, we estimated the volume of the whole cerebral and cerebellar cortex involved in the modality-specific activations in the three tasks. The fields activated in the spatial frequency task occupied larger volumes (20,950 mm3) than those activated in the orientation task (13,772 mm3). In both tasks relatively few activations were present in the occipital lobes (9.6 and 15.5%

+ Spatial Frequency and Orientation Discrimination

TABLE IV. Activated fields during orientation discrimination (continued)

HBA coordinatesa

Volume Mean ArCBFAVE % change (mm) Region x y z (mm3) t-value (m1/100 g/min) (test-reference)

Frontal Superior frontal

gyrus (orbitofrontal part) R

Superior frontal gyrus L

Middle frontal gyrus L

Middle frontal gyrus R

Inferior frontal gyrus L

Inferior frontal gyrus R

Inferior frontal gyrus L

Cingulate gyrus L

Precentral sulcus R

Cerebellum Cerebellum L

6 45 -10

-14 28 48

-44 42 7

41 27 33

-53 6 36

44 4 34

-34 3 37

-11 35 25

32 -19 46

-7 -50 -14

828

1144

71 1

1113

443

445

669

483

411

785

2.95

2.78

3.00

2.97

2.88

2.71

2.99

3.02

2.90

3.02

9.69

8.39

9.79

9.46

8.36

9.38

9.63

9.92

6.95

11.10

23.59

19.61

20.41

16.59

18.15

16.66

19.32

27.43

18.92

25.91

a About the relationship between HBA coordinates and Talairach coordinates, see last paragraph in Materials and Methods.

of the volume of all activated fields, orientation and spatial frequency, respectively), whereas most activations were present in the frontal lobes (45.3 and 30.3% of the volume of all activated fields, respectively). In the orientation task a somewhat larger proportion of the volume of all activated fields was present in the temporal lobes (27.8% of all activations) than in the spatial frequency task (22.1% of all activations); however, in absolute terms the volume of activation was smaller in the orientation task (3,832 mm3) than in the spatial frequency task (4,618 mm3). On the other hand, in the parietal lobes the spatial frequency task clearly resulted in more voluminous activations than the orientation task. (Of all activated fields 29.2% were in the parietal lobe in the spatial frequency task as compared with only 17.3% in the orientation task; this was even more accentuated in absolute volume measures, for which 6,106 mm3 was the field volume in the spatial frequency task versus 2,384 mm3 in the orientation task.) The spatial frequency task caused more activation in the cerebral cortex (5.67% of the whole cerebral cortex was activated) than the orientation task (3.70%) (Table V.)

Spatial overlap of the activated fields present in both tasks

To determine the regions activated by both spatial frequency and orientation discrimination, we located field overlaps between the two tasks. As in this case the cluster images are multiplied, the resulting field overlaps can be smaller than the statistically accept- able minimum clusters in a cluster-image. Field overlaps over 100 mm3 and present in the two different tasks are listed in Table VI. As a crucial parameter of having a true field overlap between two fields is the relative closeness of the fields’ centers of gravity, we also indicated in the table the original centers of gravity of the overlapping fields in the two tasks. Cortical fields (or at least segments of fields) com- monly activated between the two tasks were present in the left cerebellar hemisphere, in the left fusiform gyrus, bilaterally in the inferior occipital gyri, in the right lateral occipital gyrus, in the left middle temporal gyrus, and in the anterior part of the right cingulate gyrus the left middle temporal gyrus, and in the anterior part of the right cingulate gyrus. (Figure 3.)

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Figure 3.


DISCUSSION

The main purpose of the present study was to localise those fields in the human brain participating in the discrimination of orientation and spatial frequency of gratings. We used PET to measure rCBF in ten normal volunteers, as an indicator of cerebral metabolism, while the subjects performed visual discrimination tasks. The results of the present experiments demonstrate that in simple visual discrimination tasks related to the fundamental visual cues of spatial frequency and orientation (1) networks of functional fields are activated in the human brain; (2) the fields are widely distributed in the cortex; (3) in a number of fields the locations overlap between the two tasks, indicating that the very same cortical fields participate in the processing of different visual features; whereas (4) other fields may participate in information processing specifically related to a given visual sub-modality. These observations, in comparison with earlier studies from our laboratory [Gulyas and Roland, 1994a,b; Gulyds et al., 1994a,b], strongly indicate that processing and analysis of single visual sub-modalities require a concerted operation from a number of cortical fields in the human brain.

The lack of any significant difference between response latencies or performance levels in the different tasks, as well as the fact that there were no significant differences among EEG frequencies, saccadic eye movements, arterial blood gas levels, or rCBF levels between the tasks indicates that the tasks were properly and closely matched in all respects except for the specific task features which were the subject of the present investigation. These observations speak for

Figure 3. Cortical fields participating in the tasks. The right hemisphere is on the left side, and the left hemisphere is on the right side (neuroradiological convention). Human brain atlas (HBA) images. The significantly activated fields (in yellow and red) are superim- posed on the standard MR brain image of the HBA. A-C: Horizontal image slices at z = - I I mm level. D-F: Horizontal image slices at z = +45 mm level. G-I: Coronal images at y = -39 mm. J-L Parasagittal slices at x = -39 mm (i.e., left hemisphere). Images in A, D, G, and J correspond to the “spatial frequency task-reference task” condition; 6, E, H, and K correspond to the “orientation task-reference task” condition; and C, F, I, and L display field overlaps between the two conditions. The horizontal lines in A-I as well as the vertical lines in panels J-L indicate the coronal plane (y = 0 mm), intersecting the anterior commissure, of the Talairach stereotactic coordinate system; the horizontal lines in J-L indicate the AC-PC plane (intersecting the anterior and posterior commissures; z = 0).

visual feature specificity of the activated fields present in the averaged ArCBF images.

In an earlier PET study on humans, the detection and identification of gratings with a given spatial frequency (0.5 cyddegree) but varying orientations specifically activated striate and extrastriate visual cortical areas, and though the authors had no firm histological reference for their interpretation, they identified the activated regions as being in Brodman areas 17, 18, and 19 [Dupont et al., 19931. Since the human homologues of the early visual areas (VLV5) in primates are thought to be located in the occipital lobe [Clarke and Miklossy, 1990; Zilles and Schleicher, 19931, the above findings indicate that in humans, similarly to cats and primates, grating (i.e., spatial frequency) and orientation-sensitive cells are present in the early visual areas. Due to the lack of MR scans, lack of rigid head fixation, normalisation of rCBF values, and 20 mm spatial filtering of the images, however, the above authors [Dupont et al., 19931 could not be specific in spatial localisation of the activation pattern.

On the other hand, Sergent et al. [1992] used sinewave gratings with varying spatial frequencies and with either vertical or horizontal orientation. The subjects had to press two response keys, one of which corresponded to horizontal and the other to vertical orientation. Under such detection conditions extensive activation was present specifically in the striate cortex, the lingual gyrus, the inferior occipital gyrus, and the banks of the parieto-occipital sulcus, indicating the importance of the striate cortex and its neighbouring cortical regions in the detection of a large range of spatial frequencies and a limited number of orientations (vertical, horizontal), which is in accor- dance with the findings of the present study.

Whereas the aforementioned studies were centered around the detection or identification of oriented grating stimuli, the present study focused on the discrimination of both spatial frequencies and orientations of gratings, i.e., a computationally more ad- vanced process.

Fields activated during spatial frequency discrimination were numerous and widely distributed in the occipital lobe and included the right cuneus (striate cortex) and fields bilaterally in the occipital superior and inferior gyri. In the orientation task three fields were activated in the occipital lobe. There was no activation present in the striate cortex, indicating that by way of subtracting the reference task from the orientation discrimination task, activations in the striate cortex eliminate each other.

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Gulyas and Roland

TABLE V. Volume of fields activated

Occipital Temporal Parietal Frontal Insula

A. Volume of cerebral cortical fields activated in the tasks (mm3)

Spatial frequency R L

R L

Orientation

8. Relative volume of cerebral cortical fields activated in the tasks (% of the total activated fields)

Spatial frequency R L

R L

Orientation

2,392 2,866 861 1,752

517 1,927 792 1,905

11.4 13.7 4.1 8.4

3.8 14.0 5.8 13.8

3,304 2,802

1,032 1,352

15.8 13.4

7.5 9.8

1,305 5,063

2,797 3,450

- 605

6.2 - 24.1 2.9

25.0 - 20.3 -

Activation of the Activation of the total cerebral cortex cerebellar cortex

(%) (%)

C. Total volume of fields activated in the task (% of the whole cortical volume)

Spatial frequency R 2.67 L 3.00 Total 5.67

R 1.69 L 2.01 Total 3.70

Orientation

1.11 1.11

- 2.49 2.49

Our observations indicate that cells already participate in spatial frequency discrimination at the striate cortex level (cf. activation along the banks of the calcarine sulcus), and the analysis of spatial frequency differences heavily engages extrastriate cortical areas as well. The role of the striate cortex is more limited in the processing of orientation information; whereas it is evident that in monkeys oriented visual stimuli elicit strong responses from striate cortical cells [Vogels and Orban, 1990,19911 and, consequently, cells in human

striate cortex probably also participate in the processing of orientation signals, their role may be limited in computing difjevences in orientations of gratings. This computational task, as indicated by activations outside the striate cortex, may predominantly be carried out by extrastriate visual fields in humans as is done in primates [Vogels and Orban, 19941. One can at this stage only hypothesise about these above observations. One possible interpretation is that whereas both retinal ganglion cells and cells in the lateral geniculate

146


TABLE VI. Field overlaps present between the two tasks

HBA coordinates (x, y, z) Distance between centers HBA coordinates of the original fields of gravities (mm) Volume x y z (mm3) SF OR OL-SF OL-OR SF-OR

5.1 4.5 5.9 1.7 7.8 7.5 6.2 10.1 2.4 5.0 3.7 14.9 3.3 23.2 1 .o 4.2 3.0 4.6

Intraparietal sulcus R 23 -58 38 105 23 -57 39 26 -62 37 1.4 Middle temporalgyrusL -53 -39 -10 116 -51 -41 -14 -52 -42 -15 4.9 SuperiorfrontalgyrusL -10 25 54 150 -10 26 54 -14 28 48 1.0 Cerebellum L -6 -49 -8 165 -8 -49 -4 -7 -50 -14 4.5 Fusiform gyrus R 38 -40 -14 186 35 -42 -12 39 -42 -15 4.1 MiddlefrontalgyrusL -43 40 4 186 -40 39 21 -44 42 7 17.5 SuperiorfrontalgyrusR 7 48 -9 306 28 38 -7 6 45 -10 23.3 InferiorparietallobuleL -44 -41 45 317 -44 -44 48 -43 -41 45 4.2 MiddletemporalgyrusL -61 -23 -8 544 -59 -23 -6 -63 -25 -7 2.8

OL: overlap; OR: orientation; SF: spatial frequency.

nucleus in primates are strongly sensitive to spatial frequencies and exhibit spatial frequency tuning characteristics, their sensitivity to orientations is nil or negligible, i.e., in the processing of spatial frequency information cells in the primary visual cortex already represent a higher stage and can further elaborate information pre-processed by cells at lower stages. On the other hand, with respect to the elaboration of orientation signals, cells in the striate cortex may represent the first stage (as indicated by the lack of orientation tuning at lower stages) and, consequently, more intricate operations regarding orientation discrimination processes must take place at higher levels in the hierarchy of visual areas,

In addition to occipital lobe activations, in both tasks activations were present in the temporal and parietal cortices. Though the locations of these activations were close to those fields found in form detection tasks [Gulyas and Roland, 1991,199413; Sergent et al., 19921, they were not in register with them. Since both orientation and spatial frequency discriminations represent crucial preliminary steps in the detection and discrimination of visual contours building up visual forms, the elaboration of which, in turn, requires the activation of neuronal populations in both temporal cortex [Gross et al., 19721 and parietal cortex [cf., e.g., Warrington and Taylor, 1973; Sergent et al., 19921, it is tempting to posit that both the temporal and parietal fields present in these tasks may represent neuronal populations which participate in the processing and analysis of spatial frequency and orientation information essential to form analysis.

Along with the observations described in the present paper on the presence of neuronal populations in temporal regions involved in spatial frequency dis-

crimination, an earlier study by Greenlee et al. I19931 has shown that spatial frequency discrimination thresholds were significantly elevated in patients with temporal cortex lesions (including circumscribed damage in the inferotemporal or medial or superior temporal cortex), indicating the involvement of temporal lobe visual regions in spatial frequency discrimination. The same study has also shown that inferotemporal damage was followed by higher discrimination thresholds for longer inter-stimulus intervals, indicating the possible role of the human inferotemporal cortex in short-term visual memory processes during delayed spatial frequency discrimination tasks. On the other hand, a few observations have been made about the role of the parietal lobe in spatial frequency discrimination processes in primates or man. In fact, Sergent et al. [1992] reported activation along the banks of the parieto-occipital sulcus during grating discrimination in humans. In patients with lesions in these regions, von Cramon and Kerkhoff [1993] have found a strong impairment in length and distance estimation (vital cues for spatial frequency discrimination). Our present observations support the view that neuronal populations not only in the temporal Iobe but also in the parietal lobe may indeed play an essentiol role in the discrimination of spatial frequencies.

Just as spatial frequency discrimination activated both the occipito-temporal and occipito-parietal visual pathways, orientation discrimination also did SO. In Inonkeys, indeed, lesions of the inferior parietal cortex caused Severe impairments in orientation discrimination [Gross et al., 1978; Eacott and Gaffan, 19911. On the other hand, earlier evidence obtained in monkeys on the role of temporal lobe regions in orientation discrimination is somewhat unclear: whereas tempo-

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Guiyas and Roland

ral lobe lesions did not impair orientation discrimination for large (> 60”) orientation differences, they did so for smaller differences (and sometimes, paradoxi- cally, even for 900) [Gross, 1978; Holmes and Gross, 19841. Dean [1978, 19821 has also reported effects of jnds in orientation after inferior temporal cortex lesions; however, due to the very large thresholds in his study the findings are not convincing. On the other hand, single cell recordings in behaving monkeys showed that inferior temporal neurons exhibit a strong same/different effect to successively presented and differently oriented grating stimuli (similar to the paradigm in our experiment), indicating a possible role of interior temporal cells in grating orientation discrimination [Vogels and Orban, 1994a,b]. In humans, von Cramon and Kerkhoff [1993] €omd disturbed orientation discrimination in patients with widespread parietal lesions (predominantiy in the post-cen tral, angular, and supramarginal gyri). These observations may support the hypothesis that in humans, as in monkeys, neuronal populations in both temporal and occipital lobes are essential in the processing of orientation signals.

In addition to the activation of fields in the occipital, temporal, and parietal lobes which, on the basis of earlier observations, can be closely related to visual perceptual processes, a relatively large number of fields was also present in the prefrontal cortex. Earlier PET studies on visual discrimination tasks also displayed the presence of strong prefrontal activations during the various tasks [Petersen et al., 1988, 1990; Corbetta et al., 1991; Gulyas and Roland, 1991,1994a,b], the locations of which are stimulus dependent and are probably related to higher cognitive and attentional features of the given task IRoland, 19931. Finally, it is worth noting the cerebellar activation in the orientation and the cerebeliar-caudate activation in the spatial frequency tasks. As eye movement frequencies are closely matched among the spatial frequency, orientation, and reference tasks, the activations cannot be related to saccadic eye movements, but to the specific visual features of the discrimination tasks. Since aria-

tomically the visual cortex is connected to both the CerebelIum and the basal ganglia [Glickstein et al., 1985; Saint-Cyr eC al., 19901, the activation in these anatomical structures indicates that relatively simple visual discrimination tasks may also engage subcortical fields by way of corticofugal connections.

The large number of activated fields in both discrimination processes speaks for a collaborative action of various cortical fields connected into a functional network which occupies between 3.70 and 5.67% of

the cortical grey matter. These data fit well with earlier observations from our laboratory, which showed between 3 and 9% involvement of the cerebral cortex in various simple visual discrimination tasks [GulyQs and Roland, 1994bl. The networks participating in spatial frequency and orientation discrimination are to some extent disparate. As a small number of field overlaps were found in the cerebral cortex between the activated fields participating in the two tasks, their presence argues for the existence of neuronal populations which may participate in the processing of both spatial frequency and orientation signals. It is worth noting here that most these ”overlapping” neuronal populations were found in the temporal and parietal lobes, i.e., indicating a temporo-parietal tendency in these locations, These findings, together with the fact that in both tasks relatively numerous fields were found in buth the temporal and parietal lobes, may further support the functional importance of temporo- parietal connections in the primate brain [Boussaoud et al., 1990; Morel and BuIlier, 19901 and indicate that processing and analysis of elementary visual inforrna- tion related to spatial frequency and orientation signals engage both the occipito-temporal and occipito- parietal visual subsystems [Ungerleider and Mishkin, 19821.

Due to the task design, the tasks did not only involve on-line discrimination components; they also required short-term memory components. In this respect, because of the shortcomings of the present task design, the short-term memory components were not ideally matched between the two task conditions and the reference condition. Whereas the reference task could have been solved immediately after the presentation of the first member of the stimulus pair (grating or not?) and the answer had to be kept in short-term memory until the “response signal” appeared in the screen, in the spatial frequency and orientation tasks the correct answer could have only been given after the presentation of the second member of the stimulus pair. These tasks could have been solved in two ways:

1. At the moment of the presentation of the second stimulus, the first stimulus had to be called into visual memory and a proper comparison had to be made between a seen visual stimulus and the visual memory representation of a formerly seen visual stimulus. The Correct answer, similarly to the reference task, had to be kept in memory until the onset of the ”response signal.”

2. It was also possible to solve this task by keeping in short-term working memory the two members of a stimdus pair and comparing the two visual memory

148

+ Spatial Frequency and Orientation Discrimination

representations to make the proper discrimination. (However, this latter option, which would require a longer neuronal operation, certainly did not play a major role during the experiment, since the response latencies between the three tasks were significantly not different.

In either case, a short-term visual memory component was also present in the spatial frequency and orientation tasks, which was not necessarily present in the reference task. In addition, whereas the spatial frequency task involved a comparison between the two members of a stimulus pair, in the orientation task the members of the stimulus pair had to be compared with each other and with an idealised reference signal (vertical), which could have added another visual memory to the others. In short, due to the task design, in the present experiment short-term visual memory components were also present. As the recall and keeping in memory of complex visual patterns with varying spatial frequencies and orientations require extensive activations in parietal, temporal, and frontal regions [Roland and Gulyas, 19951, a number of activated fields present in our findings may be due to short-term visual memory components. Indeed, comparing our present results with our earlier findings in a visual memory task including visual patterns abun- dant in spatial frequencies and orientations [Roland and Gulyas, 19951, we found field overlaps in the right inferior temporal gyrus and left posterior superior parietal lobule, right inferior parietal lobule, right superior frontal gyrus and left middle frontal gyrus (spatial frequency task versus visual memory task), and bilaterally in the inferior parietal lobuli, right middle frontal gyrus, and right cingulate gyrus (anterior part) (orientation task versus visual recall task). These fields may represent those cortical regions needed to keep in short term memory and recall visual images.

One can speculate about the functional importance of the processing and analysis of spatial frequency and orientation information in the brain. These signals are essential to generate the percepts of visual forms or more complex visual scenes. Indeed, earlier PET studies on the discrimination of visual forms generated by different visual cues indicated [Corbetta et al., 1991; Sergent et al., 1992; Gulyas and Roland, 1994b, Gulyas et al., 1994a,b] that, depending on the input cues, disparate cortical networks with constituent cortical fields in the occipital, temporal, parietal, and frontal cortices are involved in the processing and analysis of visual form information. Similarly, complex and widespread cortical activations were present when subjects

had to learn and recognise complex visual patterns [Roland and Gulyas, 19951. However, whereas in the studies by Gulyas et al. [1994a,b] the networks of functional fields elaborating visual form information were completely disparate and visual cue dependent, the functional networks activated during spatial frequency and orientation discrimination were partially overlapping. In fact, this should not be surprising in the context of the stimulus paradigm used by us in the present experiment which leaves room for co-processing of orientation and spatial frequency information, including a short-term memory component during which the image of a grating pattern had to be kept in mind; this component was not necessarily present in the reference condition (see above).

The present data support the view that processing and analysis of basic visual cues, such as spatial frequency and orientation, require the concerted action of a relatively large number of cortical fields, representing large neuronal populations. These networks of fields are only partially overlapping, indicating that, indeed, a convergence-divergence principle [Gulyas and Roland, 1994bl is present in the brain during visual perceptual operations: whereas the same visual cue may be processed and analysed by a number of different cortical fields (divergence), the very same cortical field may participate in the processing and analysis of various visual cues (convergence). Fi- nally, whereas both spatial frequency and orientation discrimination processes engage both occipito-temporal and occipito-parietal visual pathways, spatial frequency discrimination processes require markedly more cortical field activation in the occipito-parietal regions than do orientation discrimination processes.

ACKNOWLEDGMENTS

The authors express their thanks to Dr. Rufin Vogels and two anonymous reviewers for their valuable comments on earlier versions of the manuscript, to Walter Pulka for radiotracer production, and to John Pedersen for software assistance.

This paper is dedicated to the memory of Justine Sergent, a friend and colleague, with whom details of the present experiments and findings were discussed.

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Cortical fields participating in spatial frequency and orientation discrimination: Functinal anatomy by positron emission tomography