Orientation discrimination in the cat: Its cortical locus II. Extrastriate cortical areas

THE JOURNAL OF COMPARATIVE NEUROLOGY 364~32-50 (1996)

Orientation Discrimination in the Cat: Its Cortical Locus 11. Extrastriate

Cortical Areas

JAMES M. SPRAGUE, PETER DE WEERD, DENG-KE XIAO, ERIK VANDENBUSSCHE, AND GUY A. ORBAN

Departments of Neuroscience and Cell and Developmental Biology, Institute of Neurological Sciences, School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania

19104-6058 (J.M.S.); Laboratorium voor Neuro- en Psychofysiologie, Katholieke Universiteit te Leuven, Campus Gasthuisberg, B-3000 Leuven, Belgium (P.D.W., D.-K.X., E.V., G.A.O.)

ABSTRACT Luminance-defined edges or bars are among the basic units of visual analysis: a

“primitive” component of perception. We have utilized this stimulus in a psychophysical study of bar orientation discrimination in the cat before and after selective lesions in visual cortical areas. The cortices have been divided on the basis of their connectivity into three tiers. Tier I refers to areas 17 and 18, tier I1 includes areas that receive directly from tier I, and tier I11 includes those areas that receive directly from tier 11. Previous studies (Vandenbussche et al. [1991] J. Comp. Neurol. 305:632-658) have shown that the discrimination of bar orientation depends heavily upon the integrity of areas 17 and 18 (tier I). The present study indicates that several extrastriate areas in tiers I1 and I11 contribute to this discrimination task. Our data suggest that the anterior medial lateral suprasylvian, the posterior lateral lateral suprasylvian (tier 111, and the anterior lateral lateral suprasylvian (tier 111) areas are most likely to contribute to bar orientation discrimination. D 1996 Wiley-Liss, Inc.

Indexing terms: visual cortex, ablation, visual perception, behavior

The evolution of the mammalian brain has resulted in a multiplicity of subcortical visual centers and cortical areas containing cell assemblies sensitive to many cues that serve to detect, perceive, and discriminate essential parts of the complex visual scene. One approach to an understanding of the elements of such a complex process is a simplifying one that measures the thresholds for discriminating simple stimuli differing primarily in a single dimension (cue). Since Hubel and Wiesel’s (1959) discovery that visual cortical neurons respond specifically to oriented lines or bars, it has become widely accepted that coding of bar orientation is an elementary feature of visual analysis: a “primitive” component of perception.

The use of such a simple stimulus in a behavioral study has several advantages, in that the behavior of the animal is controlled by a single or dominant dimension of the stimulus. Thus, the alteration of discriminative behavior can be linked to a single stimulus parameter: in this case, contour orientation.

A widely accepted scheme in computational vision is that the brain first performs a local analysis of the image (filtering). This early visual analysis is dependent on the registration of a set of simple primitives or functional features that are not represented by single cells, as envis-

aged in the theory of feature analysis (Barlow, 1972). Rather, they are coded in the distributed pattern of activity in a large population of cells (Georgopoulos et al., 1986; Orban et al., 1990; Vogels, 1990). This local analysis is followed by a number of more complex operations that lead to segregation, to the representation of three-dimensional surfaces, and to object recognition. In attempting to relate such a concept with the realities of the anatomical organization of the cortical visual system, we decided to make a somewhat arbitrary division between so-called “lower order” areas and “higher order” areas. The lower order or “early” areas are those receiving a strong and specific input from the dorsolateral geniculate nucleus (LGNd), namely, areas 17 and 18, which are the exclusive recipients of laminae A and Al. For the “later” or higher order stage, we chose those cortical areas that receive direct projections from areas 17 and 18; namely, areas 19, 20a, 21a, and 21b as well as the anterior medial lateral suprasylvian (AMLS), suprasylvian (PMLS), and posterior lateral lateral suprasyl-

Accepted June 6,1995 Address reprint requests to Prof. Dr. G.A. Orban, Laboratorium voor

Neuro- en Psychofysiologie, Katholieke Universiteit te Leuven, Campus Gasthuisberp, Herestraat 49. B-3000 Leuven, Belgium.

EXTKASTRIATE CORTICAL AREAS AND ORIENTATION 33

vian (PLLS) areas. These areas also receive afferents from the LGNd laminae other than laminae A and A,, from the superior colliculus-pretectum via sectors of the lateral posterior (LPj-pulvinar complex and the intralaminar nuclei. We term areas 17-18 “tier I” cortex, and we refer to the areas that receive direct projections from tier I as “tier 11.” The forward projection of tier I1 areas terminates in what is referred to as “tier 111.” This tier includes the anterior lateral lateral suprasylvian (ALLS), ventral lateral suprasylvian (VLS), dorsal lateral suprasylvian (DLS), and posterior suprasylvian (PS) areas as well as area 7p. An important anatomical detail is the feed-back reciprocal projection of each tier onto the “preceding” tier (Rosenquist, 1985).

In a series of studies, we measured thresholds in orientation discrimination in the cat using contours defined by either a simple luminance difference (luminance bar) or by opposite line ends (referred to as illusory contours), and we assessed the effects of tier I and I1 visual cortex lesions on these thresholds. In addition, we studied the segregation of textures made of small oriented bars before and after the same types of lesions. The lesion effects we observed gave us interesting insights into the division of labor among the many visual cortical areas in the cat (Orban et al., 1990; Vandenbussche et al., 1991; Sprague et al., 1993; De Weerd et al., 1993, 1994). Removal of both areas 17 and 18 resulted in severe deficits in bar orientation discrimination, which, however, was followed by partial recovery (Orban et al., 1990; Vandenbussche et al., 1991). In the tasks involving illusory contours and textures, the deficits were at least as severe as for bar orientation discrimination, and there was no recovery (De Weerd et al., 1993,1994). On the other hand, removal of several, but not all, of the tier I1 areas receiving direct projections from areas 17 and 18 resulted in pronounced deficits in orientation discrimination of illusory contours, whereas deficits in bar orientation discrimination were small or negligible (De Weerd et al., 1993). We concluded that contours that can be directly derived from the local luminance distribution in the image are processed predominantly by areas 17 and 18, whereas stimuli such as illusory contours and textures, which require adequate combination of the output of local filters (e.g., grouping), need processing in areas beyond 17 and 18. Despite the massive parallel input to most visual cortical areas in the cat from several subcortical centers (Rosenquist, 1985), these findings were consistent with a hierarchical scheme in which areas 17 and 18 are involved in the initial filtering of the image and in which areas receiving projections from areas 17 and 18 perform additional operations on the basis of the input from these two areas.

Although extensive lesions of both area 17 and area 18 (complete in cat 22) without subcortical damage resulted in marked deficits in orientation discrimination of simple bars, the basic capacity to perceive and discriminate such oriented contours was not abolished (Vandenbussche et al., 1991). This, of course, suggests that extrastriate cortex is involved to some degree in this function. We are left with several questions unanswered: What happens with the output of areas 17 and 18? Is it sent directly to motor centers controlling this function, or does it reach motor centers via tiers I1 and I11 cortex? In our earlier studies, did we underestimate the contribution of extrastriate cortex because the lesions spared parts of tier I1 and all of tier I11 cortex? What would happen after complete tier I1 or a combined tiers I1 and 111 lesion that spared parts or spared much of tier I? We have investigated these questions in the

present study. Preliminary results have been reported previously by Vandenbussche et al. (1989) and Sprague et al. (1993).

MATERIALS AND METHODS Subjects

Eleven sexually mature cats of both sexes were used. They were kept in individual cages in the animal colony. Prior to training, they were reduced to 85% of their free-feeding weight. At the end of the training, their weight drifted back to about 90%’ of their normal weight. Access to water was unlimited. During weekdays, they obtained food only by performing correct discriminations during training or testing. The amount of food they got for every correct response was empirically determined, so that we could keep the desired weight of the animals stable during testing. At the end of the day, skimmed milk was Dven to stimulate drinking and to avoid high urea concentrations. Vitamins were added to their food daily.

Apparatus and stimuli The animals were trained and tested in a two-choice

discrimination apparatus designed after Berkley ( 1970). The apparatus has already been described in full detail in earlier papers (Vandenbussche et al., 1986; De Weerd et al., 1990a-c). I t consisted of a testing chamber (0.52 x 0.29 x 0.41 meters) with a 0.28 meter hole at one end through which the cat could thrust its head into a Plexiglas chamber. Facing the outer end of this chamber were two transparent keys through which they could see the stimuli projected on a screen placed behind the keys. Cats were required to push one or the other key with their noses to activate a food terminal that delivered a small food reward for a correct response.

Stimuli were back-projected on a circular screen 0.30 meters in diameter and were placed at 0.285 meters from the cats’ eyes. The stimuli were two light bars projected simultaneously on the screen by two slide projectors. The distance between the centers of the bars on the screen was 24.0” (visual degrees). The full screen was split by a vertically oriented separator, so that only one bar at a time could be seen by the animal. Each projector was fitted with a slitmaker, which defined the length and the width of the light bar. The standard bar was 12.0” long and 0.2” wide. Each bar was projected through a rotating dove prism and an adjustable filter. By means of stepper motors, the filters and the prism could be rotated so that the luminance and the orientation of the light bar could be adjusted whenever required. Stimulus duration was controlled by shutters placed in front of each projector. The two projectors and the test chamber were placed in a tunnel that protected the screen from the ambient light present in the experimental room. Thereby, the background illumination on the screen was kept at a constant level of 0.5 cd/m2. Luminance of the standard bar was 15.8 cd/m2, yielding a 1.48 contrast (log AI/I). Before each animal was placed in the test apparatus, the positioning of the light bar in the center of the screen as well as its luminance and orientation were calibrated.

To evaluate rigorously the effects of cerebral lesions on visual perception, it is essential to use sensitive behavioral methods. A procedure that measures the lowest thresholds, referred to as just noticeable differences (JNDs), has been found to be a most sensitive tool with which to reveal deficits in orientation discrimination following cortical le-

34 J.M. SPRAGUE ET AL.

random sequence in such a way that the S+ was never presented more than three times in a row behind the same response key. In addition, within each group of six succes- sive trials, the s+ was presented three times behind the left key and three time behind the right key. Within these limitations, all possible successions of leftiright presenta- tions were administered. When the animal developed a preference for one key (position bias), which we defined as six consecutive responses to the same key, the S+ was presented behind the nonpreferred key until the numbers of left and right key responses were again equalized.

Two types of parametric variations have been carried out using the bar stimulus: manipulations of bar contrast and of bar length. Length experiments have been used to investigate whether the cats used alternative cues to solve the discrimination task in addition to orientation (De Weerd et al., 1990b).

Because we wanted to measure orientation discrimination performance by means of thresholds, we used the differential exposure method (DEM; De Weerd et al., 1990a) to train the animals. This method greatly shortens training duration through the use of cueing trials in which the exposure duration of S- is shorter than the exposure of S+. Both the presence and the strength of this temporal cue as well as the orientation difference are made dependent on the efficiency of discrimination behavior. This method allows the cats to reach good performance quickly at small orientation differences; after this, a staircase procedure is used to determine the exact orientation thresholds (see below). The animals need no special training to perform in the bar detection task, and optimal performance can be reached by the use of staircase measurements alone (see below).

In the contour orientation discrimination task, we wished to determine the smallest difference in orientation between two bars that the animal could reliably distinguish at a fixed, optimal contrast. In the bar detection task, on the other hand, we determined the lowest contrast at which the bar could be reliably detected. The latter task is a measure of a very basic visual capacity, and the way in which performance in this task is affected can be helpful in the interpretation of lesion effects.

To determine the thresholds, we used a staircase procedure (see De Weerd et al., 1990~) during which the parameter under investigation was continually adapted to performance. In the contour orientation discrimination task, the orientation difference was decreased after three consecutive correct responses or after two correct responses followed by an incorrect and a correct response. The orientation difference was increased after a single incorrect response, after a correct response followed by an incorrect response, or after two correct responses followed by two incorrect responses. In the bar detection task, bar contrast was made dependent upon performance in an manner analogous to that described above for the contour orientation discrimination task. Here, the contrast [log (AIiI)] was adapted to performance by adding or subtracting a value of 0.1 to the current contrast.

When implementing the staircase in this way, we estimated the 73.5% correct point on the psychometric distribution (Wetherill and Levitt, 1965). The use of this moderate criterion enhances the possibility that it can be achieved even by severely lesioned animals. Those staircases in which the animal did not reach 66% correct even for large orientation differences (40” maximum) were considered to

Training procedures.

Testingprocedures.

sion. An important additional requirement is that behavior must be stable before the lesion, and the effects of the lesion must be followed long enough to ensure that the postoperative performance is also stabilized. Thus, in this study, performance was measured up to a year before the lesion, and the effects of the lesion were followed for up to an additional year.

Behavioral procedures Initial shaping and detection task. By a shaping proce-

dure, a cat was trained to thrust its head into the Plexiglas chamber and was rewarded for developing “looking behavior,” in which the animal made head movements towards the left or the right key. In this phase, there was no separator, and the cat could see the complete screen and a large square stimulus that was present on the left or on the right. In the second phase of shaping, the animal was rewarded only when it made a head movement toward the stimulus. Reinforcement was used to bring the cat’s nose increasingly closer to the nose keys until it pushed the key. Once the cat was pushing the keys, it was rewarded for pushing the key with the square stimulus (shape-detection task). Cats were taught to work for smaller and smaller squares in order to accustom them to working on difficult tasks. In the three animals that received the largest lesions, training in bar orientation discrimination was preceded by a shape-discrimination task in which the cat had to distinguish a square (S+) from a circle (S-) of equal area and luminance. The positions of the shapes were randomized (as was the position of the square in the square-detection task), and task difficulty was increased by decreasing the size of the shapes.

Bar discrimination and detection tasks General aspects. In the discrimination task, cats had to

distinguish between two identical contours (bars) of different orientation. The orientation of one of the two discriminanda remained fixed throughout the task and is referred to as the reference orientation, which served as the positive stimulus (S+). The second stimulus deviated in orientation from the reference orientation and served as S-. To ensure the generality of our observations, the orientation discriminations were taught around two reference orientations: the horizontal (H) and the right oblique (RO). When the reference orientation was H, the S- deviated clockwise, and it deviated anticlockwise when the reference orientation was RO. The order in which the animals were trained for each reference orientation was randomized among animals.

In the bar detection task, the animal was only presented with the reference orientation, and no stimulus was present on the other side of the screen. Here, the animal’s task was merely to push the response key behind which the bar was presented.

A discrimination or detection trial started upon stimulus onset. During the first 350 msec of stimulus presentation, the animal had to delay its response [response delay period (RDP)J to enforce attention. Because responses during the RDP were never rewarded, they extinguished as the animals became more experienced. After the RDP, the animal was rewarded for pushing the nose key behind which the S+ was presented. Upon the animal’s response, the stimuli disappeared, and a 7 second intertrial interval (ITI) was started during which only a dark background was visible.

The S + was presented behind the left and right keys in a balanced pseudorandom order to avoid any associations of S+ with one of the two resDonse kevs. We balanced the

EXTKASTKIATE CORTICAL AREAS AND ORIENTATION 35

be without stimulus control (De Weerd et al., 1993), and no threshold was calculated.

A single staircase measurement lasted 75 trials. This number of trials generally yielded 12-16 reversal points (Fig. 8). Because the staircase measurement started near threshold level, and because of the proportional rule used to vary the orientation difference, the threshold was calculated as the geometrical mean of all reversal points. Two thresholds were measured daily for each reference orientation for either the detection task or the discrimination task. The first threshold measurement of each reference orientation was preceded by a 20-trial introduction block in which a fixed orientation difference was presented 1.5 times larger than the estimated threshold expected from previous sessions.

Anesthesia was induced by intra- muscular injection of 0.5 ml Ketamine (Ketalar",; 0.2 mlikg) followed by 1.0 ml atropine. The femoral vein was cannulated, and pentobarbital (Nembutal'".) diluted 50150 with saline, was administered until respiration was stabilized at 10-16iminute and no nociceptive reflexes could be evoked. Hair on top of the head was removed with a depilatory. The external meati were filled with an analgesic ointment, and the cat was placed in a stereotaxic instru- ment. Body temperature was maintained between 37.0"C and 375°C. Surgery was carried out using rigorous sterile techniques. At the end of surgery, antibiotic Cefazolinum (Kefzol"; 200 mg, i.m.) was administered.

Cortical lesions were made by subpial aspiration of the grey matter. Placing of lesions restricted to selected cortical areas or even to single cortical area has been made possible by the careful maps prepared using differences in anatomical organization and in physiological characteristics of the constituent neurons. The visual cortices of the cat have been defined histologically by Otsuka and Hassler (1962) and by Sanides and Hoffmann (1969) and retinotopically by Tusa et al. (1978, 1979, 1981) and by Palmer et al. (1978). The retinotopic maps of areas 17, 18, 19,20, and 21 and the lateral suprasylvian (LS) area are summarized in Rosen- quist (1985). The study of Updyke (1986) on the visual areas of the posterior suprasylvian sulcus and gyrus pro- vides a detailed description of area PS. In removing the PS and area 21b, care was taken not to invade the visual belt of the posterior ectosylvian gyrus described by Bowman and Olson ( 1988), which has been implicated in visual orienting (Toga et al., 1979). Retinotopic organization of the lateral geniculate was mapped by Sanderson (1971). Such maps, by necessity, are derived from relatively few animals but with some attention paid to individual variation. We have used the results of all of these mapping studies in placing our lesions. As indicated below, their accuracy has been checked in three ways: 1) the retinotopic data obtained in the physiological study conducted just before killing the animals; 2) histological reconstruction of the lesions using both myeloarchitecture and cytoarchitecture of the remain- ing cortex; and 3) retrograde atrophy in the thalamus, especially the dorsolateral geniculate complex, when the lesions involved areas 17, 18, and 19.

After completion of the lesions, the bone defects were covered with Gelfilm, the muscles were sutured in two layers, and the skin was closed with clips. The animals were usually awake and eating the next day and could be returned to their home cages within 48 hours. Neurological tests (see Vandenbussche et al., 1991) were given weekly until responses were normal or until deficits were stable

Surgical procedures.

(2-3 weeks). By this time, the incisions were healed, and the animals were returned to the daily testing routine.

Physiological and anatomical evaluation of the lesions. After postoperative training and testing were completed, the animals were prepared for single-unit recording using standard techniques (Orban et al., 1981a,b). Penetrations were made into the cortex of areas 17 and 18, and the visual responsiveness of the units was assessed along with the receptive field locations. The locations of cells recorded in successful penetrations were marked with small electrolytic lesions for histological identification.

At the end of the physiological recording sessions (typi- cally 2 days), the anesthesia was deepened by injection of Nembutal I' , and the animals were killed by intracardiac perfusion (first with saline and then by 10% formal-saline). After hardening in the perfusate, the brains were blocked stereotaxically and were removed from the skull. They were embedded in parlodion, and coronal sections were cut at 48 pm and stained alternately in cresyl violet for cell bodies and in Mahon for fibers. Representative stained sections were projected and drawn, and cortical areas were identified using the anatomical criteria of Otsuka and Hassler (1962) and Sanides and Hoffmann (1969) and using the physiological maps of Tusa et al. (1981). The cortical lesions were reconstructed, and the retinotopic position of retrograde atrophy in the LGNd was estimated using the study of Sanderson (1971). Lesion extent was plotted on the visual field maps as determined in the studies of Tusa et al. (1978, 1979,1981) and Palmer et al. (1978). The use of these maps was validated to a degree by the recent deoxyglucose study of Vanduffel et al. (1995). These authors report significant differences in metabolic activity between most neighboring cortical areas defined by these maps. The visual field plots of the lesions are useful in estimating the size and retino- topy of the lesions, but they do not show the cortical magnification. Therefore, the lesions were replotted on flat maps of the visual cortex modified from Van Essen and Maunsell(1980) and described in De Weerd et al. (1994).

Deficits in discrimination of luminance-defined bars have followed large tier I lesions (areas 17 and 18) but not after comparable lesions of area 19 and adjacent parts of area 18 (Vandenbussche et al., 1991). The present paper describes the effects on bar discrimination of more extensive tier I1 lesions that are comparable to or larger than those used in the illusory contour and texture experiments of De Weerd et al. (1993, 1994). In order to make these extensive lesions, the convexity of the middle suprasylvian gyri was removed in all animals. This lesion included area 7p, which does not receive directly from areas 17-18 but is closely related to many areas of tier I1 cortex (Olson and Lawler, 1987). An initial group of cats received lesions largely restricted to areas 19, 20a, 21a, PMLS, and 7p comparable to those used in the illusory contour and texture segregation studies (De Weerd et al., 1993, 1994). Given the modest effect of these lesions, a second group of cats received more extensive lesions that included not only tier I1 but also tier I11 areas.

The lesion effects were statistically evaluated in one of two ways. Where preoperative control data were available, pre- and postoperative JNDs at a given parameter setting were compared by a two-tailed t test for independent samples using separate variances. In those cats for which no preoperative data were available, postoperative JNDs were compared to those of four control cats using a two-way analysis of variance (ANOVA), with ani-

Plan of the lesions.

Statistical testing.

36

A

J.M. SPRAGUE ET AL.

CAT 69 B

2

Fig. 1. The brain of cat 69 is shown in dorsal (A) and lateral (B) surface views with the lateral (11, postlateral (2), middle (31, and posterior (4) suprasylvian sulci opened to expose both banks. The lesions are indicated by stippled areas bounded by dashed lines. The horizontal lines in A (a-g) and the vertical lines in B (a-gj indicate the

mals and parameter (length or contrast) as factors. For those ANOVAs in which the factor animal was significant, the posthoc Scheffe test was used to compare postoperative and control JNDs at each parameter value.

RESULTS Anatomical results

The extent of the lesions in all cats is shown in Table 1. These lesions can be divided into three groups: 1) lesions primarily in areas 19, 21a, 20a, PMLS, and 7p in the first four cats; 2) lesions extending more widely in tier I1 and tier I11 or with much involvement of tier I (next four cats); and 3) very large lesions involving most of tiers I, 11, and I11 (last three cats). Given the large number of animals involved, we looked for a way to provide an overview of the lesions in all animals. To complement Figures 1-6, which describe lesions in four animals (cats 69, 33, 95, and 841, Table 1 presents the lesions in terms of percentages of each area destroyed estimated from the flat maps, which, as men- tioned earlier, reflect the cortical magnification factor. When the lesions involved the cortex of representation of central vision (area centralis), this is indicated by an asterisk. In addition to the tier I1 and tier I11 cortex actually removed by aspiration, in most cases, there was some inadvertent invasion of white matter innervating areas 17 and 18 (tier I). The degree to which this occurred was estimated by recording in areas 17 and 18 before killing, by study of the fiber stained sections of the cortex, and by mapping the presence of retrograde atrophy in LGNd and its retinotopic coordinates using Sanderson (1971).

The lesions in cats 69, 85, 66, and 58 have much in common and involve many parts of tier I1 cortex: areas 19, 21a, 20a, and PMLS, sparing AMLS, and, in most cases, sparing PLLS and area 21b. The only portion of tier I11 cortex that was lesioned consistently was area 7p. Inadvertent damage to areas 17 and 18 by invasion of white matter was minimal to modest, except for area 17 in cat 69. The lesions in cat 69 are shown in surface view in Figure 1 and are transposed to flat maps in Figure 2. The physiological recordings obtained in all four cats confirmed that area 17 was functional. Single cells with receptive field properties similar to those of normal animals were recorded either at the area 17-18 border near the area centralis representation (cats 66 and 85) or on the medial bank (cats 69 and 58)

Group Z (n = 4).

:

, . a b c

levels selected for full reconstruction of the lesions. Numbers in the left hemisphere of A indicate: 1, medial bank of lateral sulcus; 2, inferior bank of posterior lateral sulcus; 3, lateral bank of middle suprasylvian sulcus; 4, superior bank of posterior suprasylvian sulcus.

as illustrated in Figure 2A (azimuth, 5-10") and in Figure 2B (azimuth, 30").

This group included animals with lesions involving more tier I1 areas than in group I and also involving some tier I11 areas. Cat 12 had the smallest lesions, not unlike those of cats in group I, but the lesions included VLS and DLS. Physiological recordings made into the medial bank (area 17) and the area 17-18 border confirmed that area 17 was functional in this animal. Cat 33 had more extensive lesions in tier I1 cortex that included the areas involved in group 1 animals plus areas 21b, PLLS, AMLS, and tier I11 cortex (VLS, DLS, PS, and area 7p). The secondary involvement of tier I cortex (areas 17 and 18) was comparable to that found in group 1 cats. Cat 95 had extensive lesions similar to those in cat 33, but they were larger in area 20a, PLLS, and area 17. Cat 98 had tier I1 cortical lesions similar to those in group 1 (except for involvement of AMLS) but had very extensive involvement of the white matter innervating tier I (areas 17 and 18). The lesions in cat 33 are shown in Figure 3, and the lesions in cat 95 in are shown in Figures 4 and 5 .

The lesions in cats 84, 93, and 99 represented an attempt to remove all units of tier I1 cortex, and, in this sense, they were successful. However, they also invaded many areas of tier I11 (ALLS, VLS, DLS, and, in cat 84, PSI. In addition, these extensive lesions involved the white matter supplying areas 17 and 18, resulting in extensive denervation of both units of tier I in cats 93 and 99 but sparing part of area 18 in cat 84. The lesions in cat 84 are shown in Figure 6. Physiological recordings were made only in cats 84 and 93. In general, visual cortex (areas 17 and 18) was unresponsive. However, in cat 84, multiunit recordings confirmed that, in the left hemisphere, parts of area 18 remained functional. These recordings also suggested some sparing in area 17, because visually driven, orientation-selective multiunit activity was recorded in the medial bank of the right hemisphere with a receptive field at 5" azimuth and 7" elevation (Fig. 6). Careful inspection of the right LGN in cat 84 revealed that, indeed, there was a small sparing, which, according to Sanderson's map, corresponded to approximately +2" to +5"" elevation and 2" to 5" azimuth: a very nice match with the physiological result. This observation underscores the power of the combined physiological-anatomical assessment of damage to areas

Group ZZ (n = 4).

Group ZZZ (n = 3).

17-18.

EXTRASTRIATE CORTICAL A4REAS AND ORIENTATION 37

CAT 69 A RIGHT HEMISPHERE A

CAT 33 RIGHT HEMISPHERE n MEDIAL ,SPENIAL s

CORONAL S. POSTER10 VIAN PRASYLVIAN S

B

ECTOSYLVIAN S A

LEFT HEMISPHERE B

ECTOSYLVIAN S A

L E F T HEMISPHERE n

POST ERlOR POST ERlOR

Fig. 2. Flat maps of the tier I1 lesion in cat 69. Light stippled areas indicate sulci after opening. The fundus of each sulcus is shown by a dashed line, borders of different cortical areas are indicated by heavy lines, and the extent of the lesions of these areas is indicated by stripes. The stripes in area 17 does not indicate actual invasion of the cortex by the lesion but reflects unintentional damage to the geniculocortical fibers providing afferents to 17 as determined by atrophy in laminae A and A, of the dorsal lateral geniculate nucleus (LGNd). Elevation lines are shown and labeled in A, and azimuth lines and unlabeled elevations are shown in B. The stars in area 17 of A and B represent the anatomical position of visually driven single cells in two penetrations. HM, horizontal meridian; VM, vertical meridian; AMLS, anterior medial lateral suprasylvian area (LSA); ALLS, anterior lateral LSA; PMLS, posterior medial LSA, PLLS, posterior lateral LSA, VLS, ventral LSA; DLS, dorsal LSA.

In cat 93, no driven cortical activity was observed. However, occasionally, visually responsive LGN fibers were recorded. To some extent, the lesions in cats 98,84,99, and 93 involved stripping the pia rather than the subpial aspiration, and, for that reason, more extensive damage was done in the fundus of the sulci to the white matter supplying areas 17 and 18.

Behavioral results The cats were trained in bar orientation discrimination

and were tested for thresholds using standard conditions

Fig. 3 . A,B: Flat maps of the tier I1 lesions in cat 33. Abbreviations and symbols as in F i p r e 2.

for optimal visibility determined in a previous study (Van- denbussche et al., 1991). This standard consisted of bars 12.0" long and 0.2" wide with a contrast of 1.48. The animal worked at two reference orientations: horizontal and oblique (see Materials and Methods). The lesion effects were similar for the two references, and, in keeping with our previous studies (Vandenbussche et al., 1991; De Weerd et al., 19931, we will only use the data obtained at the horizontal reference, which are the most sensitive and which yield the clearest deficits. Performance was also measured when two parameters of the stimuli were varied: contrast and bar length. Even for a simple stimulus such as a bar, it is difficult to vary only orientation without also changing another dimension of the stimulus that could be used to make the discrimination. For example, the positions of the endpoints of the bars change with the change in orientation (Orban et a]., 1984). We have previously shown (De Weerd et al., 1990b) that orientation and endpoint position are the only two cues that cats use in this task and that the data obtained at different bar lengths can be used to determine which of the two cues the animals used.

When an animal is confronted with stimuli carrying two different cues, it is highly likely that it will use the more


CAT 95 B

Fig. 4. The brain of cat 95 is shown in dorsal (A) and lateral (B) views with the sulci opened to show both banks. Lesions are indicated by the stippled areas. Numbers in the left hemisphere of A indicate the positions of cortical areas: 1, AMLS; 2, ALLS; 3, PMLS; 4, PLLS; 5, DLS; 6, VLS; 7, area 21b; 8, posterior suprasylvian area (PS); 9, area

CAT 95 A RIGHT HEMISPHERE

POSl

B

ATERAL S

CORONAL S

SUPRASYLVIAN

LEFT HEMISPHERE

21a; 10, area 19; 11, area 20a; 12, area 7p. Because the lesions are almost symmetrical, only the lesion in the right hemisphere is shown in A, and only that in the left hemisphere is shown in B. See Figure 2 for abbreviations.

CAT 84 A RIGHT HEMISPHERE

LATERAL S

CORONAL S

SUPRASYLVIAN ULCUS

B LEFT HEMISPHERE

/LA POSTERIOR POSTERIOR

Fig. 5. A,B: Flat maps of the tier I1 lesions in cat 95. Abbreviations and symbols as in Figure 2.

salient cue to guide its discrimination. The orientation cue becomes less salient as the bar shortens, because the lendhiwidth ratio determines the amount of orientation

Fig. 6. A,B: Flat maps of the tier I1 lesions in cat 84. Abbreviations and symbols as in Figure 2.

information available. Therefore, it is possible that, at short bar lengths, the animal will shift to another cue such as the relative Dosition of the endDoints. The thresholds obtained

EXTRASTRIATE CORTICAL AREAS AND ORIENTATION 39

TABLE 1. Grouping by Anatomical Criteria)

Cat Area Hemisphere Area 17 18

Anatomic$ group I 69 69 85 85 66 66 58 58

12 12 33 33 95 95 98 98

84 84 93 93 99 99

Anatomical group I1

Anatomical group 111

R L R L R L R L

R L R L R L R L

R L R L R L

65' 75' 20 25 25*

0 30'

0

1201 I201 40' 40' 70 70- 95" 90'

70* 70* 90" 85* SO^ 70'

104 15' 10 13

5 0

0

10 10 20

5 10

95' 90-

60 15 95- so* 90- 70"

1

0

Area Area Area Area Area Area 19 21a 21h 20a PMLS PLLS AMLS ALLS VLS DLS PS i p EVA 20h

70- 70' 45* 50- 40* 60' 60' 60'

40 40 so* SO'

loo* 80-

100' 100'

100- so* 80- 70* 80" 95"

100 100' 100' loo* loo* 90'

100' 100-

50 70

loo^ 100' 100' 80* 95' 95'

100' 100- 100" 100' looh loo*

25 25

0 0 0 0 0 0

50 0

100- loo*

0 0 0 0

loo* 100'

50> 100"

50' 50'

30' 50' 60" 50" 70' 30' 50' 60'

40 40

loo* 40

loo* 80'

100' 75'

100- 100'

50 50 50 50

90' 90% 75 80 70 70 80' 40

75 75 90' 90'

100' 1004 95- 95'

100- 100' 100" 100' 100" loo*

0 0 0

20 (1 0 0 0

0 0

25' 25'

100' 100' 0 0

1008 100' 100' 100' 100' 100.

0 0 0 0 0 0 0 0

0 0

35. 35'

0' 0*

50* 50'

80' 80'

100' 100' 100'

50

0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0

SO' 80'

100- 100' 100'

50

0 0 0 0 0 0 0 0

70 70

100' 100' 95' 80'

0 0

loo* 100' 100%

75 50 50

0 25 0 25 0 0 0 0 0 0 0 0 0 0 0 0

50 0 70 0

100' 100' 100' 20 95' 0 801 0

0 0 0 0

100" 75* 100' 75% 100' 0

75 0 100' 0 loo* 0

100 100 100 100 100 100 100 100

100 100 100 100 100 100 100 100

100 100 100 100 100 100

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

0 0 0 0 0 50% 0 0 0 0 0 0 0 0 0 0

90% 0 0 0 0 0

40 0 100' 0 100" 0

' S u m m a y of the extent and size of the lesiuns in 11 cats used in this study Three groups are distinguished on the basis of lecion size The numbers represent estimates of t h e percentage irf tissue destroyed in each cortical area, the designations of which follow Rosenquist 119851. Asterisks indicate tha t t h e area of central vision (a rea centralis. 0-5- eccentricity1 was involved in the lesion The parentheses for cat 12 indicate tha t actual damage t o area 17. although probably correct, is somewhat uncertain because ofpoor staining of t h e doraolaterd geniculate nucleus. Boldface is used fur percentages of 60": and over PMLS. posterior medial lateral buprasylvian. PLLS. posterior lateral lateral suprasylvian: .4MLS. anterior medid lateral suprasylvian: ALLS, anterior lateral lateral supracylvian: VLS, ventral lateral suprasylvian. DLS. dorsal lateral zuprasylvian. PS, posterior suprasylvian. EVA. ectoiylvian vi.<ual area.

TABLE 2. Grouping by Behavioral Criteriai

JNDs orientation JNDs orientation JNDs onentation Detection contrast of last preoperative of first postoperative of last postoperative of postoperative

Cat test ( in davsi test (in davs) test f in davsi tests (in davsJ

Behavioral group 1 69 69 85 85 66 66 58 58 12 12

Behavioral group 2

Beha\ioral p i u p 3

33 33 95

95 98 98 84 84 93 93 99 99

4 5 ( 0 8 1 ~ 12 to -2

581151 -11 t o -1

4.9 11.01 -99 t o -93

9.5 11.31 -66 to -54

5 2 i l 7 l -24 to - 1

471081 -16 to -8

6.8 12.01 -45 t o -30

5 7 12.31 -129to-112

17.9 14.91 -121" -1

9.1 12.61 - 1 2 t o - 1

7 7 1 1 7 1 -15 tu -1

7.0 ! 2 . 2 1 ^ " + 15 t o -26

8.1 I3 2)" + I 9 to +26

8.9 i2.01'*' t 4 4 to +56

15 4 13 31"* -33 to +42

9 6 13.81' +8 to + I 2

+ 15 t o -26

1 2 6 to +30

+ 5 7 to +68

-15 to + 2 6

+ 15 to +26

+ 1 5 t o - 2 6

10 11451 ' ' '

No discrimination

No discrimination

S o discrimination

No discrimination

S o discrimination

6.3 ! I 71"' +58 t o +65

5.2 I 1 ii -43 to +54

i . 9 12 It*-* - 5 i to t i 0

10 112.91 + l l X t a - 1 2 6

5 3 ' 1 4 1 + I 5 to -26

, a iI 51" + 2 9 t o +33

15 3 15.81"' + I13 to 1 1 2 6

13.8 18 81*-* +127 to +I30

So discrimination +39 to -146

S o discrimination t86 to +92

No discrimination +83 t o +96

_ I -

-0.8

-0.8 * 152 to + 159

+ I 7 2 to + I 8 0 -

-0.9

-0.9 + 1 6 0 t o - l 6 i

+296 t o -321 -

-0.4 +I92 t o +211

- 0 5 +249 to +260

-

Summar? of discrimination and detection thresholds l JSDsl of t h e same cats whrise lesionb are represented in Table 1 arranged here ~n groups based on behavioral deficits. The numbers in parentheses represent 1 S D variance. Minus and plus numbers a re pre- and postoperative days. respectively. in which t h e means were taken. The column on t h e right shows t h e contrast a t which detection was possible Pre- and postoperative JSDs were compared using a two-taded t test ' P < 0.05 " P < 0 01 - ' * P < 0 I101

at different lengths can be expressed either as thresholds in orientation or as difference in endpoint position using the formula D = L ( l - cos a ) /2 , where L is the bar length, a is the threshold in orientation, and D is the difference in endpoint position at threshold. Both measures can be plotted as a function of bar length. The fact that thresholds for one cue remain constant whereas thresholds for the other cue change for a given range of bar lengths indicates that, for that range, the animal used the former cue (De Weerd et al., 1990b).

Differing from the anatomical grouping (Table 11, the animals can be divided into three groups on the basis of

behavioral criteria (Table 2). The first group (n = 6 ) includes animals without postoperative retention deficit and with small, long-lasting effects. The second group (n = 2) includes animals with postoperative retention deficit and longer lasting effects than group 1. Animals in the third group (n = 3) never recovered postoperatively.

Figure 7 illustrates the mean performance of the six animals during pre- and postoperative testing. All six animals had a significant initial deficit (Table 2) when measured 2-8 weeks after the lesion. In all six animals, there was some recovery with time, and three cats recovered completely (cats 12,85, and 58). In the other three cats

Group 1.

40

w [L 0 w 2 3 0 -

J.M. SPRAGCE ET AL.

NO STIMULUS CONTROL

1

A CAT 69

3 0 1 .

-1'00 -00 -60 - i o -20 0 20 4b 60 I .

C CAT 66

W

0 a

25

20

15..

lo-0

5 .. O r

+v

..

.-

0 0 0

: 11'30 -1'00 - i o -40 - i o 20 50 60

E CAT 12 NO STIMULUS CONTROL

w 8 15

l o t 5 9 Q 04 I I -50 -40 -30 -20 -10 0 10 20 30 40 50

TIME ( DAYS )

Fig. 7. A-F: Thresholds (JNDs) of orientation discrimination at horizontal reference in cats 69, 85, 66, 58, 12, and 33 (Table 2) plotted as a function of time of testing before (negative numerals) and after surgery (designated by the vertical line at 0). Each dot represents the

(cats 69, 66, and 331, a small significant deficit of 40-65% increase in JND remained. In cat 85, threshold rose again at 10 weeks postoperatively of unknown causes, but it is not considered seriously here, because earlier postoperative thresholds were not different from DreoDerative thresholds.

B CAT 85 STIMULUS CONTROL

15

10

5

D CAT 58 NO STIMULUS CONTROL

F CAT 33 NO STIMULUS CONTROL

1 1 -10 0 10 20 30 40 50

TIME ( DAYS )

mean of six to ten test sessions (30 trials/session) that used standard parameters (bar length, 12"; width, 0.2"; contrast, 1.48). Vertical lines on the dots represent 1 S.D. unless variability was too small to show. Open symbols, preoperative; closed symbols, postoperative.

points of a pre-and postoperative staircase taken 1 day before and 60 days after the lesions, respectively. The postoperative JND was 3.7" compared to 3.9" preoperatively.

In all six animals, JNDs were measured postoperatively This is illustrated in Figure 8A, whch'shows the reversal at different contrast (Fig. 9) in order to assess more

EXTRASTRIATE CORTICAL AREAS AND ORIENTATION -11

A 40 1 30

15

10

CAT 85

0 5 10 15 20 25 30

B CAT 95

I 0 5 10 15 20 25 30

REVERSAL NUMBER

Fig. 8 Preoperative (open symbols) and postoperative (solid symbols, staircase measured in cat 85 (A) and cat 95 (B) . The orientation difference IS plotted as a function of the order of reversal points.

precisely the degree of deficit. Because no preoperative testing had been performed, the postoperative data of each cat were compared to those of a control population of four cats with an ANOVA. The results in cat 69 are typical of this group, in that JNDs were significantly increased postoperatively at a few (low as well as high) contrasts. A very similar pattern was observed in cats 12 and 33 and also in cat 66, although the deficits here were somewhat more numerous. The two animals in which contrast manipulations revealed the largest deficits were cats 85 and 58, in which postoperative performance was significantly worse than preoperative performance at most contrasts. In four of the animals (cats 69, 85, 58, and 12), the detection contrast thresholds were measured, and, in all four animals, those values were in the normal range (Table 2) .

In all six animals, JNDs were measured at different bar lengths (Fig. 10). In three cats (cats 66, 58, and 12), orientation discrimination had been tested a t different lengths preoperatively, and, in these animals, pre- and postoperative JNDs were compared using a t test at each length. For the other three cats, the postoperative data of each animal were compared to a normal control population using an ANOVA. Again, cat 69 was rather prototypical for the whole group. JNDs in orientation were increased postoperatively at a number of lengths, including several middle lengths (6-10"). The pattern was similar in the

other cats, with some variations: Cats 66 and 12 were the least affected, and cat 58 was the most affected.

The length data were replotted as threshold in distance between the endpoints as a function of bar length (see Fig. 1 lA, cat 33). Thresholds expressed in distance of endpoints steadily rose from 1" to 14" length, whereas thresholds expressed in orientation difference remained stable for lengths between 6" and 14" (Fig. 10F). This suggests that, at the standard length (12") and, indeed, for 6-14" lengths, this cat used orientation as a cue rather than using the position of the endpoints. In the other cats, distance thresholds rose generally between 4" or 6" and 10" or 12", whereas orientation thresholds remained constant in that range, suggesting that all cats in this group primarily used orientation as a cue for the standard length.

In conclusion, it is worth stressing that there was no clear correlation between the lesions and the behavioral deficit, in the sense that rather similar behavior corresponded to different lesions. For example, cat 33, which had the largest lesion of the six animals in this group, did not stand out behaviorally in any way. Perhaps the only exception is cat 12, in which the behavioral deficits were the smallest overall and in which the tier I1 lesions were the smallest, notably in areas 21a and 20a, where the area centralis was spared.

Cat 95 was tested preoperatively over a period of 25 days that ended 30 days before surgery, a t which time threshold was 6.8". Postoperatively, this animal had no retention for 82 days, after which his performance showed no consistent stimulus control for an additional 40 days, although thresholds on individual testing sessions ranged from 29" to 6.5". Cat 95 was tested finally at 126 days, at which time threshold was 15.3" (Fig. 12A, Table 2). Figure 8B illustrates staircase measurements in cat 95 taken 97 days before and 168 days after the lesion. Preoperative JND was 5.9" compared to 16.2" postoperatively. Detection threshold was raised, and discrimination thresholds were markedly elevated over the entire range of contrasts (Fig. 13A) and at all bar lengths except at 2" (Fig. 14A). Endpoint distance as a function of bar length (Fig. 11B) was marked different from controls but indicated that this cat used orientation as a cue a t all bar lengths except at 14".

Cat 98 was tested 110 days before surgery, at which time discriminative threshold was 5.7". After recovery from surgery, it was tested for 130 days. For the first 36 days of this test period, cat 98 showed no retention of discrimination. After the test period, performance came under stimulus control, and thresholds gradually decreased from about 30" to a final 13.8" almost 20 weeks after surgery (Fig. 12B, Table 2). Postoperatively, discrimination thresholds were in the normal range at high contrast but were significantly elevated a t 0.3 contrast, and no discrimination was possible at lower contrasts (Fig. 13B). Detection threshold was at - 1.3 contrast preoperatively compared to -0.5 contrast postoperatively (Table 2). Discrimination thresholds were significantly larger than preoperative values at all lengths (Fig. 14B).

Group 5. Cat 84 differed from the other two animals in this group, having a high preoperative threshold of 17.9" with considerable variability in discriminative performance. Postoperatively, no discrimination of bar orientation was possible in this animal over a period of 20 weeks

Group 2.


A CAT 69 f N O STIMULUS CONTROL in 1 -

5 L 2 5 t \ I 3 204 I

L3 5 5 ::!

04 v -2.000 -1.000 0.000 1.000 2.000

C CAT 66 I N O STIMULUS C O N T R O L n In 1

25. - 0 I-

z

0

2 20-

15--

z 10- n 5 5.-

0 1 1 -2.000 -1.000 0.000 1.000 2.000

E CAT 12 n In I N O STlL+JLUS CONTROL I

* 25.- 0 t-

Z w 0

3 20-

15--

z 10.-

7 5 0 z ..

01 v * -2.000 -1.000 0.000 1.000 2.000

C O N T R A S l

Fig. 9. A-F: JNDs measured as a function of different bar contrasts for the same six cats shown in Figure 7 compared to the JNDs of four normal controls (stippled areas). The isolated symbol above the abscissa is the detection threshold. Symbols along the postoperative curve

(Fig. 15A; Table 2). Postoperatively, cat 84 was also unable to perform a simple shape discrimination (square/circle) that had been learned before surgery (Fig. 16D). However, when it was tested for detection of one of the two discriminanda (square), this cat performed well at a surprisingly low threshold (size; Fig. 16B).

B CAT 85 N O STIMULUS C O N T R O L

04 v -2.000 -1.000 0.000 1.000 2.000

0 CAT 58 N O STIMULUS C O N T R O L

04 v 1 -5.000 -1.000 0.000 1.000 2.000

F CAT 33 I N O STIMULUS C O N T R O L

-2.000 -1.000 0.000 1.000 2.000

CONTRAST

indicate the results of the posthoc testing between the postoperative value and the control values at each contrast. Squares, P < 0.05; asterisks, P < 0.01; daggers, P < 0.001.

Cats 99 and 93 achieved lower thresholds preoperatively than 84, but, postoperatively, both animals failed in bar orientation discrimination (Fig. 15B,C; Table 2). Like cat 84, cats 99 and 93 also performed well in the shape- detection test (Fig. 16B) but failed the shape discrimination test (Fig. 16D).

EXTRASTRIATE CORTICAL AREAS AND ORIENTATION

30

43

NO STIMULUS CONTROL 0 .E

.-

- (n W W ci c3 W a

0

u

z

2 t- z w (L 0 z a z 7

- v) W W a

0

z b- 4 t- z

0

s v

0

w a z n f

- v) W W

a c3 W a

0

v

z t-

z E 0

2 LI1

z 0 z >

30 - I

25

20

15.-

10.-

5

A CAT 69

! NO STIMULUS CONTROL 0 0

-.

..

.-

B CAT 85 NO STIMULUS CONTROL

0 1 I 0 2 4 6 8 10 12 14 16

01 0 2 4 6 8 1 0 1 2 1 4

C CAT 66 0 CAT 58

04 1 0 2 4 6 8 10 12 14 16

E CAT 12

NO STIMULUS CONTROL

NO STIMULUS CONTROL I O T

01 0 2 4 6 8 1 0 1 2 1 4

F CAT 33

30 # I -- I

NO STIMULUS CONTROL

O J I

BAR LENGTH (DEGREES)

0 2 4 6 8 10 12 14 16

Fig. 10. A-F: JNDs measured as a function of bar lengths for the same six cats shown in Figures 7 and 9 compared to the preoperative data (open symhols), if available, or to the JNDs of four normal controls (stippled areas). Statistical testing was done using a two-tailed t test if

DISCUSSION This paper and preceding publications (Orban et al.,

1990; Vandenbussche et al., 1991; De Weerd et al., 1993, 1994) have sought to establish the contribution of different areas of the visual cortex to the perception and discrimina-

25

20 -.

15.-

10

5 - -

0 4 0 2 4 6 8 1 0 1 2 1 4


preoperative JNDs were available and using an analysis of variance (ANOVA) when comparison was made to normal control values (see Fig. 9 for descriptions).

oriented bars, oriented illusory contours, and textures composed of oriented bars.

The visual cortex in the cat lies in occipital, parietal, and temporal lobes and is composed of at least 18 areas in which visual information is processed, not counting the frontal eye fields (Rosenquist. 1985; UDdvke. 1986: Bowman and

tion of several types of visual k im& in the cat: simple Olson, 1988; Scannell and Yoing 1993; Vanduffel et al.,

44

- W v, W K 0 W

0 3 0 - v

6 25.- c 5 20.- LL’

z

7 5

15.-

9 l o ; ; +

O t

J.M. SPRAGUE ET AL.

rNO STIMULUS CONTROL 0 . 0 .

A

ln

n 1.500--

2 1.250.- n

1.000--

f 0.750.-

0,500--

0.250 -.

v

0

e

CAT 33 2.000 - 1.750

0.000 I I 0 4 8 12 16

8 CAT 95 2.000, - - 1.750.-

1.500- ln

n

0 8 1.250.-

1.000--

0.750.-

6 0.500-

v

0

2 ln

I 0.250t i 0.000 J I

0 4 8 12 16

BAR LENGTH ( DEGREES )

Fig. 11. Endpoint distance cue plotted as function of bar length for cat 33 (A) and cat 95 (B) compared to four normal controls (stippled areas).

1993). A serial concept of cortical organization has grown up that regards areas 17 and 18 as “primary” visual cortex in which the constituent neurons respond optimally to specific qualities of the stimuli, including edge orientation, and these responses are more sharply tuned than in other cortical areas (Orban, 1984). Using this concept of areas 17-18 as “primary” in both the anatomical and physiological sense, we have termed them tier I in the visual cortical hierarchy. They have an extensive cortical projection that is reciprocally organized, and we have termed the areas that receive direct projections from them tier 11. These tier I1 areas, in turn, project forward to other units of visual cortex that we term tier 111, which, again, are reciprocally organized.1

Although areas 17-18 receive afferents from all laminae of LGNd and from the intralaminar nuclei and the claustrum, they have an exclusive projection from laminae A and Al of the geniculate. Many of the tier I1 and I11 areas receive subcortical afferents from different laminae of the lateral geniculate nuclear complex and via parallel paths from the superior colliculus-pretectum via the thalamic lateral posterior-pulvinar thalamic nuclei, from the intralaminar nuclei, and from the claustrum (Rosenquist, 1985).

Our previous results have shown that cats with large lesions of tier I cortex had a long-lasting retention deficit of bar orientation discrimination followed by an extremely

A CAT 95

El CAT 98

-150-100 -70 -40 -10 20 50 80 110 140

TIME ( DAYS )

Fig. 12. JNDs in bar orientation discrimination in cat 95 (A) and cat 98 (B). See Figure 7 for descriptions.

slow recovery and by elevated thresholds (Orban et al., 1990; Vandenbussche et al., 1991). A subsequent study (De Weerd et al., 1993) using similar lesions but employing different training and testing procedures found no retention deficit but confirmed the presence of elevated thresholds after a more rapid recovery. Both groups of animals demonstrated that stable, low threshold discrimination of oriented bars is dependent on areas 17 and 18 but that the ability to discriminate these stimuli remains after removal of tier I cortex. However, performance is less stable,

‘The prevalent concept that areas 17-18 in the cat, or area 17 in other species including primates, is the “primary” visual cortex does not take into consideration the evidence from phylogenetic studies and comparative neurology showing that the extrastriate and tectofugal systems develop before the striate system (see Karten and Shimizu, 1989,1991). According to this view, area 17 or areas 17-18 in the cat might be considered to be a later cortical addition, and it is not surprising that not all of the visual input reaching the extrastriate cortices has to go through the “primary” cortex first. Certain important visually guided behaviors including basic perceptual and discriminative capacities remain after the removal of “primary” cortex (Diamond and Hall, 1969; Doty, 1971; Pasik and Pasik, 1971; Denny-Brown and Chambers, 1976; Diamond, 1976; Sprague et al., 1977, 1985; Berkley and Sprague, 1979; Kruger et al., 1986; Ptito et al., 1988). This does not imply that vision without “primary” cortex is qualitatively or quantitatively normal. These surviving functions are different in different mammalian species, depending a t least in part on the organization of the thalamocortical pathways.


- v) W W LL (3

45

vr W W

LL u W

NO STIMULUS CONTROL

0

30

B NO STIMULUS CONTROL

0 * - -

CAT 98

25

20

15

l o - -

5

I NO STIMULUS CONTROL - vr 1

- -

--

--

--

W W CY 0 W n v

z + Z w K 0

0 ;I

z n z 3

I I T 0

z

c 4 c z

LL 0

0

w

z n z 3

B CAT 98

04 I


0 2 4 6 8 10 12 14 16

CONTRAST

Fig. 14. JNDs measured as a function of bar lengths in cat 95 (Ai and cat 98 (Bi. Open circles, preoperative; solid circles, postoperative See Figure 10 for descriptions.

Fig 13. JNDs measured as a function of bar contrasts in cat 95 (A) and cat 98 (B) . Open symbols, preoperative; solid symbols, postoperative. See Figure 9 for descriptions.

requires higher contrast, and has an elevated threshold. These findings suggest that cortical areas beyond 17 and 18 take part in the discrimination of oriented bars. The present study documents this conclusion and presents several hypotheses on the role of extrastriate cortices in this function.

Area 7p, which was defined by Olson and Lawler (1987) as lying in the middle suprasylvian gyrus, was included in the lesions. Many cells in area 7p show purely visual responses, and others are related to saccades, to vergence, or to fixation and attention (Joseph and Giroud, 1986; Olson, 1991; Yin and Greenwood, 1992a,b). Lesions of this area impair depth perception in cats (Kruger et al., 1993). Because the area was removed completely in all animals, we feel that, in itself, it is not significantly related to the deficits described here.

The six animals of behavioral group 1 had somewhat different lesions. Four cats (69, 85, 66, and 58) belonged to group I anatomically with lesions restricted to areas 19, 21a, and 20a and to PMLS, whereas cats 12 and 33 were placed in group I1 because of additional involvement of VLS and DLS (in cats 12 and 33) and also of area 21b and PS (in cat 33). Thus, within behavioral group 1, there was no clear correlation between the lesion and the behavior. The cat

with the largest lesion (cat 33) falls right in the middle of the group when behavior is considered. Conversely, the cat that seemed most impaired (cat 58) had a lesion that was not larger than the other animals. The only weak correlation between behavioral performance and lesion was that the animal that was the least impaired (cat 12) had among the smallest lesions in group I; in particular, the removal of areas 21a and 20a was more limited and spared the area centralis representation in area 20a. Thus, one can conclude that areas 19, 7p, PMLS, 21a, and 20a and probably also VLS, DLS, and PS make only a minor contribution to our bar orientation discrimination task and that there is perhaps a slightly larger contribution from areas 21a and 20a.

I t is difficult to understand what the modest contribution of these areas might be. One possibility is that they provide additional indirect links between tier I and those tier I1 or I11 areas that are critical for the task. Removal of a number of these areas would reduce somewhat the strength of the links within the network underlying discrimination. A second possibility is that these areas provide inputs to those tier I1 and I11 areas critical for the discrimination but that these inputs do not carry signals relevant to the task and simply provide excitatory drive to the neurons in the critical areas.


A CAT 84 - NO STIMULUS CONTROL In

W w LT 0

0 0 . 0 0 . 0 . 0 W Q v

z P e Z

LT 0

2 w

-20 5 30 55 80 105 130

B CAT 99 NO STIMULUS CONTRGL ln w

W LT 0 W

0 0 . 0 0

o 30- v I

C CAT 93 - NO STIMULUS CONTROL

In W W LT 0

0 0 . 0 0 W

30 I 1

O J 1 1 -20 0 20 40 60 80

TIME ( DAYS )

Fig. 15. JNDs in orientation discrimination in cat 84 (A), cat 99 (B), and cat 93 (C; Table 2) plotted as a function of time of testing. See Figure 7 for descriptions.

Although the six cats of behavioral group 1 were only modestly impaired, the situation is very different in cats 95 and 98, both of which had marked postoperative deficits in discrimination and detection (group 2). The lesions in cat 95 differ from those of cat 33 in that thev showed a =eater

involvement of area 17 and of PLLS in tier I1 and showed less involvement in area 21b and in AMLS. The effects of the lesions in cat 95, however, were much greater than those in cat 33. An immediate temptation is to ascribe the cause of the greater deficit to the larger involvement of area 17. This explanation cannot be sustained for several reason: Our previous work (Orban et al., 1990; Vandenbussche et al., 1991) had shown that orientation discrimination of simple luminance-defined bars is represented almost equally in both area 17 and area 18. Lesions placed primarily in area 17 or in area 18 produced no deficit at our standard conditions and resulted in elevated thresholds only at low contrast and narrow bar width. Lesions in two cats placed primarily in area 17 that were as large or larger than in cat 95 but that spared considerable amounts of area 18 (as in cat 95) resulted in minimal deficits in bar orientation discrimination when tested at standard conditions. There- fore, the deficits seen in cat 95 were not due to involvement of area 17 alone but, rather, were due to the lesions in tier I1 (areas 19,21a, 20a, PMLS, and PLLS) and in tier 111 (areas VLS and DLS) probably together with the effect of lesions in area 17.

In the case of cat 98, the deficits were very likely the result of the extensive involvement of both area 17 and area 18 together with the near total lesions of areas 19,21a, 20a, and PMLS and the partial lesion of AMLS. The severity of atrophy in LGNd means that the surprising recovery seen in cat 98, in all likelihood, was mediated by other than this small surviving geniculocortical path, probably by the parallel pathway through the superior colliculus-pretectum via LP-pulvinar to surviving tier I1 (area 21b, PLLS, and AMLS) and tier 111 cortex (ALLS, VLS, DLS, and PSI. Both cat 95 and cat 98 showed a partial recovery of orientation discrimination, albeit with increased variability of performance and about a threefold increase in the threshold. In the case of cat 98, it is likely that the cortices involved in this recovery were crucial parts of tier I1 (PLLS and AMLS) and of tier I11 (ALLS and DLS), which receive afferents from the superior colliculus-pretectum via LP-pulvinar. The recovery of cat 95, however, may well have been mediated by area 18, which was largely intact, and by surviving parts of area 17, tier I1 (AMLS), and tier I11 (ALLS).

Interestingly, one of the main differences between cat 95 and cat 33 is the extensive lesion of PLLS in the former animal. The possibility that this area contributes to bar orientation discrimination is supported by a comparison of the deficits in cats 95 and 98 (group 2) to those in cats 84, 93, and 99 (group 3). Cats 95 and 98 showed a retention deficit in bar orientation discrimination followed by partial recovery, whereas cats 84, 93, and 99 were not able to perform any discrimination task but were able to perform a detection task.

A comparison between cats 84, 93, and 99 (group 3) on the one hand and cats 95 and 98 (group 2) on the other hand confirms a possible contribution of PLLS to bar crientation discrimination and also points to a function for AMLS and ALLS. Indeed, cats 93 and 99 had involvement of areas 17 and 18 almost equal to that of cat 98, yet they showed no discrimination during 13 weeks of testing. This deficit, which exceeded that of cat 98, appears to be due to the much greater involvement of tier I1 (PLLS and AMLS) and/or tier 111 cortex (ALLS, VLS, and DLS). Cat 84 led us to the same conclusion: Area 17 involvement is approximately the same as that in cat 95 (the lesion in cat 18 is


5- 5.

u” 4- 4 .

01

cl J 3 . 3 -

2. L - 2-

1 - 1-

0, 0

47

DETECT ION

4

1 2 3 4 5 6 7 0 9 1 2 3 4 5 6 7 8 9

SHAPE DISCRIMINATION C

normals N = 8

greater on one side), but extension of the lesions into tiers !I (AMLS) and I11 (ALLS, PS) cortex was considerably greater in cat 84. No discrimination was found in cat 84 over 20 weeks of postoperative testing. The data from these animals suggest the importance of PLLS, AMLS, and ALLS in bar discrimination.

We derived the possible function of PLLS, AMLS, and ALLS in bar orientation discrimination from the increases in behavioral deficits when these areas are damaged in addition to damage in a large number of other areas. We do not know whether removal of these areas alone would result in any significant deficit at all: Therefore, the question can be asked whether the neural mechanism involved in bar orientation discrimination in normal animals in- :ludes these areas. In other words, PLLS, AMLS, and ALLS nay be important for the recovery of orientation discrimina- ;ion after large visual cortex lesions, but they may be of imited importance in normals (at least for AMLS and 4LLS). A recent 2-deoxyglucose study by Vanduffel et al. 1993) suggests the contrary. These authors disconnected

me hemisphere by sectioning the ipsilateral optic tract, the :orpus callosum, and the anterior commissure and com- Jared metabolic activity in visual areas of the two sides of ,he brain during a bar detection task (n = 2), a bar rientation discrimination (n = 3). and a control condition

in which the cats were rewarded only for performing the same visuomotor behavior but without discriminanda (n = 2). The cortical areas in which the interhemispheric ratio of metabolic activity was significantly higher in the discriminating than in the normal controls included areas PLLS, ALLS, and AMLS. The present results and those of Vanduf- fel et al. (1993) suggest that areas 19, 20a, 21a, 21b, and PMLS are involved little in bar orientation discrimination, and the same may be said for tier I11 areas VLS, DLS, and 7p. In contrast, areas PLLS, ALLS, and AMLS appear to play a role in this discrimination in addition to that played by areas 17 and 18.

We do not know what the function is of areas PLLS, AMLS, and ALLS in bar orientation discrimination. Al- though it is mainly area PMLS that has been implicated in motion analysis (Spear and Baumann, 1975; Pasternak et al., 1989), areas PLLS and AMLS have also been implicated in the analysis of motion (Rauschecker et al., 1987; Toyama et al., 1990): Therefore, our conclusion that they contribute to bar orientation discrimination may seem surprising. However, this surprise is based on the assumption that the lesion deficits we observed after tier 11-111 lesions were linked specifically to the bar stimulus, which is question- able. It is possible that removal of PLLS, AMLS, and ALLS destrovs a more general function t,hat cnntrihut,es t,n t,his


discrimination task. Reorienting an object in space causes different parts of that object to take different positions relative to surrounding boundaries and objects (even if this object is only a bar). Because parietal cortex is important in coding the spatial relation between objects and parts of objects (Desimone and Ungerleider, 1989; Farah, 1990), discrimination between oriented objects may be impaired by parietal lesions, which has been suggested by a recent lesion study in the monkey (Eacott and Gaffan, 1991). Assuming that parietal cortex in the cat performs functions similar to those of other species, one could propose that the added deficit seen after lesions including PLLS, AMLS, and ALLS is due to the spatial component in the bar orientation discrimination task.

In addition, the same areas that may contribute to bar orientation discrimination in the way suggested above are also involved in the reorganization that takes place after damage to other parts of the visual system. Clearly, removing the areas that may be critical in the reorganization after damage to other visual cortical area will increase the deficit. We do not know what processes are involved in this reorganization, but a comparison of the studies from De Weerd et al. (1993) and Vandenbussche et al. (1991) may give us a clue. Vandenbussche et al. (1991) demonstrated severe deficits following large lesions in both area 17 and are 18. Not only was there no postoperative retention for prolonged periods, but, when the capacity to discriminate returned, it was at a much elevated threshold and was present only when tested with long bars and high contrast. De Weerd et al. (1993) trained their animals with a differential exposure method (DEM; De Weerd et al., 1990a) rather than an equal exposure method (EEM) and measured threshold using a staircase procedure (De Weerd et al., 1990~) rather than using the method of constant stimuli. They were trained first for bar orientation discrimination using the methods in the present study followed by discrimination of two illusory contours. Three cats received large lesions in areas 17 and 18 (comparable to those in Vandenbussche et al., 1991). Postoperative testing followed the same sequence, and, under these conditions, there was no retention deficit of bar discrimination, although thresholds were elevated, and performance was more variable. The fact that the deficits were significantly less marked than in the earlier study could be due to the differences in training and testing methods. However, an equally plau- sible explanation is that the training in illusory contour orientation discriminations preoperatively taught the animals the efficient use of the grouping mechanisms essential to reconstruct contours. After a lesion in areas 17-18, these animals might successfully apply these grouping mechanisms on the direct unoriented input reaching almost all tier I1 and tier I11 areas from the C-laminae of the LGN and other subcortical structures (Rosenquist, 1985). In view of this, cats with area 17-18 ablations and without training in the discrimination of illusory contours recover more slowly because they have to develop these efficient grouping mechanisms postoperatively. This hypothesis is now being tested in a new group of cats. Interestingly, Spear and Baumann (1979) have shown changes in neuronal responses in LS cortex consistent with an increased function in the analysis of stationary stimuli after lesions in areas 17, 18, and 19 (note that our strongest argument for the contribution of PLLS, AMLS, and ALLS comes from animals with severe damage to areas 17,18, and 19 or damage to areas 17 and 19). %ear and Baumann (1979) did not find

changes in orientation selectivity in LS neurons, but their animals were not involved in any behavioral task.

Finally, many units of tiers I1 and 111 project to the motor mechanisms in the striatum (Updyke, 1993) and to the intermediate and deep layers of the superior colliculus (Sprague, 1975; Huerta and Harting, 1984; Harting et al., 1992). Thus, in cats 84, 93, and 99, where the total lack of discrimination could not be explained by near complete destruction of tier I alone, extensive damage in tier I1 and tier 111 and the resulting disconnection from motor structures might have caused the discrimination deficit. Note that detection remained possible in animals with tier I partly spared but with extensive damage in tiers I1 and I11 and even in animals with most of visual cortex removed. This suggests that visual input guiding a detection task reaches motor structures via a pathway different from the pathway involved in a discrimination task. Indeed, retinal input reaches the superficial (sensory) laminae of the colliculus directly (Laties and Sprague, 1966; Rosenquist, 1985) or via areas 17-18 (Garey et al., 1968; Palmer et al., 1972; Kawamura et al., 1974; Updyke, 1977; Huerta and Harting, 1984), which have only a minimal projection to the striatum (Royce, 1982; Updyke, 1993). Output from the colliculus to motor structures (Huerta and Harting, 1984; Grantyn and Berthoz, 1985; Sparks and Hartwick-Young, 1989; McIlwain, 1991) may be sufficient to guide a detection task. Indeed, Vanduffel et al. (1993) obtained evidence that the visual system uses different outlets to the motor system in detection and discrimination tasks.

Although previous studies from this laboratory (Vanden- bussche et al., 1991; Orban et al., 1990; De Weerd et al., 1993) have shown an important role of areas 17 and 18 in the filtering of bar orientation and in the sensorial representation of bar orientation, the present study indicates that visual cortex beyond areas 17 and 18 contributes to discrimination tasks that make use of that representation. Com- bined evidence from this lesion study and the 2-deoxyglucose study of Vanduffel et al. (1993) suggest a possible role for PLLS, AMLS, and ALLS. A combination of physiological and behavioral approaches will be required to pinpoint the function of these areas in orientation discrimination of a luminance bar.

ACKNOWLEDGMENTS The authors thank C. Fransen for help with the training

and testing of the animals. We appreciate the skilled technical support of G. Vanparrijs, G. Meulemans, P. Kayenbergh, and Y. Celis. For the histological preparations, we thank W. Algeo. P.D.W. held a National Fonds voor Wentenschappelijk Onderzoek (NFWO) aspirant mandate and a junior research fellowship from the Research Council of the University of Leuven. This work was supported by grants from the University of Leuven Research Council and the NFWO to G.A.O., by grant IUAP-22 Vision and Memory from the Federal Ministry of Science to G.A.O., and by a grant from the Research Foundation of the University of Pennsylvania to J.M.S.

LITERATURE CITED Barlow, H.B. (1972) Single units and sensation: A neuron doctrine for

perceptual psychology? Perception 1 ;37 1-394. Berkley, M.A. (1970) Visual discriminations in the cat. In W. Stebbins (ed.):

Animal Psychophysics: The Design and Conduct of Sensory Experi- ments. New York: Amleton Centurv-Crofts. nn. 231-247.

Berkley. M.A., and J.M. Sprague f 19791 Striate cortex and visual acuity functions in the cat. J. Comp. Neurol. 187.697-702.

Bowman. R.M.. and C.R. Olson (19881 Visual and auditory association areas of the cat’s posterior ectosylvian gyrus: Cortical afferents. J. Comp. Neurol. 27230-42.

De Weerd, l’., E. Vandenhussche, and G.A. Orban 11990al Speeding up visual discrimination learning in cats by differential exposure of positive and negative stimuli. Eehav. Brain Res. 36:1-12.

I)e Weerd. P.. E. Vandenhussche, and G.A. Orban (1990hl Bar orientation discrimination in the cat. Visual Neurosci. 4257-268.

De Weerd. P., E. Vandenbussche, and G.A. Orhan l1990cl Staircase procedure and constant stimuli method in cat psychophysics. Behav. Brain Res. 40:201-214.

De Weerd, P., J.M. Sprague, S. Raiguel, E. Vandenbussche, and G.A. Orhan (1993, Effects of visual cortex lesions on orientation discrimination of illusory contours in the cat. Eur. J . Neurosci. 5:1695-1710.

De Weerd. P.. J.M. Sprague, E. Vandenhussche, and G.A. Orhan 11994) Two stages in visual texture segregation: A lesion study in the cat. J . Neurosci. 14.929-948.

Denny-IIrown. D., and R.A. Chambers (19761 Physiological aspects of visual perception. I. Functional aspects of visual cortex. Arch. Neurol. 33.219- 242.

Desimone, R., and L.G. Ungerleider 11989) Neural mechanisms of visual processing in monkeys. In F. Boller and J . Grafman (eds.1: Handbook of Neuropsychology, Vol. 2. New York: Elsevier, pp. 267-299.

Diamond. 1.7. I19761 Organization ofthevisual cortex: Comparative anatomical and behavioral studies. Fed. Proc. 35.60-67.

Diamond. L‘K, and W.C. Hall ( 19691 Evolution of neocurtex. Science 164:25 1-262.

Doty, R.W. 1971) Survival of pattern vision after removal of striate cortex in the adult cat. J. Comp. Neurol. 143:341-370.

Eacott. M.J., and D. Gaffan (19911 The role of monkey inferior parietal cortex in visual discrimination of identity and orientation of shapes. Behev. Brain Res. 46:95-98.

Farah. M.J. (19901 Visual Agnosia: Disorders of Object Recognition and What They Tell us About Normal Vision. Cambridge, MA: The MIT Press.

Garey. L J . . E.G. Jones, and T.P.S. Powell (19681 Interrelationships of striate and extrastriate cortex with the primary relay sites of the visual pathway. J . Neurol. Neurosurg. Psychiat. 31:135-157.

Georgopoulos, A.P.. A.B. Schwartz, and R.E. Kettner 119861 Neuronal population coding of movement direction. Science

Chantyn, A.. and A. Berthoz (19851 Burst activity of identified tecto-reticulo- spinal neurons in the alert cat. Exp. Brain Res. 57:417-421.

Harting. J .K.. B.V. Updyke, and D.P. van Lieshout (19921 Corticotectal pro.jections in the cat: Anterograde transport studies of twenty-five cortical areas. J . Comp. Neurol. 324.379-411.

Huhel, I).H., and T.N. Wiesel 119591 Receptive fields of single neurones in the cat’s striate cortex. J. Physiol. (London) 148:574-591.

Huerta, M.F., and J.K. Harting 119841 The mammalian superior colliculus: Studies of its morphology and connections. In H. Vanegas (ed. 1: Compara- tive Neurology of the Optic Tectum. New York: Plenum Press, pp. 687-77X

Joseph. J .P. . and P. Giroud (19861 Visuomotor properties of neurons of the anterior suprasylvian gyrus in the awake cat. Exp. Brain Res. 62.355- 362.

Karten. H.J. , and T. Shimizu (1989) The origin of neocortex: Connections and lamination as distinct events in evolution. J . Cogn. Neurosci. 1:291-301.

Karten. H.J., and T. Shimizu 11991) Are visual hierarchies in the brains of the beholders? Constancy and variability of the visual system of birds and mammals. In P . Bagnoli and W. Hodos (eds.): The Changing Visual Systtsm. New York: Plenum Press, pp. 51-59.

Kawamura. S., J.M. Sprague, and K. Niimi 11974) Corticofugal projections from the visual cortices to the thalamus, pretectum and superior colliculus in the cat. J . Comp. Neurol. 1581339-362,

Kruger, K., H. Heitlander-Fansa, H. Dinse, and G. Berlucchi 119861 Detec- tion performance of normal cats and those lacking areas 17 and 18: A behavioral approach to analyze pattern recognition deficits. Exp. Brain Res. 63:233-247.

Kruger. K.. W. Kiefer, and A. Groh f 19931 Lesion of the suprasylvian cortex impairs depth perception of cats. Neuroreport 4.883-886.

Laties, A.M., and J.M. Sprame (19661 The prqjection of optic fibers to the

McIlwain, J .T. (1991 I Distributed spatial coding in the superior colliculus: A review. Visual Neurosci. 6.3-13.

Olson, C.R. 119911 Area 7 and the spontaneous capture of attention by unexpected stimuli. Soc. Neurosci. Ahstr. 17:1282.

Olson, C.R., and K. Lawler (1987) Cortical and suhcortical afferent connections of a posterior division of feline area 7 (area 7pl. J . Comp. Neurol. 2Fi9r13-30.

Orhan, G.A. (1984) Neuronal Operations in the Visual Cortex. Berlin: Springer-Verlag.

Orban, G.A., H. Kennedy, and H. Maes 11981al Response to movement of neurons in areas 17 and 18 of the cat: Velocity sensitivity. J. Neuro- physiol. 4.5: 1043-1058.

Orhan, G.A., H. Kennedy, and H. Maes (1981bl Response to movement of neurons in areas 17 and 18 of the cat: Direction selectivity. J. Neuro- physiol. 45: 1059-1073.

Orhan. G.A.. E. Vandenhussche, and R. Vogels (1984) Human orientation discrimination tested with long stimuli. Vision Res. 24:121-128.

Orhan, G.A., E. Vandenhussche, J.M. Sprahqe, and P. De Weerd (1990) Orientation discrimination in the cat: A distributed function. Proc. Natl. Acad. Sci. USA 87:1134-1138.

Otsuka, It., and R. Hassler (1962) Uher Aufbau und Gliederung der corticalen Sehsphiire hei der Katze. Arch. Psychiat. Z. Ges. Neurol. 203:212-234.

Palmer, L.A., A.C. Kosenquist, and J.M. Sprague 119721 Corticotectal systems in the cat: Their structure and function. In T.L. Frigesi, E. Rinvik, and M.D. Yahr feds.1: Corticothalamic Projections and Sensori- motor Activities. New York: Raven Press, pp. 491-523.

Palmer, L.A., A.C. Rosenquist, and R.J. ‘I’usa 119781 The retinutopic organization of lateral suprasylvian visual areas in the cat. J . Comp. Neurol. 177.237-256.

Pasik, T., and P. Pasik (19711 The visual world of monkeys deprived of striate cortex: Effective stimulus parameters and the importance of the accessory optic system. Vision Res. 3:S419-S435.

Pasternak, T.. K.M. Horn, and J.H.R. Maunsell (19891 Deficits in speed discrimination following lesions of the lateral suprasylvian cortex in the cat. Visual Neurosci. 6365-375.

Ptito. M., F. Lepore, F. Tremblay, and J.-P. Guillemot (19881 Initial acquisition ofvisual discriminations following selective cortical lesions in cat. J . Hirnforsch. 29279-287.

Rauschecker, J.P.. M.W. von Grunau. and C. Poulin 119871 Centrifugal organization of direction preferences in the cat’s lateral suprasylvian visual cortex and its relation to flow field processing. J . Neurosci. 7.943-958.

Rosenquist, A.C. 119851 Connections of visual cortical areas in the cat. In A. Peters and E . G Jones leds.): Cerebral Cortex, Vol. 3. New York: Plenum Press, pp. 81-1 17.

Royce, G.J. f 1982) Laminar origin ofcortical neuruns which project upon the caudate nucleus: A horseradish peroxidase investigation. J. Comp. Neurol. 205.8-29.

Sanderson, K.J. 119711 The projection of the visual field to the lateral geniculate and medial interlaminar nuclei in the cat. J. Comp. Neurol. 143: 101-1 18.

Sanides, F., and J. Hoffmann 119691 Cyto- and myeloarchitecture of the visual cortex of the cat and of the surrounding integration cortices. J . Hirnforsch. 11:79-104.

Scannell, J .W., and M.P. Young I19931 The connectional organization of neural systems in the cat cerebral cortex. Curr. Bid. 3:191-200.

Sparks, D.L., and K. Hartwick-Young (19891 The deep layers of the superior colliculus. In R. Wurtz and M. Goldherg (eds.1: The Neurohiology of Saccadic Eye Movements. New York: Elsevier, pp. 213-255.

Spear, P.D., and T.P. Baumann 11975) Receptive field characteristics of single neurons in lateral suprasylvian visual area of the cat. J. Neuro- physiol. 98:1403-1420.

Spear, P.D., and T.1’. Baumann (19791 Effects of visual cortex removal on receptive-field properties of neurons in lateral suprasylvian visual area of the cat. J. Neurophysiol. 42:31-56.

Sprague, J.M. 119751 Mammalian tectum: Intrinsic organization. afferent inputs. and intepxtive mechanisms. In D. Ingle and J.M. S p r a y e Ieds.1: Sensorimotor Function of Midbrain Tectum. Neurosci. Res. Prog. Bull. 13:204-215

Sprabwe, J.M., J . I,evy, A. DiBerardino, and G. Uerlucchi 11977) Visual cortical areas mediating form discrimination in the cat. J . Comp. Neurol.

EXTRASTRIATE CORTICAL AREAS AND ORIENTATION 49

visual centers in the cat. J . Comp. Neuroi. 127:35-70. 17244 1-488.


Sprague, J.M., G. Berlucchi, and A. Antonini (1985) Immediate postoperative retention of visual discriminations following selective cortical lesions in the cat. Behav. Brain Res. 17.145-162.

Sprague, J.M., P. De Weerd, E. Vandenbussche, and G.A. Orban (1993) Orientation discrimination in the cat and its cortical loci. In T.P. Hicks, S. Molotchnikoff, and T. Ono (eds.): Progress in Brain Research, Vol. 95. Amsterdam: Elsevier, pp. 381-400.

Toga, A.W., B.S. Layton, and S. Horenstein (1979) Visuallydirected behavior is influenced by the posterior ectosylvian gyrus in the cat. Brain Res. 178306-608.

Toyama, K., K Fujii, and K. Umetani (1990) Functional differentiation between the anterior and posterior Clare-Bishop cortex of the cat. Exp. Brain Res. 81:221-233.

Tusa, R.J., L A Palmer, and A.C. Rosenquist (1978) The retinotopic organization of area 17 (striate cortex) in the cat. J. Comp. Neurol. 177,213-236.

Tusa, R.J., A.C. Rosenquist, and L.A. Palmer (1979) Retinotopic organization of areas 18 and 19 in the cat. J. Comp. Neurol. 185,657-678.

Tusa, R.J., L.A. Palmer, and A.C. Rosenquist (1981) Multiple cortical visual areas. Visual field topography in the cat. In C.N. Woolsey (ed.): Cortical Sensory Organization, Vol. 2. Clifton, NJ: Humana Press, pp. 1-31.

Updyke, B.V. (1977) Topographic organization of the projections from cortical areas 17, 18, and 19 onto the thalamus, pretectum and superior colliculus in the cat. J. Comp. Neurol. 17333-122.

Updyke, B.V. (1986) Retinotopic organization within the cat’s posterior suprasylvian sulcus and gyrus. J. Comp. Neurol. 246.265-280.

Updyke, B.V. (1993) Organization of visual corticostriatal projections in the

cat, with observations on visual projections to claustrum and amygdala. J. Comp. Neurol. 327.159-193.

Van Essen, D.C., and J.H.R. Maunsell (1980) Two-dimensional maps of the cerebral cortex. J. Comp. Neurol. 191.255-281.

Vandenbussche, E., G.A. Orban and H. Maes (1986) Velocity discrimination in the cat. Vision Res. 26,1835-1849.

Vandenbussche, E., J.M. Sprague, P. De Weerd, and G.A. Orban (1989) Effect of higher cortical ablations on cat orientation discrimination. Soc. Neurosci. Abstr. 15,1255.

Vandenbussche, E., J.M. Sprague, P. De Weerd, and G.A. Orban (1991) Orientation discrimination in the cat: Its cortical locus. I. Areas 17 and 18. J. Comp. Neurol. 305.632-658.

Vanduffel, W., E. Vandenbussche, W. Singer, and G.A. Orban (1993) Bar orientation discrimination in the cat: A 2-deoxyglucose study. SOC. Neurosci. Abstr. 19,772.

Vanduffel, W., E. Vandenbussche, W. Singer, and G.A. Orban (1995) Metabolic mapping of visual areas in the behaving cat: A P4C12- deoxyglucose study. J. Comp. Neurol. 354.161-180.

Vogels, R. (1990) Population coding of stimulus orientation by striate cortical cells. Biol. Cybern. 64.25-31.

Wetherill, G.B., and R. Levitt (1965) Sequential estimation of points on a psychometrical function. Br. J. Math. Stat. Psychol. 18:l-10.

Yin, T.C.T., and M. Greenwood (1992a) Visual response properties of neurons in the middle and lateral suprasylvian cortices of the behaving cat. Exp. Brain Res. 88:l-14.

Yin, T.C.T., and M. Greenwood (1992b) Visuomotor interactions in responses of neurons in the middle and lateral suprasylvian cortices of the behaving cat. Exp. Brain Res. 88:15-32.

Documents

Orientation discrimination in the cat: Its cortical locus II. Extrastriate cortical areas