Receptive-field characteristics of single neurons in lateral suprasylvian visual area of the cat.

Receptive-Field

Characteristics of Single Neurons in

Lateral Suprasylvian Visual Area of the Cat PETER

D. SPEAR

AND

THOMAS

P. BAUMANN

Department of Psychology, Kansas State University,

Manhattan,

THE LATERAL SUPRASYLVIAN Visual Cortex (LS, or Clare-Bishop area) is an integral part of the visual system of the cat. Among its known afferents is a direct retinothalamic input via the medial interlaminar nucleus (MIN) of the dorsal lateral geniculate body (LGD) (26,39,54). The LS area also receives inputs from the posterior nucleus (PN) and the lateral posterior nucleus (LP) of the thalamus (5, 11, 14, 26, 30, 39), and these nuclei each receive visual system inputs from the superior colliculus (1, 10, 12, 23, 32) and from visual cortical areas 17, 18, and 19 (8, 10, 12, 23, 24, 31). The LS area also receives bilateral corticocortical projections directly from areas 17, 18, and 19, as well as an input from the contralateral LS area (8, 14, 20, 22, 42-44, 53). Thus, among its inputs, the LS area is a major point of convergence of the tectothalamic and geniculostriate visual systems, as well as receiving a direct retinothalamic input of its own. Early evoked-potential studies and later single-unit experiments showed that at the midportion of the middle suprasylvian sulcus, the LS area lies on the medial bank of the sulcus from approximately the dorsal lip down to the fundus (6, 21, 27, 50, 56). Further, within a narrow anteriorposterior region explored (from stereotaxic coordinates A4-A6), Hubel and Wiesel(2 1) showed that a visuotopic organization is present. These studies did not determine the anterior-posterior extent of the LS area, nor was its visuotopic organization determined beyond the midportion of the middle suprasylvian sulcus. However, anatomical studies of the pattern and extent of LS area afferent terminations Received

for

publication

May

7, 1975.

Kansas 66506

suggest that the anterior-posterior extent of the LS area may be quite large, including much of the middle and posterior suprasylvian sulci (14, 22, 30, 39, 43). Two reports of the receptive-field properties of cells in the midportion of the LS area have appeared previously (2 1, 56). The receptive-field properties were reported to be similar to the orientationselective complex and lower order hypercomplex receptive fields described for cells in area 17, 18, and 19 by Hubel and Wiesel (18,20), although the receptive fields of LS area cells were much larger (2 1, 56). The present paper reports a further investigation of the receptive-field characteristics of the LS area cells, including a number of properties not previously studied. In addition, all of the middle suprasylvian sulcus and much of the posterior suprasylvian sulcus was explored in an attempt to determine electrophysiologically the extent of the LS area and to learn more about its visuotopic organization. METHODS Animal preparation Adult cats of either sex were used in the experiments. An initial preparation was performed 3-7 days prior to the recording session. At this time, the cat was anesthetized with pentobarbital sodium and placed in a stereotaxic instrument. Two bolts, held in a specially constructed attachment to the stereotaxic instrument, were cemented to the skull with dental acrylic. A 6-mm trephine hole was started over the lateral suprasylvian sulcus on each side. At the beginning of the recording session, the cat was anesthetized with Fluothane in 50% 0450% N,O. Either a tracheotomy was performed or the cat was intubated. The animal was paralyzed by an intravenous injection of 40 mg of gallamine triethiodide followed by continu1403

ownloaded from www.physiology.org/journal/jn by ${individualUser.givenNames} ${individualUser.surname} (132.174.254.155) on November 30, 201 Copyright © 1975 the American Physiological Society. All rights reserved.

1404

P. D. SPEAR

AND

ous infusion at a rate of 28 mg/h. The cat was artificially ventilated, and end-expired CO2 was closely monitored with a Beckman LB-l or LB-2 medical gas analyzer and maintained at 4.00/o. The head was rigidly held in stereotaxic coordinates by use of the bolts previously attached to the skull, without the use of ear, eye, or pressure bars. This left the entire visual field free of obstruction. The previously started trephine holes were completed through the skull and enlarged if necessary for multiple-penetration mapping studies. The dura was reflected, and agar-gel was applied over the skull openings. In some experiments the cisternurn magnum was drained to increase recording stability. Body temperature was maintained at 38OC with a heating pad, and the ECG was monitored continuously. All wound edges were coated with a longacting local anesthetic (Anucaine). During recording, Fluothane was discontinued and the cat was anesthetized with 25% 02/75% N20. The pupils were dilated by topical application of 1% atropine sulfate and the nictitating membranes retracted with 10% phenylephrine hvdrochloride. The corneas were proiected with zero power contact lenses. A tangent screen, 91 cm wide and 83 cm high, was placed 57 cm from the approximate nodal point of each eye. The eyes were refracted and the optic discs were projected and plotted on the tangent screen using the method of Fernald and Chase (7). Spectacle lenses were used to focus the eyes on the tangent screen plane. The tangent screen could be moved into any position along a semicircle with a radius of 57 cm from either eye while its surface remained tangent to the semicircle. This made it possible to map receptive fields virtually anywhere in the visual field. When the tangent screen was moved, the optic discs were replotted as reference points. Recording Single-cell activity was recorded with electrolytically sharpened tungsten microelectrodes insulated with Isonel varnish and having impedances of 3-5 Ma (tested with a 0.5 ms duration square-wave input). Activity was led into a Grass HIP51 1 high-impedance probe and then into a Grass P511 AC preamplifier. Action potentials were monitored with an audio monitor and displayed on an oscilloscope. Some records were stored with a Honeywell 8100 eight-channel FM tape recorder for future analysis, along with appropriate stimulus markers and verbal information on a voice channel. Poststimulus time histograms (PSTH) of cellular responses to repeated stimuli were produced using an Ortec 4620/462 1 time-histogram analyzer.

- . v-w w. m*_v -1. -Y. BAUMANN

Action potentials thought to arise from cell bodies were distinguished from nerve axon spikes by waveform criteria described by Bishop, Burke, and Davis (3). The present results concern cell body recordings only. Visual stimulation Light and dark visual stimuli of virtually any size and shape could be projected onto the tangent screen. Light stimuli were projected from a hand-held Keeler Pantoscope or with an overhead projector. They ranged in luminance from - 1.25 log cd/m2 to 0.0 log cd/m2. Background tangent screen luminance typically was - 1.5 log cd/m2, although a luminance of -0.25 log cd/m2 sometimes was used as well. Dark stimuli were shadows of - 1.0 log cd/m2 luminance projected onto a tangent screen of -0.25 log cd/m2 luminance. Receptive fields of the cells first were mapped using hand-held stimuli and the response was judged by listening to the audio monitor. For some of the cells, quantitative analysis of the responses to repeated stimulus presentations was subsequently made. Repeated presentation of stationary or moving stimuli was provided by means of an automated visual stimulator (35). Histology The location of the electrode tip was marked with small electrolytic lesions at two or three positions in the last penetration in each hemisphere studied. At the end of the experiment, the cat was given a lethal dose of pentobarbital sodium and perfused through the heart with 0.9% saline followed by 10% formal-saline. The brain was blocked, frozen-sectioned serially at 52 pm, and stained with cresyl violet. Every penetration for which data are reported was located histologically. Brain shrinkage was calculated from the distance between the electrolytic lesions. The shrinkage and the positions of the lesions were correlated with microdrive readings made during recording and used to reconstruct the positions of the cells along the penetrations. RESULTS

Receptive-Jield classes and their characteristics

The receptive-field properties of 213 visually responsive cells were studied in 24 cats. The responsive cells could be grouped into one of four classes according to their response properties. SELECTIVE. Eighty-one (172/2 13) of the cells gave a re-

DIRECTIONALLY

percent


LATERAL

SUPRASYLVIAN

VISUAL

AREA

The vast majority (92%) of the directionally selective cells gave their maximal response to a stimulus moving in a single preferred direction (plus or minus some range, as described below) and showed inhibition or no response to movement in the opposite (null) direction. A small number of cells (3%) had a preferred direction, but continued to give a very weak response to all other directions (directional preference cells). The remainder of the directionally selective cells (5%) gave nearly equal responses to stimulus movement in two oppo-

sponse which was dependent on the direction of stimulus movement through the receptive field (Figs. 1 and 3). About half of these cells gave no response to stationary stimuli of any sort flashed on or off. The remainder gave only weak or inconsistent transient responses to stationary stimuli flashed on, or off, or both. The response to stationary stimuli was homogeneous throughout the receptive field. In every case, the response to stimuli moving in the txeferred direction was better than that to Stationary stimuli.

NA 35-23

NA 26-15

2 L-

2I 40

A

I

B

0

C

I

0

20

0 0 0

* * *

-

c -J--.----I-

-*** rz”--wc“U---=-‘~*--~

&L,nm

0

E

0 0 0 FIO

CO * *- .* -.

l

0

--,-*

-,w-h-.r-

I

D

1405

-

I-

.c...“-:*~-~

_

-

-

-

-

D I E/

I

0

* -AT**

.

.--

-

. **--

-.. _

.-b--- - -dLvL-u---,

FIG. 1. Responses of two directionally selective cells to stimuli of different sizes and shapes. Each PSTH starts with the onset of stimulus motion and ends with the return of the stimulus to its starting position after passing through the receptive field in the preferred and null directions. Position of the receptive field in the sweep and directions of stimulus movement shown above. Horizontal calibration: distance traversed by the stimulus. Vertical calibration: spikes per bin. Left (NA 35-23): this cell showed slight spatial summation to increases in stimulus size (A, C, E and B, D, F-note especially the early discharge peak). However, stimulus shape had no effect on the response when stimulus size was kept constant (i.e., spot diameter equals slit length: A-B, C-D, and E-F). Sum of 12 stimulus sweeps in each PSTH. Stimulus velocity, 44”/s. Receptivefield size, 17.5 x 16.5”. Stimulus size: A, 4 x 1.5”; B, 3.5”; C, 7 x 2”; D, 6.5”; E, 16.5 x 3.5”; F, 16.5”. Right (NA 26-15): this cell also showed spatial summation (A, B); however, the maximum stimulus size was less than the activating region of the receptive field (B-C, D-F). In this case a spot produced a somewhat greater response than a slit (C-D). Changing the orientation of the slit by 45” without changing the direction of movement had little effect on the discharge of the cell (D-E). Sum of 10 stimulus sweeps. Stimulus velocity, 28”/s. Receptivefield size, 10.5 x 7’. Stimulus size: A, 0.75”; B, 1.5”; C, 3”; D, 3 x 0.5”; E,, 3 x 0.5”; F, 8 x 0.5”.


P. D. SPEAR

AND

site directions along an axis through the receptive field and gave no response to movement orthogonal to the preferred axis (axial directional cells). The directional selectivity was not due to subareas or receptive-field asymmetries. The same direction-specific response was obtained regardless of the location of a small stimulus within the activating region of the receptive field. Further, the preferred direction was never changed by reversing the contrast of a stimulus edge from dark-light to light-dark. The majority of cells (90%) responded to both darklight and light-dark edges moving in the preferred direction, though in a few cases only dark-light (6%) or light-dark (4%) borders produced a response. A few’ direction-selective cells were seen which only responded to dark-shadow stimuli on the tangent screen, and five cells gave little or no response to any stimuli on the tangent screen but gave brisk responses to an object moved close to the head in the preferred direction. Stimulus size was an important parameter in determining the magnitude of response of most directionally selective cells (Fig. 1). About half of the cells responded well to spots of 0.5’ diameter or less. Many cells (37%) required stimuli l-3” in diameter, and in some cases (10%) stimuli as large as 5-7” diameter were required to produce a response. Eighty-seven percent of the directionally selective cells showed spatial summation within the activating region of the receptive field so that once a response was obtained, its magnitude increased with increasing stimulus size. In most cases spatial summation continued up to the size of the receptive field (Fig. 1, left), and in others it did not (i.e., the optimum stimulus size was smaller than the activating region of the receptive field). For 32% of the directionally selective cells, an inhibitory mechanism was present which placed an upper limit on the size of an optimal stimulus. This could occur in cells with or without internal spatial summation. Two types of inhibitory mechanisms were seen. In some cases (15% of those with inhibition), the maximum response was obtained for stimuli smaller than the activating region of the receptive

T. P. BAUMANN

field, and further increases in size within the activating region resulted in a decreased response (Fig. 1, right). Thus, these cells appeared to have mutually inhibitory areas within the activating region of the receptive field. For other cells (85% of those with inhibition), the inhibition was seen only when the stimulus extended beyond the activating region of the receptive field into its surround region (Fig. 2). No response was ever obtained from stimulation of the surround alone. We found little or no evidence that cells in the LS area are sensitive to variations in stimulus shape. Since the two previous studies (2 1,56) reported that cells in the LS area were orientation selective, we analyzed this parameter very carefully after our initial experiments suggested that they were not. Orientation selectivity was assessed in three ways: 1) Response magnitudes were compared for spot versus slit stimuli moving in the preferred direction through the receptive field. The curved leading and trailing edges of a spot stimulus contain all possible orientations as long as the spot diameter is equal to or smaller than the receptive field. Nevertheless, if a spot stimulus was employed with a diameter equal to the length of a slit moved perpendicular to its orientation, the responses to the two stimuli typically were the same. In addition, changes in spot diameter had the same effect on the cells’ discharges as changes in the length of an oriented slit (Fig. 1). Thus, the spatial summation was not restricted to increases in length along a single axis of orientation. These comparisons were made for 113 directionally selective cells. About 90% responded equally to slits and spots of the same size and showed the same spatial summation to both types of stimuli. About 5% responded better to slits than to spots of the same size and could be considered orientation selective by this criterion. The remaining 5% responded better to spots than to slits of the same size (e.g., Fig. 1, right; and Fig. 3, cells NA 34-19 and NA 20-10). Changing the orientation of a slit moving through the receptive field in the preferred direction by up to 45” also had little effect on response magnitude of the cells (Fig. 1, right). Slit length was kept less


LATERAL

SUPRASYLVIAN

VISUAL

NA 5-14

AREA

1407

NA 35-19

B

FIG. 2. Demonstration of surround the slit beyond the activating region 5-14): receptive-field size, 4.5 x 2.5”. Duration of each oscilloscope trace is Stimulus velocity, 5O”/s. Receptive-field conventions as in Fig. 1.

inhibition for two directionally selective cells. In both cases, extending of the receptive field completely suppressed the response. Left (AM Stimulus size in A, C, F: 4.5 x 0.5”; B: 13.5 x 0.5”; D, E: 9 x 0.5’. 2 s. Right (AM 35-19): each PSTH is the sum of 15 stimulus sweeps. size, 17” diameter. Stimulus size, 14.5 x 4” in A; 27 x 4” in B. Other

than the receptive-field size in these tests to avoid the appearance of a stimulus moving perpendicular to its orientation. 2) The range of directions to which a cell responded for spot versus slit stimuli In striate cortex, oriwere compared. entation-selective cells respond over a narrower range of directions of stimulus movement to slits moved perpendicular to their orientation than to spots (15, 16, 35). The increased response specificity (narrower response range) is due to the addition of orientation as a parameter in the slit stimulus. This comparison was made for 36 cells in the LS area (Fig. 3). While overall response magnitude varied with the size of the stimulus (as described above), the LS

area cells did not respond over a narrower range of directions for slit stimuli as compared to spots. Slight variations in range for the two types of stimuli were seen from cell to cell. However, the differences in range were usually within the limits of response variability of LS area cells to reseated nresentations of the same stimulus, andA the narrower range was seen as often for spot stimuli as for slits (Fig. 3). 3) If a cell responded consistently to stationary flashing slits, the effect on the cell’s response of changing the orientation of the slit was determined. This is the most definitive test for orientation selectivity since, in the absence of a moving stimulus, there is no possibility of confusing direc-


1408

P. D. SPEAR

AND

T. P. BAUMANN

NA 36-7

NA 34-19

0

‘0’ 5

FIG. 3. Directional response range for four directionally selective cells to spot versus slit stimuli. Presentation of spot and slit stimuli were alternated for each direction of movement. Slits were oriented perpendicular to the movement direction. Polar diagrams show the response magnitude as a function of direction of the moving stimulus. Concentric circles indicate the number of spikes, as labeled. Each point represents the mean of 10 repetitions for cells NA 36-4 and NA 36-7, 3 repetitions for AL4 20-10, and 2 repetitions for NA 34-19. Receptive field (outline drawings) and stimulus (in black) sizes are given by the horizontal calibration bars. For cells AL4 36-7, NA 34-19, and NA 20-10, stimuli were kept equal to or less than the size of the receptive field because inclusion of the surround eliminated responses of cells to any direction of movement. See text for further discussion.

tional selectivity for orientation selectivity (15). However, responses to stationary stimuli were typically absent or very weak, particularly to narrow slits which did not fill the receptive-field activating region. Nevertheless, it was possible to test 22 directionally selective cells in this way (Fig. 4). All of these resnonded to all orientations tested, and differences in magnitude of response to different orientations were minimal. This was true for stimuli confined to the receptive-field activating region as well as those-extending well beyond it. We conclude from these tests that these LS area cells are directionally selective and many are sensitive to changes in stimulus

size, but they are relatively insensitive to changes in stimulus shape or orientation. Using these same methods we have had no difficulty in classifying orientation-selective cells in striate cortex of the cat (unpublished observations). The distribution of preferred directions was plotted for 150 directionally selective cells (Fig. 5A). All possible preferred directions were observed and no one preferred direction was seen significantly more freauentlv than others. The data also were analyzed with regard to the visual field quadrant in which each receptive field was located in order to assess the possibility that the preferred directions tended to -point


LATERAL

SUPRASYLVIAN

\

/

4. Responses of two directionally selective cells to stationary slits of different orientations. Both cells responded with a transient burst, lasting about 100 ms, when the stationary light slit was turned off. The mean number of spikes in the off-response (ordinate) is plotted for 20 repetitions at each orientation (abscissa). Mean spontaneous activity during random lOO-ms periods was 0.16 spike for cell NA 36-9 and 0.23 spike for NA 36-10. A 26 x 2.5’ slit centered on the receptive field was used in both cases. Receptive-field size: 26 x 29.5’ for cell NA 36-10; 23 x 22.5’ for cell NA 36-9. In both cases the preferred direction for moving stimuli was vertically upward. FIG.

B

A UPPER 17

27 LOWER

90 RESPONSE

135

h 180

RANGE

225

270

(DEGREES)

FIG. 5. A.- distribution of preferred directions for 150 directionally selective cells (axially directional cells are not included). Each arrow points in a direction of stimulus movement in the contralateral visual hemifield and shows the number of cells with that preferred direction. B: distribution of the directional ranges for 107 directionally selective cells (axially directional and directional preference cells not included). Each response range class (abscissa) represents the total range of directions of stimulus movement to which the cell responded. For example, a cell which responded over a range of directions + 45” to either side of the preferred direction would be placed in the 90” response-range class.

VISUAL

AREA

1409

away from the area centralis toward the periphery of the visual field, as has been reported for the cat superior colliculus (45-47). There was only a slight tendency for LS area cells with preferred directions pointing away from the area centralis (60%) to occur more frequently than cells with preferred directions pointing toward the area centralis (40%), and this tendency was not statistically reliable. The range of directions of stimulus movement through the receptive field which produced a response was determined for 107 cells (Fig. 5B). Typically, this range was relatively symmetrical around the preferred direction. The narrowest range which was observed was 40” (+ 20’ from the preferred direction) and the broadest was 270”. Axially directional cells tended to have relatively narrow ranges of 45-90’ around each of the two preferred directions. There was no relationship between the presence or absence of an inhibitory surround in the receptive field and the directional range of the cells. MOVEMENT SENSITIVE. Seven and onehalf percent ( 16/2 13) of the cells responded maximally to a stimulus moving through the receptive field in any direction. In other respects, their stimuilus requirements were similar to directionally selective cells. They gave weak on- and/or off-responses to stationary stimuli anywhere within the receptive field. Most responded well to small (l-2”) moving stimuli and showed spatial summation within the receptive-field activating region. Reversing the contrast of the stimulus had little effect on the response. Six of the nondirectional movement sensitive cells had inhibitory surrounds which were present on all sides of the receptive field.

Five percent ( 1 l/2 13) of the responsive cells gave their maximum resonse to stationary flashing stimuli. These responded at light onset (two cells), offset (seven cells), or both (two cells). All but two of the stationary cells had concentric antagonistic surrounds. Typically, no response was obtained from stimulation of the surround alone, although two cells discharged to light-off in the center and to light-on in the’ surround. STATIONARY.


1410

P. D. SPEAR

AND

Cells with stationary receptive fields also responded to moving stimuli, particularly if the movement was sufficiently rapid. However, reversing stimulus contrast changed the movement response in ways which could be predicted from the center-surround receptive-field organization. Further, the response to a moving stimulus was never greater than that to a stationary flashing stimulus of the same size. OR INDEFINITE. Six and one-half percent (14/2 13) of the responsive cells are included in this category. Some (57%) gave brisk and consistent responses to whole-eye illumination, but no localized receptive field could be found on the tangent screen. Others (43%) responded to stimulation within a localized area of the visual field, but the response was too weak or inconsistent to adequately define the receptive-field properties. In addition to the 2 13 responsive cells, 38 cells within the LS area were studied which did not respond to any of the visual stimuli tested. Both the nonresponsive cells and those with diffuse or indefinite receptive fields were found interspersed among cells with well-defined receptive fields. Although they were tested extensively with a large variety of visual stimuli, we cannot exclude the possibility that they actually had well-defined receptive fields which we failed to detect. DIFFUSE

Other properties of LS area cells VELOCITY. Analysis of the responses to different velocities of stimulus movement was performed for 41 cells with directionally selective or movementsensitive receptive fields (Figs. 6 and 7). The majority failed to respond to stimulus movement slower than 5-loo/s, and many required a minimum stimulus speed of 15-200/s or more. Most of the cells continued to respond to movement well above 2OO”/s. For some of the cells, there was a relatively narrow range of stimulus velocities which produced a clearly maximal resonse, and this range typically centered around 300/s (Fig. 7). However, most of the cells gave nearly equivalent responses to an extremely wide range of STIMULUS

A 1 v-m *. m-w* - 1. -Y. BAUMANN

stimulus velocities. Directionally selective cells remained directionally selective for all velocities tested. DOMINANCE. Over 65% of the cells which had their entire receptive field within a 45” radius of the area centralis (the approximate binocular overlap field for the cat) ( 13, 4 1) were driven independently from the two eyes. There were no obvious differences in the receptive-field organization mapped for each eye. An additional five cells responded only to binocular stimulation, but not to either eye alone. The ocular dominance of the cells was rated on a seven-point scale ( 18), and the distribution is shown in Fig. 8. The high proportion of cells driven solely by the contralateral eye (group 1) tended to decrease for receptive fields closer to the area centralis. All of the cells with receptive fields extending outside a 45’ radius of the area centralis were driven only by the contralateral eye. OCULAR

RECEPTIVE-FIELD SIZE AND SHAPE. As may be seen in Fig. 9, most of the receptive fields were roughly circular or elliptical in shape, although some were clearly rectangular. The preferred direction of directionally selective cells was frequently, but not always, perpendicular to the major axis of elongated receptive fields. The area of each receptive field was estimated by mutliplying the length of the major axis times the length of the minor axis. An extremely broad range of areas was seen. The smallest field was approximately 3 deg2 (a circular receptive field 1.75’ in diameter) and the largest was 1,810 deg2 (47 x 38.5”). The mean receptive-field size was 278.4 deg2. There was no relationship between the receptive-field classification of a cell and the size of its receptive field. However, among the directionally selective cells, there was a small but significant correlation between directional range and receptive-field size (r = 0.22, P < 0.05).

Extent and visuotopic organization of LS area In most cases, one to two penetrations were made in a hemisphere in order to study single-cell responses in addition to


LATERAL

SUPRASYLVIAN

NA 34-19

VISUAL

1411

AREA

NA 34-18

25. 5

8

10

16

--

‘I -,--”

--*-

-

.-m:--:q--

--_

-*-

32 40

64

60

128

100

-*-

--7

--* -

: TT,

d--

-M-e-

-

.

160

--*

--

125

-_

.

-* -r -.--

--m-h-

150 200 6. Responses of two directionally selective cells to different velocities of stimulus movement. Numbers to the left of each PSTH give the stimulus velocity in degrees per second. Ascending and descending sequences through the entire range were alternated in collecting data. All conventions as in Fig. 1. At high-stimulus velocities, the PSTH response peaks shift to the right. This is not due to a loss of directional selectivity in responses; it occurs because the cells’ response latencies are relatively constant, while the total sweep duration decreases with increases in stimulus velocity (sweep distance is constant). Left (NA 34-19): sum size, 2’ light spot. Right (NA of six stimulus sweeps in each PSTH. Receptive-field size, 15 x 10.5’. Stimulus 34-18): sum of eight stimulus sweeps in each PSTH. This cell failed to respond at 2OO”/s (not shown). Receptive-field size, 19 x 20’. Stimulus size, 2’ light spot. FIG.

visuotopic organization. In six cats, multiple penetrations were made and the visuotopic organization was verified and extended using multiunit-recording techniques. In each of these cats, the receptive-field characteristics of several single

neurons also were studied to ensure that a functionally unitary cortical area was being mapped. EXTENT. Anteriorly, the LS area extends to the anterior bend of the suprasylvian


1412

I

0

P. D. SPEAR

1

1

1

40

,

L

80

1

1

1

120

1

AND

.

160

200

I,

)200

SPEED (DEGREES/SECOND) FIG. 7. Range of velocities over which each of 41 directionally selective and movement-sensitive cells responded. Each cell is represented by a horizontal line which shows the range of stimulus speeds (abscissa) to which that cell responded. For those cells which produced a clearly maximal response to a narrow range of velocities, the optimal velocity is indicated by a vertical slash. The remaining cells gave nearly equivalent responses over most of the range of velocities to which they responded (see Fig. 6).

T. P. BAUMANN

sulcus (Fig. 9A, upper left). That it does not extend beyond the bend of the sulcus was verified in two cats in which penetrations were made successively outside and inside the area. The LS area continues posteriorly along the entire medial bank of the middle suprasylvian sulcus and around its caudal bend into the posterior suprasylvian sulcus. We have not determined the posterior limit of the area; however, it is clear that it extends several millimeters pos teroven trally along the caudal bank of the posterior suprasylvian sulcus. In the anterior and middle parts of the middle suprasylvian sulcus, the area extends from the dorsal lip of the medial wall ventrally into the fundus (Fig. 9A and B). In the most posterior part of the middle suprasylvian sulcus and around the bend in the posterior suprasylvian sulcus, the area appears to start lower on the medial wall and continue slightly beyond the fundus into the bottom of the ectosylvian (lateral) wall. Ten cells have been studied at the bottom of the ectosylvian side of the sulcus (within 2.5 mm of the fundus) between stereotaxic coordinates A5 and AP 0 and their receptive-field properties did not differ from those in the suprasylvian bank. REPRESENTATION. The positions of the area centralis and the horizontal and vertical meridia were determined from the optic disc projections on the tangent screen using the data of Bishop, Kozak, and Vakkur (4). The position of each receptive field in the visual field then was determined with respect to these landmarks. Receptive fields were observed which extended 90’ or more into the contralateral temporal visual field (Fig. 9B, cats A?. 29 and NA 24), 45” into the upper visual field along the vertical meridian (Fig. 9B, cat AU 16), and 65” into the lower visual field along the vertical meridian (Fig. 9A, cat NA 28). Except for fields near the vertical meridian, we found little or no representation of the upper quadrant of the contralateral visual hemifield beyond 10-20’ above the horizontal meridian (Fig. 9). The representation of the lower visual field quadrant apVISUAL-FIELD

i-

2

OCULAR

3

4

L 5

6

7

DOMINANCE

FIG. 8. Ocular-dominance distribution for 81 cells which had their receptive fields entirely within a 45” radius of the area centralis. Group 1 cells were driven only by the contralateral eye, group 2 showed a marked dominance by the contralateral eye, group 3 had a slight contralateral dominance, group 4 cells were driven about equally by either eye, group 5 had a slight dominance by the ipsilateral eye, group 6 showed a marked ipsilateral dominance, and group 7 cells were driven only by the ipsilateral eye.

I


LATERAL

SUPRASYLVIAN

peared to be more extensive. In terms of numbers of cells, 840/o in our sample had the center of their receptive field below the horizontal meridian. It was common to find cells which had receptive fields extending across the vertical meridian and 8’ or more into the ipsilateral visual hemifield (Fig. 9A and B). The furthest overlap into the ipsilateral visual field was 24’ for the receptive fields of two cells in different animals. There was a small correlation between the size of the receptive field and distance from the area centralis (r = 0.27, P < 0.0 1). Receptive-field classification, and characteristics within each class, did not vary systematically with visual-field position. The visualORGANIZATION. field position of the receptive fields was extremely variable from cell to cell in a single penetration (Fig. 9). Nevertheless, an overall systematic topographic organization was apparent. In our most posterior penetration (in the posterior wall of the posterior suprasulvian sulcus; Fig. 9B, cat NA 24) a progression was seen with fields near the far peripheral horizontal meridian represented high in the sulcus and more central fields deeper in the sulcus. However, even at the bottom of the cortical grey matter, the fields still were as far as 30-35’ from the vertical meridian. More anteriorly (in the posterior part of the middle suprasylvian sulcus; Fig. 9B, cat NA 3l), a similar pattern was repeated except that the receptive fields extended further into the central visual field at the bottom of the sulcus. In cases in which cells were recorded in the fundus or the bottom of the ectosylvian wall of the sulcus, their receptive fields were on or near the vertical meridian (Fig. 9B, cat NA 16). pattern of This temporal-to-central visual-field representation was repeated throughout the posterior two-thirds of the middle suprasylvian sulcus (Fig. 9, cats A?. 16, 1%4 29, NA 33), although there was a great deal of scatter from cell to cell in the vertical position of the receptive field. This repeating pattern of representation was verified in a single cat in which seven microelectrode penetrations were made

VISUAL

AREA

1413

between stereotaxic coordinates P2 and A5, and the same pattern was seen repeated in each penetration. In the more anterior portion of the LS area (in the anterior quarter to one-third of the middle suprasylvian sulcus), a change in the visual-field representation occurred and the cortex appeared to be devoted to a representation of the vertical meridian. Cells in the upper part of the suprasylvian bank of the sulcus had their receptive fieds near the vertical meridian in the upper visual field, and the lower vertical meridian was represented in the bottom part of the sulcus (Fig. 9A, cats NA 35 and NA 28). We have verified this general pattern of visuotopic organization in many cats. However, the details seem to be extremely variable from cat to cat.

VISUOTOPIC

RELATIONSHIPS. Cells with characteristics common receptive-field tended to occur in clusters. For example, two or more cells with stationary or movement-sensitive receptive fields often occurred in succession in a penetration. The same was true for axially directionally selective cells. In addition, directionally selective cells recorded simultaneously or in close succession typically had the same preferred direction. From these data and those reported by Hubel and Wiesel (2 l), it seems likely that the LS area contains a columnar organization. However, a firm conclusion cannot be made without further data (see ref 19).

FUNCTIONAL

DISCUSSION

Our results indicate that most cells in the LS cortex are specialized for response to moving stimuli, and that the vast majority of these are directionally selective. The range of directions to which these cells respond tends to be relatively broad. Unlike the superior colliculus (45-47), all possible preferred directions are about equally represented. Most cells respond to a wide range of stimulus velocities. Small stimuli usually are effective, and most cells show spatial summation to increases in stimulus size within the large receptive fields. However, for about a third of the cells, an inhibitory mechanism limits the maximum size a stimulus may attain.


1414

P. D. SPEAR

AND

T. P. BAUMANN

NA 28 (A-11.5)

/

NA 35 (A-8) w

V

87 9

-

119

I

lmm

’

-7

9. A: drawing to the upper left shows the extent of the LS area. The anterior bend of the middle suprasylvian sulcus is at stereotaxic coordinate Al2 and the posterior bend is at P3. However, this varied somewhat from cat to cat. Each filled dot represents the position of one or more responsive penetrations. Forty-nine penetrations were made in both hemispheres; all are shown here as being in the right hemisphere for convenience. The two open dots represent verified nonresponsive positions around the anterior bend of the lateral suprasylvian sulcus (see text). In A and B, camera lucida drawings are shown for seven representative penetrations. The penetration at Al 1.5 (NA 28) was the most anterior responsive penetration, and that at P1.5 (NA 24) was the most caudal penetration around the bend in the posterior suprasylvian sulcus. Each slash mark along the reconstructed microelectrode penetrations represents a single neuron. Filled dots indicate responsive cells, and SW indicates multiunit background activity for which receptive fields are shown in the visual field drawings. Positions marked B represent electrolytic marking lesions. Boundaries of the visual-field drawings extend from 8” ipsilateral to the vertical meridian (V) to 90” into the contralateral visual field, and from 45” above to 55” below the horizontal meridian (H). The top-to-bottom sequence of leaders corresponds to the sequence in which cells whose receptive fields they point to were encountered in the penetration. FIG.


LATERAL

SUPRASYLVIAN

VISUAL

NA 29 (A-5)

AREA

1415

16 (A-4)

24

NA 31 (A-2) 21 22

FIGURE

Comparison area cells

with previous

studies

of LS

Our results confirm in many respects the previous studies by Hubel and Wiesel (21) and Wright (56). An important exception concerns their conclusion that the LS area cells are orientation selective. Both studies reported that the receptivefield properties resembled those of “complex ” and “lower order hypercomplex” cells in visual cortical areas 17, 18, and 19, except that the receptive fields of LS area cells were much larger. We also found that the LS area cells behaved very much like complex or hypercomplex cells when

9B.

they were tested with straight-edge or slit stimuli, as would be expected from the spatial receptive-field properties summarized above. However, comparisons of responses to spot and slit stimuli indicated that these cells are not orientation selective. For example, very few responded better to straight-edge slits moving in the preferred direction than to curved-edge spots of the same size. Further, increasing the size of either type of stimulus produced the same increase in response, indicating that the spatial summation did not depend on the orientation or axis along which stimulus size was var-


1416

P. D. SPEAR

AND

ied. This was demonstrated further in tests which showed that the responses of directionally selective cells were about equal to stationary flashing slits of any orientation. In addition, they responded over about the same range of directions to moving slits as to moving spots. The degree of direction selectivity was relatively independent of the shape or orientation of the stimulus, and the addition of orientation in the stimulus did not alter the response specificity of the cells. It is interesting to note in this regard that Wright’s (56) data on the range of orientation specificity of LS area cells tested with slits agree well with our data on the range of directional selectivity of LS area cells tested with spots. Neither of the previous two studies reported tests with nonoriented stimuli to distinguish between the influence of stimulus size, orientation, and direction of movement (21, 56). These tests indicate that the relevant stimulus parameters are size and direction of movement, but not orientation. We cannot exclude the possibility that a small number of LS area cells are orientation selective and, in fact, some of our cells showed response properties compatible with this possibility. However, these cells were relatively rare and there was an equal number which appeared to prefer curved spot stimuli over oriented slits. Whether this is of some functional significance or is simply the result of cellto-cell response variability is unknown. Other aspects of the three studies are in close agreement. For example, the percentage of cells with internal or surround inhibition (cells classed as hypercomplex in the previous studies) is nearly the same. Further, all three find a low incidence of cells with axial directional selectivity. Although Hubel and Wiesel (21) did not report any nondirectionally selective cells, Wright (56) found that about 18% of the LS cortex cells were not directionally selective, a figure which is close to ours. Extent and topographic LS area

organization

of

Our results concerning the extent of the LS area along the middle and posterior suprasylvian sulci agree well with

T. P. BAUMANN

anatomical delineations of the area based on the pattern and extent of termination of its afferents (14, 22, 30, 39, 43). Heath and Jones (14) cautioned that the projections in the posterior suprasylvian sulcus might represent a separate functional area. However, our physiological results suggest that this extension around the posterior bend of the suprasylvian sulcus is a functional continuation of the LS area. In a recent abstract, Palmer (33) has described the extent and retinotopic organization of the LS area as determined by multiple-unit recording methsods. Our findings are in close agreement with Palmer’s (33). Taken together, they indicate that in its posterior extent, the LS area contains a large repeating representation of the contralateral hemifield moving from the far temporal periphery near the lip of the sulcus to the central visual field deep in the sulcus. In our most posterior penetrations, we found that deep in the sulcus this progression did not reach fully to the vertical meridian. Presumably, the more central visual field would have been found in the portion of the LS area which continues up the lateral ectosylvian wall of the sulcus in the caudal portion of the area (14, 33). In the middle of the middle suprasylvian sulcus, corresponding to the region from which Hubel and Wiesel (2 1) recorded, the entire temporal-to-central field progression is found in the medial bank of the sulcus. In its most rostra1 portion, the LS area is devoted to a representation of the vertical meridian, with upper visual fields represented high in the sulcus and lower fields in the depths of the sulcus. It is possible that this rostra1 portion is a different visual area with a separate visuotopic organization. However, we found no evidence that cells in this region differed in their functional character&tics from those elsewhere in the LS sulcus. Furthermore, the anatomical studies provide no evidence that the rostra1 and caudal portions of the middle suprasylvian sulcus receive different types of projections (14, 22, 30, 39, 43). There was only a limited representation of the upper visual field in the LS cortex.


LATERAL

SUPRASYLVIAN

VISUAL

AREA

1417

Although receptive fields high on the ver- the possibility that only complex (and cells project to tical meridian were found, we rarely ob- perhaps hypercomplex) served receptive fields extending far the LS area, in a fashion similar to the striate cortex projection to superior colabove the horizontal meridian elsewhere liculus (17, 34). Nevertheless, it is clear in the contralateral hemifield. In addition, it was common to find receptive fields ex- from the comparisons with its afferents tending well into the ipsilateral hemifield that the LS cortex does not represent a higher sequential level of visual process(up to 24”). It is of interest that all three of the thalamic nuclei which project to the ing after areas 17, 18, and 19. Rather, it LS area (MIN, PN, and LP) also contain in some way combines and integrates the separate inputs from each of areas 17, 18, cells with receptive fields extending from 13 to 36’ into the ipsilateral hemifield (9, and 19 with the varied inputs from each of the thalamic nuclei. The way in which 25, 40). Furthermore, both the PN and LP nuclei contain little or no representathis occurs awaits further analysis. tion of the upper visual field (9, 25). Since the MIN (25,40) and cortical areas 17, 18, SUMMARY and possibly 19 (2, 49, 55) all contain a The visual receptive fields of 2 13 cells more complete representation of the in the lateral suprasylvian visual cortex upper quadrant of the contralateral hemi(LS, or Clare-Bishop area) were studied in with nitrous oxide. field, the possibility exists that only por- cats anesthetized tions of these areas project to LS cortex, Eighty-one percent of the cells were direcwhile portions containing the upper visual tionally selective. They responded poorly field representations do not. to stationary stimuli flashed on or off, but gave a directionally selective response to Comparisons with afferent receptive fields stimuli moving through the receptive The receptive-field properties of cells in field. Most of these had a single preferred LS cortex are very similar to those of cells direction and an opposite null direction. in the tectothalamic system from which it They typically responded to a range of receives a major input. For example, directions of stimulus movement from 45 many cells in the LP nucleus are directo 90’ to either side of the preferred ditionally selective and show spatial summarection. Small stimuli ( l-2’ or smaller) tion within very large receptive fields (9, typically were effective, and 87% of the 25, 37, 51, 57). Others have movementdirectionally selective cells showed spatial sensitive, stationary, or diffuse receptive summation. About 32% had inhibitory fields (9, 37, 57) similar to those we have mechanisms which decreased the refound in the LS area. While very little is sponse of the cell if the stimulus exceeded known about the properties of PN nua maximum size. There was little or no cleus cells, their receptive fields appear to evidence that LS area cells were orientaresemble those of the LP nucleus (9, 25, tion selective or sensitive to variations in 48). In contrast, cells in the MIN have stimulus shape independent of size. small concentrically organized receptive About 7.5% of the cells responded to fields similar to those of cells in the main stimuli moving in any direction. Otherbody of the dorsal lateral geniculate (25, wise, their stimulus requirements were similar to those of directionally selective 28) Cells in visual cortical areas 17, 18, and cells. Five percent of the LS area cells 19 have small orientation-selective recepgave their maximum response to stationtive fields (15, 16, 18, 20, 36, 38, 52), ary stimuli flashing on and/or off. Nearly which differ in many respects from the LS all of these had concentric antagonistic area and its thalamic inputs. Nevertheless, surrounds. About 6.50/O of the LS area the complex and some hypercomplex re- cells had diffuse receptive fields or gave ceptive fields have a number of spatial indefinite responses to light. and temporal (e.g., velocity) characterisMost of the directionally selective and tics in common with receptive fields of LS movemen t-sensitive cells tested responded area cells (18, 29, 36, 38, 52). This raises over a broad range of stimulus velocities,


1418

P. D. SPEAR

AND

from 5-loo/s to over 2OO”/s, with little or no response. to slower moving stimuli. Over 65% of the cells which had their receptive field within a 45” radius of the area centralis were driven independently by the two eyes, although there was an overall dominance bv the contralateral eye. The receptive fields tended to be extremely large (mean area, 278.4 deg2), although there was a great deal of variation in size. The extent and visuotopic organization of the LS area was studied using single cell and multiunit recording. It extended along the entire medial bank of the middle suprasylvian sulcus from the anterior bend of the sulcus to beyond the posterior bend of the sulcus, and then ventrolaterally along the caudal bank of the posterior suprasylvian sulcus. The posterior twothirds or more of the area contained a large repeating representation of the con-

T. P. BAUMANN

tralateral hemifield moving from the far temporal periphery near the lip of the sulcus to the central visual field deep in the sulcus. In its most rostra1 portion, the LS area was devoted to a representation of the vertical meridian, with upper visual fields represented high in the sulcus and lower fields in the depths of the sulcus. Except for those near the vertical meridian, receptive fields in the upper visual field were rarely observed. There was an extensive nasotemporal overlap, with some receptive fields extending across the vertical midline as far as 24’. ACKNOWLEDGMENTS

The authors thank Terry Janssen, Helen Barbas, and Donald Holmes for their assistance. This study was supported by Public Health Service Grants 5 ROl EYO1170 and MH08359, a Public Health Service Biomedical Sciences Support Grant, and a grant from the Kansas State University Bureau of General Research.

REFERENCES 1.

J. AND CARPENTER, M. Fiber projections of the superior colliculus in the cat. J. Camp. Neural. 116: 157-178, 1961. 2. BILGE, M., BINGLE, A., SENEVIRATNE, K. N., AND WHITTERIDGE, D. A map of the visual cortex in the cat. J. Physiol., London 191: 116-118, 1967. 3. BISHOP, P. O., BURKE, W., AND DAVIS, R. The identification of single units in central visual pathways. J. Physiol., London 162: 399-431, 1962. 4. BISHOP, P. O., KOZAK, W., AND VAKKUR, G. J. Some quantitative aspects of the cat’s eye: axis and plane of reference, visual field coordinates and optics. J. Physiol., London 163: 466-502, 1962. 5. BURROWS, G. R. AND HAYHOW, W. R. The organization of the thalamo-cortical visual pathways in the cat. An experimental degeneration study. Brain Behav. Evol. 4: 220-270, 197 1. 6. CLARE, M. H. AND BISHOP, G. H. Responses from an association area secondarily activated from optic cortex. J. Neurophysiol. 17: 271-277, 1954. 7. FERNALD, R. AND CHASE, R. An improved method for plotting retinal landmarks and focusing the eyes. Vision Res. 11: 95-96, 197 1. 8. GAREY, L. J., JONES, E. G., AND POWELL, T. P. S. Interrelationships of striate and extrastriate cortex with the primary relay sites of the visual pathway. J. Neural. Neurosurg. Psych&. 3 1: 135-157, 1968. 9. GODFRAIND, J. M., MEULDERS, M., AND VERAART, C. Visual properties of neurons in pulvinar, nucleus lateralis posterior and nucleus supraALTMAN,

geniculatus investigation.

thalami in the cat. I. Qualitative Brain Res. 44: 503-526; 1972. 10. GRAYBIEL, A. M. Some fiber pathways related to the posterior thalamic region in the cat. Brain Behav. Evol. 6: 363-393, 1972. 11. GRAYBIEL, A. M. Some ascending connections of the pulvinar and nucleus lateralis posterior of the thalamus in the cat. Brain Res. 44: 99125, 1972. A. M. 12. GRAYBIEL, Some extrageniculate visual pathways in the cat. Invest. Ophthalmol. 11: 322-332, 1972. 13. GUILLARY, R. W. AND KAAS, J. H. A study of normal and congenitally abnormal retinogeniculate projections in cats. J. Camp. Neurol. 143: 73-100, 1971. 14. HEATH, C. J. AND JONES, E. G. The anatomical organization of the suprasylvian gyrus of the cat. Ergeb. Anat. 45: l-64, 1971. 15. HENRY, G. H., BISHOP, P. O., AND DREHER, B. Orientation, axis and direction as stimulus parameters for striate cells. Vision Res. 14: 767-777, 1974. 16. HENRY, G. H., DREHER, B., AND BISHOP, P. 0. Orientation specificity of cells in cat striate cortex. J. Neurophysiol. 37: 1394-1409, 1974. 17. HOFFMANN, K.-P. Conduction velocity in pathways from retina to superior colliculus in the cat: a correlation with receptive-field properties. J. Neurophysiol. 36: 409-424, 1973. 18. HUBEL, D. H. AND WIESEL, T. N. Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex. J. Physiol., London 160: 106-154, 1962.


LATERAL 19.

AND WIESEL. T. N. Shape and of columns in cat’s striate cortex. London 165: 559-568, 1963. HUBEL, D. H. AND WIESEL, T. N. Receptive fields and functional architecture in two nonstriate visual areas (18 and 19) of the cat. J. Neurophysiol. 28: 229-289, 1965. HUBEL, D. H. AND WIESEL, T. N. Visual area of the lateral suprasylvian gyrus (Clare-Bishop area) of the cat. J. Physiol., London 202: 251260, 1969. KAWAMURA, K. Corticocortical fiber connections of the cat cerebrum. III. The occipital region. Brain Res. 5 1: 4 l-60, 1973. KAWAMURA, S. Topical organization of the extrageniculate visual system in the cat. Exptl. Neurol. 45: 451-461, 1974. KAWAMURA, S., SPRAGUE, J. K., AND NIIMI, K. Corticofugal projections from the visual cortices to the thalamus, pretectum and superior colliculus in the cat. J. Camp. Neurol. 158: 339-362, 1974. M. A., AND BISHOP, KINSTON, W. J., VADAS, P. 0. Multiple projection of the visual field to the medial portion of the dorsal lateral geniculate nucleus and the adjacent nuclei of the thalamus of the cat. J. Camp. Neurol. 136: 295-316, 1969. MACIEWICZ, R. J. Afferents to the lateral suprasylvian gyrus of the cat traced with horseradish peroxidase. Brain Res. 78: 139-143, 1974. MARSHALL, W. H., TALBOT, S. A., AND ADES, H. W. Cortical response of the anesthetized cat to gross photicand electricalafferent stimulation. J. Neurophysiol. 6: 1-14, 1943. MASON, R. Cell properties in the medial interlaminar nucleus of the cat’s lateral geniculate complex in relation to the transient/sustained classification. Exptl. Brain Res. 22: 327-329, 1975. MOVSHON, J. A. Velocity preferences of simple and complex cells in the cat’s striate cortex. J. Physiol., London 242: 121P-123P, 1974. NIIMI, K., KADOTA, M., AND MATSUSHITA, Y. Cortical projections of the pulvinar nuclear group of the thalamus in the cat. Brain Behav. Evol. 9: 422-457, 1974. NIIMI, K., KAWAMURA, S., AND ISHIMARU, S. Projections of the visual cortex to the lateral geniculate and posterior thalamic nuclei in the cat. J. Camp. Neurol. 143: 279-312, 1971. NIIMI, K., MIKI, M., AND KAWAMURA, S. Ascending projections of the superior colliculus in the cat. Okajimas Folia Anat. Japan. 47: 269-287, 1970. PALMER, L. A. Extent and retinotopic organization of the Clare-Bishop area of the cat. Anat. Record 175: 406, 1973. PALMER, L. A. AND ROSENQUIST, A. C. Visual receptive fields of single striate cortical units projecting to the superior colliculus in the cat. Brain Res. 67: 27-42, 1974. PETTIGREW, J. D. The effect of visual experience on the development of stimulus specificity by kitten cortical neurones. J. Physiol., London 237: 49-74, 1974. HUBEL,

arrangement J. Physiol., 20.

21.

22.

23.

24.

25.

26.

27.

28.

29.

30.

31.

32.

33.

34.

35.

D. H.

SUPRASYLVIAN

VISUAL 36.

AREA

1419

J. D., NIKARA, T., AND BISHOP, P. 0. Responses to moving slits by single units in cat striate cortex. Exptl. Brain Res. 6: 373-390, 1968. 37. RICHARD, D., ANGYAN, L., AND BUSER, P. Controle, par le cortex visuel, du groupe thalamique lateral posterieur chez le chat. Exptl. Brain Res. 15: 386-404, 1972. 38. ROSE, D. AND BLAKEMORE, C. An analysis of orientation selectivity in the cat’s visual cortex. Exptl. Brain Res. 20: 1-17, 1974. 39. ROSENQUIST, A. C., EDWARDS, S. B., AND PALMER, L. A. An autoradiographic study of the projections of the dorsal lateral geniculate nucleus and the posterior nucleus in the cat. Brain Res. 80: 71-94, 1974. 40. SANDERSON, K. J. The projection of the visual field to the lateral geniculate and medial interlaminar nuclei in the cat. J. Camp. Neurol. 143: 101-118, 1971. 41. SHERMAN, S. M. Visual field defects in monocularly and binocularly deprived cats. Brain Res. 48: 25-46, 1972. K. 42. SHOUMURA, Patterns of fiber degeneration in the lateral wall of the suprasylvian gyrus (Clare-Bishop area) following lesions in the visual cortex in cats. Brain Res. 43: 264-267, 1972. 43. SHOUMURA, K. An attempt to relate the origin and distribution of commissural fibers to the presence of large and medium pyramids in layer III in the cat’s visual cortex. Brain Res. 67: 13-26, 1974. 44. SHOUMURA, K. AND ITOH, K. Intercortical projections from the lateral wall of the suprasylvian gyrus, the Clare-Bishop area, of the cat. Brain Res. 39: 536-539, 1972. 45. STEIN, B. E. AND ARIGBEDE, M. 0. A parametric study of movement detection properties of neurons in the cat’s superior colliculus. Brain Res. 45: 437-454, 1972. 46. STERLING, P. AND WICKELGREN, B. G. Visual receptive fields in the superior colliculus of the cat. J. Neuqbhysiol. 32: 1-15, 1969. 47. STRASCHILL, M. AND HOFFMANN, K.-P. Functional aspects of localization in the cat’s tecturn opticum. Brain Res. 13: 274-283, 1969. 48. SUZUKI, H. AND KATO, H. Neurons with visual properties in the posterior group of the thalamic nuclei. Exptl. Neurol. 23: 353-365, 1969. 49. TALBOT, S. A. AND MARSHALL, W. H. Physiological studies on neural mechanisms of visual localization and discrimination. Am. J. Ophthalmol. 24: 1255-l 264, 194 1. 50. VASTOLA, E. F. A direct pathway from lateral geniculate to association cortex. J. Neurophysiol. 24: 469-487, 1961. 51. VERAART, C., MEULDERS, M., AND GODFRAIND, J.-M. Visual properties of neurons in pulvinar, nucleus lateralis posterior and nucleus suprageniculatus thalami in the cat. II. Quantitative investigation. Brain Res. 44: 527-546, 1972. D. W. AND BERKLEY, M. A. The 52. WATKINS, orientation selectivity of single neurons in cat striate cortex. Exptl. Brain Res. 19: 433-446, 1974. PETTIGREW,


1420 53. 54.

55.

P. D. SPEAR

AND

M. E. Cortico-cortical connections of the cat visual areas.]. Anat. 102: 375-386, 1968. WILSON, M. E. AND CRAGG, B. G. Projections from the lateral geniculate nucleus in the cat and monkey. J. Anat. 101: 677-692, 1967. WOOLSEY, c. N. Comparative studies on cortical representation of vision. Vision Res. Suppl. 3: 365-382, 1971. WILSON,

T. P. BAUMANN 56.

M. J. Visual in a cortical area remote in the cat. Nature 223:

57.

WRIGHT, M. J. Responsiveness to visual stimuli of single neurones in the pulvinar and lateral posterior nuclei of the cat’s thalamus. J. Physiol., London 219: 32P, 1971.

WRIGHT,

receptive fields of cells from the striate cortex 973-975, 1969.


Visual receptive fields in the lateral suprasylvian area (Clare-Bishop area) of the cat.

Inhibition of visual responses of single units in the cat visual area of the lateral suprasylvian gyrus (Clare-Bishop area) by the introduction of a second visual stimulus.

Visual response properties of neurons in the middle and lateral suprasylvian cortices of the behaving cat.

Influence of the presentation of remote visual stimuli on visual responses of cat area 17 and lateral suprasylvian area.

Visual properties of neurons in the posterior suprasylvian gyrus of the cat.

Regressive changes among corticocortical neurons projecting from the lateral suprasylvian cortex to area 18 of the kitten's visual cortex.

Development of the projections from the dorsal lateral geniculate nucleus to the lateral suprasylvian visual area of cortex in the cat.

Synaptic organization of cortico-cortical connections from the primary visual cortex to the posteromedial lateral suprasylvian visual area in the cat.

Thalamic projections to the lateral suprasylvian visual area in cats with neonatal or adult visual cortex damage.

Visuomotor interactions in responses of neurons in the middle and lateral suprasylvian cortices of the behaving cat.

Functional roles of the lateral suprasylvian cortex in ocular near response in the cat.

18 border neurons contributing to the visual transcallosal pathway in the cat.

Delayed signal transmission in area 17, area 18 and the posteromedial lateral suprasylvian area of aged cats.

Ocular convergence-related neuronal responses in the lateral suprasylvian area of alert cats.

Acute alcohol exposure impairs neural representation of visual motion speed in the visual cortex area posteromedial lateral suprasylvian cortex of cats.

Spatiotemporal characteristics of direction-selective neurons in the middle temporal visual area of the macaque monkeys.

Maintained activity of single neurons in the cat visual cortex at different levels of retinal adaptation.

Microcircuitry of cat visual cortex: classification of neurons in layer IV of area 17, and identification of the patterns of lateral geniculate input.

The retinotopic distribution of visual callosal projections in the suprasylvian visual areas compared to the classical visual areas (17, 18, 19) in the cat.

Interactions between cat lateral geniculate neurons.

Osmosensitive neurons in the rat's preoptic area: medial-lateral comparison.

Responses of single cells in cat's lateral geniculate nucleus and area 17 to the velocity of moving visual stimuli.

Centrifugal motion bias in the cat's lateral suprasylvian visual cortex is independent of early flow field exposure.

The axonal arborizations of lateral geniculate neurons in the striate cortex of the cat.