J. Phypiol. (1977), 268, pp. 391-421 With 1 plate and 13 text-figures Printed in Great Britain

391

LAMINAR DIFFERENCES IN RECEPTIVE FIELD PROPERTIES OF CELLS IN CAT PRIMARY VISUAL CORTEX

By CHARLES D. GILBERT From the Department of Neurobiology, Harvard Medical School, 25 Shattuck Street, Boston, Massachusetts 02115, U.S.A.

(Received 27 September 1976) SUMMARY

1. Cells in area 17 of the cat visual cortex were studied with a view towards correlating receptive field properties with layering. A number of receptive field parameters were measured for all units, and nearly every unit was marked with a microlesion to determine accurately the layer in which it was found. 2. Cells were defined as simple or complex by mapping with stationary stimuli, using the criteria of Hubel & Wiesel (1962). Complex cells fell into two groups: those that showed summation for increased slit length (standard complex) and those that did not (special complex). 3. The simple cells were located in the deep part of layer 3, in layer 4, and in layer 6. This corresponds to the distribution of afferents from the dorsal layers of the lateral geniculate nucleus. In these cortical layers the simple cells differed primarily with respect to their receptive field size, cells in layer 4 having the smallest, layer 3 intermediate, and layer 6 the largest fields. Layer 4 was the only layer in which simple cells showed endinhibition (a reduction in response to slits extending beyond the excitatory portion of the receptive field). 4. The standard complex cells were found in all layers, but were quite scarce in layer 4. As with the simple cells, field size varied with layer: in layer 2 + 3 they had small to intermediate field sizes, in layer 5 intermediate, and in layer 6 very large. Layer 6 cells showed summation for slits of increased length up to very large values, and responded best when the slits were centred in the receptive field. The only standard complex cells that showed end-inhibition were those in layer 2 + 3, and these were similar to the layer 4 simple cells in terms of proportion of end-inhibited units and degree of end-inhibition. 5. The special complex cells, originally described by Palmer & Rosenquist (1974), were found in two tiers: the upper one at the layer 3/layer 4 border and the lower one in layer 5. They were different from the

392 C. D. GILBERP standard complex cells in having a high spontaneous activity, high velocity preference, and large fields which were similar in size (at a given eccentricity) from one cell to the next. Many showed reduced response to slits of increasing length, even for slits that did not extend beyond the borders of the responsive region. 6. Cells in layer 6 (the origin of the corticogeniculate projection) were antidromically activated from the lateral geniculate nucleus. The antidromically activated units included both simple and complex cells, and they had the long receptive fields characteristic of the overall population of cells in layer 6. 7. The results showed that there are different types of simple and complex cells, and that cells in different layers have different properties. Taken together with their differences in site of projection, this demonstrates that the anatomical lamination pattern is reflected in functional differences between cells in different layers. INTRODUCTION

One of the most striking features of the cerebral cortex, when viewed in Nissl stained sections, is its segregation into separate layers in which the cells have characteristic size, morphology and packing density. This segregation is reflected in connectivity, the cells in different layers differing in their afferents and in the sites to which they project. In primary visual cortex, the afferents from each of the layers of the lateral geniculate nucleus have distinct laminar patterns of termination, both in the monkey (Hubel & Wiesel, 1972) and in the cat (LeVay & Gilbert, 1976). Since cells in the ventral layers of the cat's geniculate have different receptive field properties from those in the dorsal layers (Hubel & Wiesel, 1961; Daw & Pearlman, 1970; Cleland, Morstyn, Wagner & Levick, 1975; Wilson & Stone, 1975) one would expect that cortical cells in zones receiving afferents from different geniculate layers would also differ in their receptive field properties. Moreover, cells in cortical layers that are completely free of geniculate afferents would presumably have receptive field properties different from those of cells in layers that do receive geniculate afferents. By examining the receptive field properties of cells in each layer one may shed some light on the processing of visual input in the cortex. In particular, by carefully examining the location of simple cells in relation to the sites of termination of geniculate afferents one can test the idea that these cells receive direct input from the lateral geniculate nucleus (Hubel & Wiesel, 1962). This approach may also provide some insight into the manner in which other receptive field types are constructed. Another major distinction between cells in different layers of the cortex

LAMINAR DIFFERENCES IN RECEPTIVE FIELDS 393 is that they project to different regions of the brain. In area 17, cells in the superficial layers project to other cortical areas, cells in layer 5 project to the superior colliculus, and cells in layer 6 project to the lateral geniculate nucleus (Toyama, Matsunami, Ohno & Takahashi, 1974; Palmer & Rosenquist, 1974; Hollander, 1974; Gilbert & Kelly, 1975). If there are receptive field properties that are unique to each layer one can gain someunderstanding of the function of the areas to which each layer projects. This approach was employed by Palmer & Rosenquist (1974) in the study of the cells responsible for the cortico-collicular projection. The layer of particular interest in the present study is layer 6, the origin of the cortico-geniculate projection. This projection is massive, in terms of the proportion of layer 6 cells that send their axons to the geniculate (Gilbert & Kelly, 1975), and the density of the cortical innervation of the geniculate (Hollander, 1972; Updyke, 1975). A study of the function of this recurrent pathway from cortex to geniculate is important to understanding the role of the geniculate in visual processing. METHODS

Adult cats were anaesthetized initially with ketamine HCL (20 mg/kg, I.M.) followed by sodium thiopental (20 mg/kg, i.v., supplemented by further injections as needed). In some experiments the level of anaesthesia was monitored with an e.e.g. The animal was then intubated with an endotracheal cannula or a cannula inserted through a tracheotomy, placed in a stereotaxic apparatus, paralysed with succinylcholine (15 mg/kg. hr) and artificially respirated. The concentration of CO2 in the expired air was monitored with a Beckman CO2 analyzer, and kept near a level of 4 %. The animal's e.k.g. and temperature were also monitored throughout the course of the experiment. The nictitating membrane was retracted with phenylephrine and the pupils dilated with atropine. Contact lenses were placed on the eyes, and a retinoscope was used to determine the radius of curvature of lens appropriate to focus the eyes on a tangent screen 1-5 m from the animal. Periodically during the experiment the positions of the area centralis and optic disk of each eye were plotted on the tangent screen using a dual-beam ophthalmoscope, with one beam directed towards the retina and the other beam pointed in the reverse direction, towards the tangent screen. For the recordings in the cortex a hole was made in the skull at Horsley-Clarke posterior 3-4 mm, close to the mid line. Single units were recorded with coated tungsten micro-electrodes advanced through the cortex by a micrometer driven hydraulic advancer. The electrode was directed on a tangential course down the medial wall of the lateral gyrus (Text-fig. 3 and P1. 1), thus remaining entirely in area 17. Due, most likely, to non-uniform slippage of the electrode through the tissue and to uneven shrinkage of the tissue during fixation and mounting, the micro-electrode advancer gave an unreliable measure of the distance between lesions (measured directly from histological sections). This could easily lead to an erroneous placement of a unit along the electrode track when its position is estimated by interpolation between two distant lesions. It was therefore necessary to mark nearly every unit with a lesion for precise localization to a cortical layer. In a number of experiments a stimulating electrode was placed in or above the lateral geniculate nucleus, through a hole in the skull made at Horsley-Clarke

C. D. GILBERT position anterior 5 5 lateral 9 0. Several different types of stimulating electrodes were used (coaxial and bipolar; stainless steel, silver and copper). Current was passed 394

through a Grass photoelectric stimulus isolation unit. The criteria for antidromic activation were as follows: (1) the unit had to follow a high rate of stimulation (greater than 200/sec), (2) it had to fire at a short latency, (3) the latency had to be constant, with less than0*2 msec jitter, (4) the supposed antidromic spike had to be blocked by an orthodromic spike (spontaneous or visually driven) for a period of at least twice the latency to stimulation plus a few tenths of a millisecond utilization time. The fourth criterion was essential for reliable identification of an antidromically driven unit since a few units satisfied the first three but not the last. In this study 184 units were studied, all in area 17, in twenty-one animals. Stimulation was done with a hand held projector, or with an optic bench, modelled on a design by Dr Peter Schiller (personal communication). The bench was equipped with a General Scanning G 300PD galvanometer which, by driving a prism, moved a slit of light over a fixed area at constant velocity on the tangent screen. Other devices on the bench could change the position, orientation, size and shape of the slit. The units were classified as simple or complex using stationary stimuli according to the criteria of Hubel & Wiesel (1962). Other parameters measured were spontaneous activity, response to moving stimuli (including a response histogram), approximate optimum velocity of movement for the stimulating slit, directionality, ocular dominance (and with some units the nature of the interaction between the eyes), orientation and orientation tuning, dimension of receptive field (measured using stationary stimuli, moving stimuli in and near the receptive field, and slits or edges of various lengths), length-response relationship, and finally the selectivity of the cell for slits of varying widths and for edges. By examining the properties common to cells in each layer, the classes of simple and complex could be further differentiated (see Results). Except for orientation tuning curves, which were made for one third of the cells, nearly every cell was studied for every parameter. After studying a unit a microlesion was made by passing 2-3,uA for 2-3 sec. This resulted in lesions of approximately 150 /%m in diameter. After the experiment was terminated the animal was perfused with 4% formaldehyde in 0 9 % saline. Blocks of tissue containing the electrode tracks were sectioned to 60,um thickness on a Vibratome (Oxford Instruments). Sections were mounted on gelatinized slides and stained with cresyl violet, and were examined for electrode tracks and lesions. The

layer in which each lesion was located was deter-

mined using the system of layering described by Otsuka & Hassler (1962). In area 17 of the cat, layers 2 and 3 are not distinguishable, but for the purpose of differentiating the properties of cells in the superficial versus deep parts of layer 2 +3 it was arbitrarily divided in half and labelled as two separate layers. RESULTS

A number of receptive field parameters were measured for the 184 cells encountered in this study. Most of the cells could clearly be classified as simple or complex, and the complex cells were divided into two major subtypes. Non-oriented units were also occasionally found, but it was not possible to determine whether they were cortical cells or afferents from the geniculate. There may be a population of cortical cells with non-oriented receptive fields, but intracellular recording and marking techniques are probably necessary to demonstrate this with certainty. For the remainder

LAMINAR DIFFERENCES IN RECEPTIVE FIELDS 395 of this paper only oriented receptive fields will be considered. The properties that distinguish the three types of oriented fields listed above will be dealt with first. This will be followed by a discussion of the laminar distribution of each, and the manner in which other receptive field parameters change with layer. Receptive field types Simple cells. The simple cell, originally named and described by Hubel & Wiesel (1962), was defined by mapping its receptive field with stationary stimuli. Like most cells in area 17, it responded best to slits of a given orientation. It could be distinguished from other cell types by the presence of separate excitatory and inhibitory regions with summation within each subfield and antagonism between subfields. Other investigators have used different criteria to distinguish one type of visual cortical cell from another. Pettigrew, Nikara & Bishop (1968), classifying cells by mapping with moving stimuli, labelled cells as simple if they had small fields, lowfrequency response, low spontaneous activity and preference for slow moving stimuli. Henry & Bishop (1972) extended this by describing subliminal excitatory or inhibitory bands flanking the central discharge region. These could be demonstrated only by stimulating the central and flanking regions at the same time. In this study, cells were examined using both stationary and moving stimuli. Simple cells were defined by the criteria of Hubel & Wiesel (1962) and were further characterized by making response histograms. A total of forty-four simple cells were analysed. Examples of simple cells are illustrated in Text-figs. 1A-D. As the receptive field maps show, there were separate on and off excitatory regions, usually numbering two or three. Often it was necessary to use two slits to elicit a response from a flanking subfield, leaving one slit on in one subfield and flashing a second slit in the other subfield. A few rare simple cells had a flanking region that inhibited the central region but would not activate the cell when a slit was flashed on or off within it, even when using the two-slit technique. All of the simple cells showed summation within each subfield and antagonism (inhibition) between them. Simple cells could respond with one or two short bursts of spikes to a slit oriented parallel to the receptive field axis and swept across the field in one or in both directions (Text-fig. 1A-D). The peak of each burst corresponded to the slit entering or leaving one of the subfields. Simple cells responded to a moving stimulus over a much more restricted area than they did to a stationary stimulus, hence their response histograms were narrow. One could usually predict the positions of the peaks of response to moving stimuli (in the response histograms) from the cell's

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to stationary stimuli. Thus in Text-fig. 1A, for a slit moving in direction the cell responded as it entered the on region and again as it left the off region; for a slit moving in the opposite direction it responded once as the slit was simultaneously leaving the off region and entering the on region. One could also predict the relative magnitude of two peaks occurring for movement in a given direction. In Text-fig. 1 B, the larger of the

response one

LAMINAR DIFFERENCES IN RECEPTIVE FIELDS 397 two peaks for movement in each direction corresponds to movement of a slit simultaneously from off to on, and the smaller for movement into the on region alone. In Fig. 1 C the single peaks corresponded to the movement from off to on, with no response for movement into the on region alone. The cells' response to stationary stimuli was not predictive of the relative magnitude of a cell's response in the two directions. For the cells in Text-fig. 1A and D movement in the direction that brought the slit simultaneously out of an off region and on to an on region elicited less of a response than movement in the opposite direction, where entering the on region and leaving the off region occurred separately. From responses to stationary stimuli one might have expected the response to the simultaneous event to have been greater. Hubel & Wiesel (1959) observed that the phenomenon of directionality could often be predicted by an asymmetry in flanking regions, but pointed out that this was not always true. Other investigators (Henry & Bishop, 1972) emphasized that there are some cells for which the preferred direction of movement cannot be predicted from the receptive field arrangement. Frequently a simple cell would give only one response to a movement that might from the stationary stimulus map have been expected to elicit two (as when the slit entered an on area, crossed to an off, and finally left the off area). Thus with similar receptive field arrangements one could get different patterns of response to moving stimuli. For example, while both of the cells represented in Text-figs. 1 B and C had a central off region flanked by two on regions, one responded with two peaks in both directions and the other responded with one peak in both directions. This Text-fig. 1. Response histograms and receptive field maps for selected examples of simple, standard complex and special complex cells. The layer in which each cell was found and the eccentricity of the centre of the field are as follows: Simple: A, layer 4a, b (50); B, layer 4c (30); C, layer 4a, b (20); D, layer 6 (7°). Standard complex cells: E, layer 2 (60); F, layer 3 (50); G, layer 6 (50; the length of the field was 160, and is not shown to scale). Special complex cells: H, layer 5 (90): I, layer 5 (7°). The response histograms were made using thin (ku) slits of light. They are labelled with a diamond, indicating the point at which the slit reversed direction, and arrows, indicating the direction of movement of the slit for the half of the histogram above the arrow. To the left of each histogram the horizontal mark represents 20 of visual field, and the vertical mark represents 10 spikes per bin. The vertical mark on the right of each histogram represents an instantaneous frequency of 20 spikes/sec. The receptive field maps were made using stationary stimuli: ( + ) indicates an 'on' response, (-) indicates an 'off' response. The arrows next to the fields are placed at the approximate positions of the peaks of the response histograms. The bar at lower right indicates the scale of the receptive field maps, and represents 1°. I5

PHY 268

C. D. GILBERT 398 is as if the threshold was higher for the cell in Text-fig 1C, so that only one peak showed above the base line. For many simple cells a slit that was longer than the receptive field elicited a smaller response than did a slit equal to the field in length. This property, which will be called end-inhibition, was considered by Hubel & Wiesel (1965) to belong predominantly to cells that otherwise resembled their complex cells. They termed these cells hypercomplex. Dreher (1972), using the criteria of Henry & Bishop (1972) for simple cells, and Rose (1974) both showed that end-inhibition was a property common among simple cells as well. When one defined simple cells using the criteria outlined in the present work, it was clear that they could not only. Simple 8C

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LAMINAR DIFFERENCES IN RECEPTIVE FIELDS 399 be end-inhibited, but showed a wide range of degrees of end-inhibition, and, as will be discussed below, were not different from complex cells in the proportion showing end-inhibition, or the amount of end-inhibition (Text-figs. 2 d-f, 9). Complex cells. Complex cells do not necessarily respond to stationary stimuli. If they do, they usually do not have separate on and off regions in their receptive fields; and they respond optimally to a slit that is much narrower than the field. Their response increases with slit width over a short range and then decreases as the slit is further widened. The slit that gives the best response is usually much narrower than the full receptive field width (the dimension perpendicular to the axis of orientation), and a slit of the appropriate orientation produces a good response wherever it is placed within the field (Hubel & Wiesel, 1962). These are the criteria used in the present study for complex cells. There were two major classes of complex cells that could be easily distinguished on the basis of their summation properties. Cells in the first class commonly showed summation along the orientation axis, that is, they gave a stronger response as the length of the stimulating slit was increased up to the full length of the receptive field. These will be referred to as standard complex cells. Cells in the second class responded at least as well to a very short Text -fig. 2. Length-response curves for selected simple cells in layer 4 (A-C), standard cell in layer 2+3 (D-F) and special complex cells in layer 3 (I) and in layer 5 (G, H). Vertical bars represent 1 S.D. on either side of average point. Response is expressed as percentage average response elicited with the slit of optimum length, which for cells A-T averaged 21, 50, 28, 62, 55, 17, 91, 37 and 88 spikes/sweep, respectively, to a slit moving in the optimal direction. For each unit the lateral borders of the receptive field were determined by testing its response to a slit centred at different positions along the axis of orientation. This gave a measure of receptive field length, indicated by the arrows. For both simple and standard complex cells the length of the receptive field along the orientation axis corresponded to that of the shortest slit that could elicit the maximum response. For the special complex cells the response peaked for slits of approximately 3° in length, but the true receptive field length was much greater. These units gave the same response to a short moving slit centred anywhere along the orientation axis within the responsive portion of the field. Another point illustrated by these curves is the fact that any of the three receptive field types can have the property of end-inhibition, where the response of a unit is worsened as the length of the stimulating slit is increased above a certain value. Units of each type can exhibit different degrees of end-inhibition. Special complex cells H and I had higher-order hypercomplex properties, showing inhibition to slits shorter than the responsive portion of the field. The eccentricities of the receptive fields of units A-I were 12, 2, 5, 8, 6, 5, 6, 9 and 6 degrees, respectively. I5-2

C. D. GILBERT 400 slit (as small as JO) as to a slit that extended the full length of the receptive field (which for these cells average 3°). These cells will be referred to as special complex cells. Standard complex cells. Representative standard complex cells are illustrated in Text-fig. 1. As mentioned above, they frequently responded to stationary stimuli (Text-fig. 1 E, F) but not always (Text-fig. 1 G). Unlike simple cells, they responded continuously as slits were moved across the full receptive field (Text-fig. 1 E-G). Like the simple cells, however, they frequently showed the property of end-inhibition, and the degree of endinhibition formed a continuum from 0 to 100% (Text-figs. 2D-F, 9). The standard complex cells shared a number of incidental properties with the simple cells: they had similar sharpness of tuning for orientation (Table 2), velocity preference (Table 2), directionality (Text-fig. 12), and spontaneous activity (Text-fig. 13). These properties are discussed in detail below. A total of ninety-five standard complex cells were analysed in this series. Special complex cells. Like the standard complex cells, the special complex cells responded to a moving slit as it was swept across the entire width of the receptive field. Those that responded to stationary slits gave a good response to a slit placed anywhere along the movement axis, and they responded optimally to a slit that was much narrower than the field. The salient property of these cells was, as indicated above, the fact that their response increased over a very narrow range of slit length, becoming maximal for slits that were much shorter than the receptive field (Textfig. 2a-I). These were originally described by Palmer & Rosenquist (1974). The special complex cells often exhibited a peculiar type of end-inhibition. The response of the cell was maximal for a very short slit, and then decreased somewhat for slits that were longer than this but still shorter than the receptive field length, and decreased still more for slits extending beyond the excitatory region of the field (Text-fig. 2B, C). This is one property of higher-order hypercomplex cells, a property previously thought to be common only in other visual cortical areas, such as 18 and 19 (Hubel & Wiesel, 1965). Since these cells had narrower orientation tuning curves for long slits than for short slits, it was important to determine the field's orientation with a long slit before making a length-response curve, to ensure that the decrease in response to a long slit was not an artifact of the narrower tuning curve. These cells tended to receive a more equal input from the two eyes than the simple and standard complex cells, almost always belonging to ocular dominance groups 3, 4 or 5 (Text-fig. 1 1). They also had the highest spontaneous activity of all striate cortical cells (Text-fig. 13), and the highest velocity preference (Table 2). Finally, the special complex cell had, on average, larger receptive fields than either simple or standard complex

LAMINAR DIFFERENCES IN RECEPTIVE FIELDS 401 cells. They were not significantly different from other classes in sharpness of tuning for orientation (Table 2) or directionality (Text-fig. 12). A total of thirty-two special complex cells were studied. iZJ

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Text-fig. 3. Sample electrode penetration, with receptive fields of units found along the track. The distance of each receptive field from the vertical meridian is represented as the distance of the field centre from the column of squares. Vertical positions of the field centres ranged from 5 to 8° below the horizontal meridian. Most units were marked by lesions (circles) in order to determine accurately their position within a layer. The cells found in this penetration demonstrate the types of receptive field characteristic for each layer (see text). Note that as the electrode moves from the deep to the more superficial layers the fields get smaller, even though they are shifting to greater eccentricities. The scale marker at lower left represents 1 mm. The abscissa at lower right also represents the scale for the receptive field size. A photo-micrograph of this penetration is shown in PI. 1.

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LAMINAR DIFFERENCES IN RECEPTIVE FIELDS 403

Correlation of receptive field properties with layer A representative electrode penetration, showing how each cell's location was determined, is illustrated in Text-fig. 3 and in PI. 1. The lesions were small enough (approximately 150 #m) and were made frequently enough to determine each cell's location within a layer. Text-fig. 3 also demonstrates that two parameters showed a particularly striking variation with layer. One was the proportion of simple and complex cells within each layer, and the other was receptive field size. 1. Type of field. Simple cells were found in the highest proportion in layer 4. They were seen also in the deep part of layer 3 and in layer 6, but occurred only rarely in layer 5 and not at all in layer 2. The result, illustrated in Text-figs. 4 and 7, is a bimodal distribution of simple cells. Standard complex cells, on the other hand, were found in layers 2 through 6, although there was a substantial drop in their numbers in layer 4 (Text-figs. 5, 7). The special complex cells were most commonly found in layer 5, but they were also frequently found in a band extending from the deeper part of layer 3 to the upper part of layer 4ab, resulting in a double-tiered distribution (Text-fig. 6). Most of the layer 4 complex cells (standard or special) lay either at the top of layer 4ab or at the bottom of 4c, leaving the middle of the layer almost entirely to simple cells (compare Text-figs. 4-6). A summary of the distribution of all three cell types with layer is given in Text-fig. 7. As mentioned above, a few units had non-oriented fields. Occasionally the recording electrode passed through a region of non-oriented hash. Both non-oriented units and non-oriented hash were encountered most commonly in layer 4, particularly in layer 4c. Again, it was not possible to tell whether these units were cells, fibres, or terminals, but if cells with Legend to Fig. 4. Text-fig. 4. Receptive fields of simple cells, found in different layers and at different eccentricities in the visual field. The location of the centre of the receptive field in this schematic indicates the layer (vertical axis) in which the cell was found and the eccentricity (horizontal axis) of the central point in the receptive field. The eccentricity axis also serves as a scale for the dimension of the receptive field. For the units illustrated in Figs. 4-6 the receptive field lengths were determined by length response curves and by mapping the field with a moving slit shifted sideways until the response ceased (see Text-fig. 2). The widths were determined using stationary slits and were also calculated from the response histograms. The smallest simple receptive fields were found for cells in layer 4. The cells in the deep part of layer 3 had fields of intermediate size, and those in layer 6 had very large fields. The density of shading of the field indicates the degree to which the cell was end-inhibited (see key).

C. D. GILBERT

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LAMINAR DIFFERENCES IN RECEPTIVE FIELDS 405 I

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Text-fig. 6. Receptive fields of special type complex cells (those that do not show summation for increased slit length). These cells had a two-tiered distribution, with one tier in the deep part of layer 3 and the upper part of layer 4ab, and the other tier in layer 5, clustered towards the top of the layer. The end-inhibition observed for these cells tended to be of the higherorder hypercomplex type. Both tiers of cells had intermediate size receptive fields. Other properties of these cells are discussed in text.

C. D. GILBERT non-oriented fields exist in the cat's striate cortex, then they are most likely to lie in layer 4. Cells with non-oriented fields have been described in layer 4c in the monkey (Hubel & Wiesel, 1968). 406

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2. Field size. Receptive field size changed markedly from layer to layer: the superficial layers had cells with small receptive fields, the deep layers (5 and 6) had cells with large receptive fields. Although in some layers one could find more than one receptive field class (such as the deep part of layer 3 or layer 5), cells situated in a given layer had receptive field sizes and shapes that were similar from one class to another (compare Text-figs. 4-6; see also Text-fig. 8). Thus it seemed that field size depended more on layer than on field type. It is known that receptive field size also changes with distance of the receptive field from the representation of the area centralis in the visual field (Wiesel, 1960; Hubel & Wiesel, 1960, 1962, 1974), but from the present results it was clear that at any given eccentricity there were marked differences in receptive field size for cells in different layers, as illustrated in Text-figs. 5-7. Text-fig. 3, which shows a sample electrode penetration,

LAMINAR DIFFERENCES IN RECEPTIVE FIELDS 407 also makes this point: when the electrode went from deep to more superficial layers, the field sizes got smaller, even though the fields were shifting to greater eccentricities. The receptive fields for all layers ranged from 0 to 150 eccentricity, making it possible to compare the median receptive field sizes for cells in different layers. 2 *

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Text-fig. 8. Length of receptive field (along axis of orientation) for cells in different layers. 0, simple cells; *, standard complex cells; A, special complex cells.

The measure of receptive field size that showed the most change from layer to layer was the length of the field along the axis of preferred orientation. Although field length was well correlated with field area, the layer 6 cells were more distinct from cells in other layers with respect to length than with respect to area or width. Text-fig. 8 is a plot of receptive field length for cells found in different layers, and Table 1 gives the median values for both length and area for each class of cell in each layer. Cells in layer 2 had small receptive fields, with median lengths of 1.5'. Most of the cells in layer 3 had lengths clustering around this value as well, but there was a population of cells in the deep part of the layer with larger fields, approximately 30 in length. The group with large receptive fields included all of the upper tier of special complex cells, all of the simple cells in layer 3, and a few standard complex cells. The cells in layer 4 had, by and large, small receptive fields. This was particularly true for the simple cells in the layer, which had a median

C. D. GILBERT length of 1.10. There were some units at the top of layer 4ab and at the bottom of layer 4c that, in having large receptive fields, wele very like the units at the bottom of layer 3 and in layer 5. These included the majority of standard and special complex cells in layer 4. The simple cells in layer 4 were quite similar in receptive field size to the standard complex cells in layers 2 and 3. 408

TABLE 1. Median receptive field sizes for simple and complex cells in each layer Layer 6 Layer 5 Layer 4 Layer 2 Layer 3 Length* (deg) 1.1 (32) 30 (4) 8.0 (7) Simple 8*0 (20) 2.8 (13) 2-0 (9) 1.3 (20) 1.5 (17)t Complex (standard) 2*9 (20) 2.8 (5) 3.2 (7) Complex (special) Area (deg2) 12.9 1.8 10.5 Simple 15-9 1-4 8*1 2-5 Complex (standard) 1*7 9*0 9*0 11.9 Complex (special) * Along axis of orientation. t The number of cells in each category are given in parentheses. TABLE 2. Orientation tuning and velocity preference for cells in different layers Cell type Layer 2

3

Orientation tuning* (deg) 43 Median 40 Range 20-60 25-85 Velocity preference

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5

6

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35 22-85

59 34-81

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Layer 5 had cells with receptive fields that were much larger and much more uniform in size than those in the upper layers, except for the large field cells at the bottom of layer 3. The fields had a median length of 2.90. Cells in layer 5 were distinct from those in the upper layers in other ways. They had high spontaneous activity (Text-fig. 13), tended to receive more equal input from the two eyes (Text-fig. 11), and had higher stimulus velocity preference (Table 2). The layer 6 cells had the largest fields of any in area 17. The following description pertains to both simple and complex cells in layer 6. Their receptive field lengths, defined by length-response curves (Text-fig. 10),

LAMINAR DIFFERENCES IN RECEPTIVE FIELDS 409 reached very large values. The widths (the dimension along the axis of movement) of the fields were much less than their lengths, making the fields long and narrow. Curves such as those in Text-fig. 10 demonstrate contributions to the cells' input from points quite distant (as much as 80) from the receptive field centre, but the contributions from peripheral parts of the field were much smaller than the contribution from the centre. This was most apparent from the linearity of the log lengthresponse curve in Text-fig. 10c, and could also be readily demonstrated by testing different parts of the field with short slits. Similarly, when a slit, moving back and forth through the field, was shifted along the orientation axis from outside the receptive field towards its centre, the cell would not respond until the slit was fairly close to the field's centre, and responded best when the slit was centred in the field. By using this technique to determine the lateral borders of the field one would get a deceptively low estimate of the field length. Occasionally a cell would not respond unless the slit covered a relatively long segment of the central part of the receptive field (Text-fig. 10B, D). The units showed summation for increased slit length up to sizes ranging from 4 to 160 (the longest slit that the apparatus was capable of generating). The field sizes for all the layer 6 simple and standard complex cells are shown in Text-fig. 8, and the median lengths and areas are given in Table 1. 3. End-inhibition. End-inhibition was common among the standard complex cells in layers 2 and 3 and among the simple cells in layer 4 (Text-fig. 9). In addition, the end-inhibition characteristic of special complex cells (see above) was frequently seen in both tiers of these cells. Very few of the standard complex cells deep to layer 3 and almost none of the simple cells outside of layer 4 were end-inhibited. It is possible to quantify end-inhibition by calculating the percentage reduction in response when comparing a cell's response to a very long slit with its response to the slit of optimum length. Thus if a cell's response was completely suppressed by a long slit, it would be classified as having 100 % end-inhibition. The percentage of end-inhibition covered the full range from 0 to 100 % for all cell classes. Text-fig. 2D-E illustrates the length-response curves taken from three standard complex cells lying in layers 2 and 3. These cells differed in the degree of end-inhibition. Some end-inhibition was found in well over half of the complex cells in layers 2 and 3 (Text-fig. 9), but 100 % end-inhibition was demonstrated in fewer than one-seventh of them. The proportion of units with end-inhibition and the median percentage of endinhibition was the same for standard complex cells in layers 2 and 3 and simple cells in layer 4. Finally, layer 6 was unique in having virtually no cells that were end-inhibited; the two exceptions had small receptive fields and may well have been axons of cells in the superficial layers.

410 C. D. GILBERT 4. Ocular dominance. Text-fig. 11 shows the ocular dominance distribution for each cell type in each layer. Of all the cells in area 17, simple cells tended to have the least mixing of input from the two eyes, and the special complex cells had the most. Accordingly, layer 4, the layer richest 2 _

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in simple cells (and also the layer receiving the densest innervation from the cells in the lateral geniculate nucleus, most of which are monocular), had the highest proportion of monocular units, with the monocular group 1 and 7 and the weakly binocular group 2 and 6 cells predominating over the moderately to strongly binocular group 3, 4 and 5 cells (by a 2-4:1 ratio). Layer 5, which had the highest proportion of special complex cells, was especially rich in cells that were equally or nearly equally influenced from the two eyes. The difference between the ocular dominance distributions of simple and complex (special plus standard) cells in all layers was primarily due to the special complex cells. There is still, however, a significant difference in the ocular dominance distributions of standard complex cells and simple cells. For the complex cells in layers 2 and 3, the ratio of group 1, 2, 6 and 7 cells to group 3, 4, and 5 cells was 1-5: 1,

LAMINAR DIFFERENCES IN RECEPTIVE FIELDS 411 whereas for the simple cells in layer 4 it was 2-4: 1. Even in layer 6 the simple cells tended to be predominantly influenced by one eye, while complex cells tended to be more equally influenced by both eyes. This suggests that the mixing of the input from the two eyes is progressive, from geniculate cell to simple cell to complex cell. A

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5. Directionality. Defining a directional unit as one whose response in the preferred direction is at least twice as great as the response in the opposite direction (after Schiller, 1976), it was clear that all layers had both directional and non-directional units. The highest proportion of directional units was found in layer 6 (Text-fig. 12). Both simple and complex cells were directional, and both covered the full range of directionality ratios. 6. Orientation and orientation tuning. Orientation tuning curves were made for approximately one-third of the cells studied. No layer was selective for a given orientation, nor did any layer have cells that were on average more sharply tuned than those in another layer. The range of

C. D. GILBERT 412 sharpness of tuning was, however, quite broad for every layer, so that with the small sample of orientation tuning curves available for each layer it was possible to miss small differences in average sharpness of tuning. No differences were seen in the orientation tuning of simple and complex cells. Layer 2+3

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7. Spontaneous activity. Most cortical cells, both simple and complex had very low spontaneous activity (Text-fig. 13). The notable exceptions were the special complex cells, which tended to have the highest and most variable spontaneous activity. As mentioned above, there were also a few standard complex cells with high spontaneous activity which had the same laminar distribution as the special complex cells. These cells covered a broad range of activity, from 0 to 30 spikes/sec. Most of the cells in other layers were silent. These results were taken from animals that were lightly anaesthetized with thiopental (i.e. they were given a dose just sufficient to produce a slow wave e.e.g. pattern). 8. Velocity preference. Although tuning curves of cells' responses to different stimulus velocities were not made, the velocity of the stimulating slit was adjusted to elicit approximately the optimal response. This gave only a rough measure of velocity preference, but it showed rather

LAMINAR DIFFERENCES IN RECEPTIVE FIELDS 413 consistent differences between different cell classes. The median velocity preferences for cells in different layers are given in Table 2. Simple cells in layer 4 had the lowest preferred velocities, and were not significantly different from the standard complex cells in the superficial layers. The 2

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for cells in different cortical layers. 0, simple cells; *, standard complex cells; A, special complex cells. A ratio of 2: i (interrupted line) is taken to divide directional from non-directional cells. No obvious differences in directionality existed for different cell types, except perhaps for the sixth layer cells, which tended to be more directional than the rest.

large-field cells at the bottom of layer 3 and the cells in layers 5 and 6 tended to have higher preferred velocities. Movshon (1975) found that on average complex cells have higher preferred velocities than simple cells. The present results show that this is true only for one type of complex cell. In summary, it appeared that layer, rather than receptive field type, was the determining factor for a number of receptive field properties. Properties of cortical cells antidromically activated from the lateral geniculate nucleus In an earlier study it was found that approximately half of the cells in layer 6 project to the lateral geniculate nucleus (Gilbert & Kelly, 1975). In the present study an effort was made to examine the receptive fields of the cortico-geniculate cells and to learn whether these cells had any special

C. D. GILBERT properties that would distinguish them from the overall population of layer 6 cells. The cells responsible for this projection were identified by activating them antidromically from a stimulating electrode placed in or above the geniculate. Although long penetrations were often made with 414

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the recording electrode in the fifth and sixth layers, few units satisfied the criteria of antidromic activation (see Methods). This was surprising in view of the anatomical results referred to above. The discrepancy may be due to a failure of the antidromic potentials to invade the somata of the layer 6 cells, which are known to have very fine axons (Cajal, 1922). In addition to the small proportion of layer 6 cells, a few units in layer 5 were activated antidromically from the lateral geniculate nucleus. This was unexpected because of the apparent lack, in anatomical studies, of any projection from layer 5 to the geniculate (Holhinder, 1974; Gilbert & Kelly, 1975). It is probable that the cortico-collicular fibres pass near the geniculate and can be activated by current spread from an electrode in it. Taken together with the difficulty of activating layer 6 units, this may explain why Toyama et al. (1974) believed layer 5 to be the source of the cortico-geniculate projection.

LAMINAR DIFFERENCES IN RECEPTI VE FIELDS 415 In layer 6 both simple and complex cells were activated antidromically (eight complex, two simple), and had the very large receptive fields characteristic for the layer. They were indistinguishable from the overall sixth layer population studied, in that they were oriented, binocular, and almost always directional. The antidromic latencies ranged from 11 to 3*2 msec, with a median latency of 1.5 msec. Five units in layer 5 were activated antidromically from the geniculate. Of these, two were special complex cells, both of which were end-inhibited. The other three were standard complex cells. The antidromic latencies of all the units ranged from 0O8 to 1*9 msec, median latency 1-5 msec. Like the over-all population in layer 5, the antidromically activated units were strongly binocular, had high spontaneous activity, and relatively large receptive field size. Neither special nor standard type complex cells in layer 3 were activated. In summary, then, the cells that were antidromically activated had properties typical of the over-all population of cells in the layer in which they were found. DISCUSSION

The clear association of receptive field characteristics with particular layers is of special interest in view of recent anatomical findings concerning the connectivity of cells in different layers. First the distribution of simple cells closely resembled that of the afferents from the dorsal layers of the lateral geniculate nucleus. Using light and electron microscopic autoradiography, LeVay & Gilbert (1976) found that the afferents from these geniculate layers terminate in two bands in the cortex, one extending from the bottom of layer 3 to the bottom of layer 4 and the other in layer 6. In the present study simple cells had a markedly similar distribution, lying at the bottom of layer 3, in layer 4 and in layer 6. The coincidence of the distribution of simple cells with that of the main body of geniculate afferents supported the hypothesis advanced by Hubel & Wiesel (1962) that the receptive fields of simple cells are constructed from the receptive fields of geniculate cells, and that this comprises the first step in information processing in the visual cortex. Secondly, most of the complex cells in the superficial layers lay outside the geniculate afferent zones, suggesting that they receive their input predominantly from an intracortical source. Except for the large pyramidal cells at the bottom of the layer, the cells in layer 2 + 3 do not send their basal dendrites into layer 4 (O'Leary, 1941), and therefore cannot get a direct input from the dorsal geniculate layers. A more likely source for their input is the population of cells in layer 4 that send their axons into

C. D. GILBERT 416 the superficial layers (Cajal 1922). In that case the simple cells would be the probable source of input for the complex cells in the superficial layers since complex cells are so uncommon in layer 4. This would fit well with the similarities in receptive field size between the layer 4 simple and the layer 2 + 3 standard complex cells. Given all this, one does not have to look too far to devise a plausible scheme to explain the manner in which complex cell receptive fields are constructed from simple receptive fields. In the transformation of visual information that occurs in the hypothetical pathway from layer 4 simple cells to layer 2 + 3 standard complex cells, many receptive field properties are conserved. The two cell classes have similar receptive field areas, orientation tuning, directionality end-inhibition and so on. The fact that simple cells responded to moving stimuli over a limited part of their receptive fields while complex cells responded over the entire field, however, requires a convergence from simple to standard complex cells (as suggested by Hubel & Wiesel, 1962), with simple receptive fields summing along the axis of movement to form standard complex fields. There need be no summation along the axis of orientation, since the receptive field lengths of layer 4 simple and layer 2 + 3 complex cells were nearly equal. Furthermore, the end-inhibition found in complex cells can be fully accounted for by the end-inhibition already present at the simple cell level, so there need be no processing in the simple-to-complex pathway or interaction between complex cells to construct hypercomplex fields. The absence of end-inhibition among standard complex cells in layers 5 and 6 then raises the possibility that their fields are constructed differently from the standard complex cells in the superficial layers. As an alternative to this hierarchical model of information processing, others (Hoffman & Stone, 1971; Stone, 1972; Stone & Freeman, 1973) have suggested that complex cells receive direct input from the geniculate in a pathway that is in parallel with the geniculate-to-simple cell pathway. This is based on evidence indicating that some complex cells can be driven monosynaptically from the geniculate (Hoffman & Stone, 1971) and that complex cells respond to higher stimulus velocities than simple cells (Pettigrew, Nikara & Bishop, 1968; Movshon, 1975). In most of these papers, complex cells were characterized as having large receptive fields (20 or more in width), high spontaneous activity (about 10 spikes/see) and response to high stimulus velocities. In the present study, these properties were common only to a subgroup of complex cells - those in layer 5 and at the bottom of layer 3, of which the special complex cell (the one that does not show summation along the orientation axis) was the predominant type. The large pyramidal cells at the bottom of layer 3 are likely candidates for the upper tier of these complex cells. Their dendrites

LAMINAR DIFFERENCES IN RECEPTIVE FIELDS 417 do invade layer 4 (O'Leary, 1941) and are therefore in a position to receive direct geniculate input. In the studies mentioned above, the cells in the more superficial part of layer 2 + 3 may have been classified as being simple, or may have been overlooked, being smaller and more sensitive to cortical damage and metabolic insult than the deep lying cells. There are, therefore, different kinds of complex cells that may have very different inputs. Those in the upper part of layer 2+ 3, which project to other cortical areas (Toyama et al. 1974; Gilbert & Kelly, 1975) would, as already mentioned, be hardly likely to receive direct geniculate input, and probably receive input from simple cells instead. Those in layer 5 (the origin of the cortico-collicular projection) and at the bottom of layer 3 (projection uncertain), on the other hand, could receive direct geniculate input. Thus, the connectivity of cells in the visual cortex depends not only on cell type but on the layer in which the cell resides. The special complex cell was situated in two tiers, one extending from the bottom of layer 3 to the top of layer 4ab, and the other in layer 5, predominantly in the upper part of the layer. This would seem to contradict the findings of Palmer & Rosenquist (1974) who believed this type to be unique to the fifth layer. It may be that the units recorded in layer 3 were merely the apical dendrites of the layer 5 cells, but the fact that they were restricted to a narrow band argues against this. The distribution of these cells bore a marked resemblance to that of the afferents from the C laminae of the lateral geniculate nucleus (LeVay & Gilbert, 1976). Whether there is a direct connexion between these afferents and the special complex cell is still an open question, but it is intriguing that this may represent another link in an interconnected system of cells that are involved with collicular function. The superior colliculus receives input from the special complex cells (Palmer & Rosenquist, 1974); the colliculus and the C laminae have similar retinal afferents (Hoffman & Stone, 1973; Fukuda & Stone, 1974; Kelly & Gilbert, 1975; Cleland et al. 1975; Wilson & Stone, 1975); and the two structures are connected with each other (Niimi, Miki & Kawamura, 1970; Graybiel, 1971). These pathways probably form the neuronal substrate for the 'two visual systems' that were demonstrated with behavioural studies (Schneider, 1969). Within the geniculo-cortical system there are separate pathways with different functions, one sending information to higher cortical areas (and ultimately involved with pattern discrimination) and one sending information to the superior colliculus (and involved with eye movements). The receptive field differences between cells in different layers are undoubtedly a reflexion of the fact that each layer has a unique site of projection. Cells in the superficial layers, the origin of the cortico-cortical

C. D. GILBERT projection, bad small receptive fields, were standard complex, and tended to be end-inhibited. Cells in layer 5, the origin of the cortico-collicular projection, were predominantly of the special complex type. The standard complex cells in the layer, although showing summation for increased slit length, were in other ways very similar to the special complex cell. They had large receptive fields (similar in median and range of areas to the special complex cell), had high spontaneous activity, belonged almost exclusively to ocular dominance groups 3-5, and were also similar to the special complex cell in their index of directionality and stimulus velocity preference. Both special and standard complex cells in this layer projected subcortically. The lack of summation, and the inhibition in some cells, for increased slit length is a phenomenon also observed in many cells in the superior colliculus, such as their high level of spontaneous activity and their tendency to be driven well by both eyes, may be important factors in the contribution of the cortex to the cells in the colliculus. The third major corticofugal projection is that from the cortex to the lateral geniculate nucleus, which originates from cells in layer 6 (Gilbert & Kelly, 1975). Perhaps the most salient characteristics of these cells were the optimal response to slits centred in their receptive fields and the summation for increased slit length up to very large values. They are well oriented, directionally selective, and predominantly binocular, which is curious in view of the fact that the geniculate cells are non-oriented, not directionally selective, and predominantly monocular. The loss of information concerning orientation and direction suggests a convergence of cortical cells having different orientation on to individual geniculate cells. The fact that the layer 6 cells are binocular and the geniculate cells monocular suggests that the cortico-geniculate pathway is inhibitory.Other workers have presented evidence that this is indeed the case. When the cortex is cooled there is an enhancement of the responsiveness of the geniculate units to visual stimuli (Kalil & Chase, 1970). Schmielau & Singer (1975) believe the influence to be different for X and Y cells in the geniculate. It may be that layer 6 is the source of inhibition of geniculate activity that occurs in the light during saccadic eye movements, which is different for X and Y cells (Noda, 1975a, b). In any event, the cortex does not seem to contribute directly to the receptive field properties of geniculate cells, in distinction to the cortical cells that project to the superior colliculuswhich do appear to have a role in constructing the receptive field properties of collicular cells (Sterling & Wickelgren, 1969; Wickel gren & Sterling, 1969). The marked differences in receptive field properties between cortical cells that project to the geniculate and cells in the geniculate suggests that the role of the cortex is more one of adjusting the level 418

LAMINAR DIFFERENCES IN RECEPTIVE FIELDS 419 of activity of geniculate units, instead of contributing to specific receptive field properties. It is common in the central nervous system for a nucleus to receive a recurrent projection from the target of its own efferents. Often the loop is closed over the shortest possible pathway, such as the cone to horizontal cell to cone loop in the retina. With the geniculocortical system this pattern is again present, and the cells that project back to the geniculate may receive a direct projection from it (LeVay & Gilbert, 1976). The finding that simple cells in layer 6 can be antidromically activated from the geniculate is consistent with this idea. Since the pattern of projection on to the geniculate is different for area 17 and for area 18 (Updyke, 1976), and since areas 17 and 18 may each receive input from a unique population of geniculate cells (Stone & Dreher, 1973; Gilbert & Kelly, 1975), each class of geniculate cell may receive a reciprocal projection from the particular population of cortical cells to which it projects. Kelly & Van Essen (1974) demonstrated that there is a strong correlation between receptive field type and cell morphology. The present study shows that a second major determinant of a cell's receptive field properties is the layer in which it lies. In the cat striate cortex the segregation of cells into layers, each layer receiving a unique set of afferents and projecting to a particular area, is reflected in differences in receptive field properties of cells in different layers. In this way cortical cells are segregated according to the functions that they serve. I thank Drs T. Wiesel and D. Hubel for their invaluable advice and criticism, Dr P. Schiller for his advice on the construction of the optic bench, Ms G. Grogan for assistance with animal preparation and histology, Mr J. Gagliardi and Ms C. Scott for help with photography, Mr M. LaFratta for machine work and Mr D. Freeman for help with the electronics. The work was supported by N.I.H. grants EY 0605, EY 0606, EY 00082. REFERENCES

CAJAL, S. RAM6N Y (1922). Studien uiber die Sehrinde der Katze. J. Paychol. Neurol. 29, 161-181. CLELAND, B. G., MORSTYN, R., WAGNER, H. G. & LEVICK, W. R. (1975). Longlatency retinal input to lateral geniculate neurones of the cat. Brain Res. 91, 306-310. DAw, N. W. & PEARLMAN, A. L. (1970). Cat colour vision: evidence for more than one cone process. J. Physiol. 211, 125-137. DREHER, B. (1972). Hypercomplex cells in the cat's striate cortex. Invest. Ophthal. 11, 355-356. FUKUDA, Y. & STONE, J. A. (1974). Retinal distribution and central projections of Y-, X- and W-cells of the cat's retina. J. Neurophysiol. 37, 749-772. GILBERT, C. D. & KELLY, J. P. (1975). The projections of cells in different layers of the cat's visual cortex. J. cornp. Neurol. 163, 81-106.

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LAMINAR DIFFERENCES IN RECEPTIVE FIELDS

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ROSE, D. (1974). The hypercomplex cell classification in the cat's striate cortex. J. Physiol. 242, 123P. SCHILLER, P. H., FINLAY, B. L. & VOLMAN, S. F. (1976). Quantitative studies in monkey striate cortex. I. The spatio-temporal organization of receptive fields. J. Neurophysiol. 39, 1288-1319. SCHMIELAU, F. & SINGER, W. (1975). Corticofugal control of the cat lateral geniculate nucleus. Expl Brain Res. 23 (abstr.), 183. SCHNEIDER, G. E. (1969). Two visual systems. Science, N.Y. 163, 895-902. STERLING, P. & WICKELGREN, B. G. (1969). Visual receptive fields in the superior colliculus of the cat. J. Neurophysiol. 32, 1-15. STONE, J. (1972). Morphology and physiology of the geniculocortical synapse in the cat: the question of parallel input to the striate cortex. Invest. Ophithal. 11, 338-346. STONE, J. & DREHER, B. (1973). Projection of X- and Y-cells of the cat's lateral geniculate nucleus to areas 17 and 18 of the visual cortex. J. Neurophysiol. 36, 551-567. STONE, J. & FREEMAN, R. B. (1973). Neurophysiological mechanisms in the visual discrimination of form. Handbook of Sensory Physiology, chap. 713. Central Visual Information A, pp. 153-207. TOYAMA, K., MATSUNAMI, K., OHNO, T. & TAKASHIKI, S. (1974). An intracellular study of neuronal organization in the visual cortex. Expl Brain Res. 21, 45-66. UPDYKE, B. V. (1975). The patterns of projection of cortical areas 17, 18 and 19 onto the laminae of the dorsal lateral geniculate nucleus in the cat. J. comp. Neurol. 163, 377-396. WICKELGREN, B. G. & STERLING, P. (1969). Influence of visual cortex on receptive fields in the superior colliculus of the cat. J. Neurophysiol. 32, 16-23. WIESEL, T. N. (1960). Receptive fields of ganglion cells in the cat's retina. J. Physiol. 153, 585-594. WILSON, P. D. & STONE, J. (1975). Evidence of W-cell input to the cat's visual cortex via the C laminate of the lateral geniculate nucleus. Brain Res. 92, 472-478. EXPLANATION OF PLATE

Photomicrograph of electrode penetration diagrammed in Text-fig. 3. The arrows point to the microlesions, not all of which are located entirely within this section. The lesions are approximately 150,um in diameter. The scale marker represents 1 mm.