0011-6989

79 Ojol-0533532.WO

MECHANISMS UNDERLYING THE RECEPTIVE FIELD PROPERTIES OF NEURONS IN CAT VISUAL CORTEX DAVID ROSE

The Physiological Laboratory. Cambridge CB2 3EG. U.K.: and Department of Anatomy. The Medical School, University Walk. Bristol BS8 ITD. U.K.’ (Received

14 October

1977:

in revised

form

17 July

1978)

Abstract-Several previous models of the circuitry of the cat’s primary visual cortex are briefly described and various difficulties with them are pointed out. It is argued that the situation is more complicated than any of these models supposed. and that some of the anomalies in previous models can be overcome if additional factors are considered. A new model is proposed in which cells with strong hypercomplex properties are driven directly by geniculate cells with superimposed receptive fields, and other cortical cells are driven by geniculate cells with more scattered receptive fields. This model accounts for many of the response properties of cortical cells. KeJ, Words-cat: cells.

receptive fields: visual cortex: orientation tuning: simple, complex and hypercomplex

IXl.RODtJCTION There is currently some debate over how the receptive field properties and response specificities of cells in

the cat’s visual cortex are generated. Several models have been proposed, but in many cases there is direct conflict between them. The mutual incompatibility of the proposals suggests that the construction of hardand-fast models may not be an appropriate method of approach: the situation is too complicated. Thus there are many properties of cortical cells which can be measured (receptive field size, shape and components, specificity for stimulus orientation, length direction of movement and binocular disparity, eye dominance, spontaneous and evoked firing rates, responses to flashing stimuli, etc.) and although cells can be grouped into clusters with similar characteristics, there are very few cells which possess all the characteristics of that cluster at the same time (Sherman, Watkins and Wilson, 1976; Rose, 1978; see also Tyner, 1975; Rowe and Stone, 1977). The formulation of overall trends and general principles may prove more helpful; the problem of how the cortex is “wired up” is not a convergent one. The previously proposed models for orientation specificity and intracortical connectivity will be briefly described first, and some of the difficulties with each of them will be pointed out. Alternative proposals to explain these and other properties of cortical neurons will then be put forward. Discussion will be restricted to the primary visual cortex (area 17) of the cat.

PREVIOL’SLYPROPOSED MODELS

Nomenclature The receptice field of a unit will herein refer to the region of the visual field in which any stimulus can influence cell firing. whereas the term dischnrge field

’ Present address: Department of Psychology, Berkeley Square. Bristol BSS 1HH. U.K.

will refer to the area of the visual field from which a particular moving stimulus (e.g. a dark edge. a bright bar, etc.) elicits an excitatory response (the “discharge centre” of Bishop. Coombs and Henry. 1971; see Fig. ID). The dimensions of these fields are the length (along the line of an optimally-oriented stimulus) and width (normal to such a stimulus). Thus for most simple cells the receptive field is wider than any of that cell’s discharge fields (Hub+ and Wiesel. 1962; Pettigrew. Nikara and Bishop, 1968; Bishop et al., 1971; Creutzfeldt. Innocenti and Brooks, 1974b; Fries and Albus. 1976; Sherman er a/.. 1976). The regions crossed by an optimal stimulus before and after it crosses the discharge field will be called sidebands (e.g. Fig. 1D. for a vertical bar moving horizontally). Finally, the regions where stimuli cannot themselves affect cell firing, but from which the responses to other stimuli can be influenced (Blakemore and Tobin, 1972; Maffei and Fiorentini, 1976: Rose, 1977; Nelson and Frost; 1978) will be called subliminal zones: these will be discussed further below. The influence of the subliminal zones will be described as to suppress or to augmenr the response from the discharge field. since these terms carry no implica’tion about mechanism (unlike the terms “inhibit” and “facilitate”). The side-bands, however, have become widely known as “inhibitory” and this nomenclature will (perhaps wrongly) be retained: it should be stressed that the exact nature of the mechanism underlying the side-bands is not certain yet_

8-10 533

First came Hubel and Wiesel’s suggestions (1962. 1965) that: (1) lateral geniculate nucleus (LGN) cells drive simple cells, which themselves drive complejr cells, which in turn excite and inhibit hypercomplex cells; and (2) the LGN inputs to a simple cell have their receptive fields lined up in a row (Fig. IA). There

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/Fig. f. Summary of some previously proposed models. On the right is the connectivity pattern for each model (LGN = LGN cell. S = simple, C = complex. W = hypercomplex, + = excitation, - = inhibition. Points about which the model is not specific are omitted. A. Hubei and Wiesel(1962 1965). Left: a row of LGN cell receptive fields (all either “on” or “off” centre, with antagonistic surround) determines the simple cell’s field. 8, Parallel input model (Hoffmann and Stone, L971: Stone and Dreher. 1973). LGN X and Y cells are distinguish~. and there may be weak excitation from simple to complex cells {dashed arrow). C. Creutrfeldt et al. (1974a b) Left: the single LGN input to a cortical cell responds equally to all orientations of a bar stimuhts, but intra-cortical lateral inhibition induces (large arrows) orientation-s~~city in the cortical ceil. D, Bishop et al. (1973); Henry et al. (1974b). Left:

plan of simple cell responsiveness to moving stimuli (optimal bar is vertical). Right: two types of complex cell are disringuished (C, and C2).

is now evidence that the hypercomplex cell stage may not be a separate one (Rose, 1974, 1977; RodisWollner, Pollen and Ronner, 1976; Wilson and Sherman, 1976; Gilbert, 1977j, and that additional, cortical inhibition improves orientation tuning (see below). Also, complex cells can be activated by stimuli to which simple cells do not respond (Movshon, 1975: Hammond and MacKay, 1977). The second, or “parallel input” mode1 has, in its extreme form, simple ceils driven by LGN X afferents and complex cells directly by Y afferents (Hoffmann and Stone, 1971; Stone and Dreher, 1973; see Fig 1B). Complex (or Y) cells inhibit simple (perhaps via an inhibitory interneuron. which would have complex or Y cell properties) (Stone and Drehet, 1973; Movshon. 1975; Singer, fretter and Cynader, f975). and there is some evidence that simple cells a Simple and complex cells are. as Creutdeldt er al. (1974a. b) suggested. assumed roughly equivalent to Creutzfeidt er nl.‘s cells with small and large discharge fields respectively (measuring size across thewidrft of the field). This terminology has also been used by Lee,Cieland and Creutzfeldt (1977b).

provide a weak. secondary drive to complex cells (Blakemore and Van Sluyters, 1975: .Movshon. 1975). A problem with this theory is that complex cells arc most commonly found outside cortical layer 4. the densest region of LGN afferent termination (Hubef and Wiesei. 1961; Kelly and Van Essen. 1974: Gilbert, 1977; cf. Creutzfeldt er al.. 1971b). The problem of whether X and ‘or Y ceils drive simple and;or complex cells applies to the following models as well. Third. the model of Creutzfeldt and co-workers (Creutzfeldt. Kuhnt and Renevento. 1974a; Creutzfeldt er al.. 1974b3 also has both simple and complex cells driven directly by LGN afferents. with complex ceils inhibiting simple cells (as well as each other)iz see Fig. 1C. Each cortical ceil is driven primarily by only one LGN cell (or by a small number with superimposed receptive tieids: Lee er al., 1977b). The orientation specificity of cortical ceils is derived entirely from intracortical lateral inhibition (Hess, Negishi and Creutzfeldt. 1975). Some cortical ceils may be driven only intracortically, but each by just one other cortical cell. i.e. without convergence of excitation such as proposed by Hubei and Wiesef (1962). The model is not specific about the properties of the second-order cells (which may be common in cortical layers 2 and 6: Toyama, Matsunami. Ohno and Tokashiki. 1974: but cf. fto, Sanides and Creutzfetdt, 1977). Thus according to the extreme form of Creutzfeldt er al.‘s model for orientation tuning (Fig. 1C) the excitatory input to first-order cortical cells is nonorientationa and inhibition is maximal at 90’ to the preferred orientation. However, intracellular recording revealed that “in most ceils, inhibition as well as excitatior appeared to be less marked during stimulation in the non-optimal orientation.. .” (Creutzfeldt ef nL, 197411 p. 263). The extreme form of the model may therefore not always be appropriate (unless the appearance of both EPSPs and IPSPs is simply made clearer when there are few IPSPs). Several of Creutzfeidt et 01.s (1974b) arguments are based on receptive field size and location which they estimated from post-stimulus-time histograms (PSTHsI. but these show discharge fields not receptive fields (see Nomenclature). However, there is further evidence to support Creutzfeldt et nf.‘s (1974a) suggestion that some receptive fields are roughly circular: this can be seen in cells which are very responsive to small spot stimuli (Rose, 1978): also the length of a simple cell receptive field as estimated quantuatively is in many cases similar to or only slightly greater than its width as estimated using stationary flashing stimuli (Gilbert, 1977; Rose. 1978). Finally, there are the proposals of Henry, Bishop and co-workers. Their plan of a simpIe cell receptive field (Bishop. Coombs and Henry, 1973: Henry, Dreher and Bishop, 1974b3, derived from the PSTHs to moving bars,. consists of a central discharge zone surrounded by an area of inhibition (the “sidebands”). except along the line of the optimal bar, where there are “non-responding end-zones” iFig. 1D). When the stimulus is moved in the non-preferred direction (in directional cells) or isr orientated and moved at 90” to the optimal. then the discharge centre and the end-zones disappear. Excitation disappears when the orientation is wrong because. as Hutxl and Wiesel (1962) postulated (Fig. 1.4). a row of LGN

jaj

Receptive field properties of neurons in cat visual cortex

receptive fields must be activated simultaneously to drive the simple cell. The suppression of the discharge ccntre when the direction of movement is wrong is due to a special inhibitory mechanism (Goodwin. Henry and Bishop. 1975). Henry. Bishop and coworkers offer no explanation as to why the end-zones disappear, but this probably occurs because they are regions where a tail-off from the excitatory discharge centre is balancing out the inhibition from the surrounding side-bands, to give no overall effect on cell firing: the end-zones therefore disappear whenever the discharge centre disappears. Henry er al. (1974b) use this plan to explain the fact that orientation tuning is broader for short bars than for long (Henry, Bishop and Dreher. 1974a; Henry et al., 1974b: Palmer and Rosenquist, 1974: Rose, 1977). As bar length is increased, the bar will encroach on the end-zones when the orientation is optimal, but more and more on the inhibitory sidebands as the orientation is turned away from the optimal. Orientation tuning for a srarionary flashing bar is very similar to that for a moving bar of the same length (Henry et al.. 1974a; Hammond, Andrews and James, 1975: Rose. 1978) and Henry er al. (1974b) therefore predict that when the inhibitory side-bands are stimulated with stationary stimuli. inhibitory responses will be observed just as for moving stimuli. However. Bishop. Dreher and Henry (1972) and Bishop er al. (1973) have made the point that when the inhibitory side-bands are stimulated with stationary stimuli. excirarory responses are frequently obtained at “on” or “off” in different parts of the side-bands.3 Orientation tuning for stationary flashing bars therefore cannot be explained solely in terms of the receptive field plan described by Bishop er al. (1973) and Henry et al. (1974b). Complex receptive fields do not contain such inhibitory side-bands, and according to Henry er al. (1974b) their orientation specificity must derive. as Hubel and Wiesel said, from simple cell input (in which case inhibitory side-bands should still be present, if very weak, in complex fields). Other complex cells studied by Henry er al. (1974b) were not more broadly tuned for the orientation of shorter bars (though this might. as they suggest, have been disproved if they had used a wider range of orientations). and since many complex cells also respond to very high velocities of movement, these authors postulated a second type of complex cell driven di-

rectly by LGN alferents instead of by simple ceils (Fig. 1D). No attempt was made. however. to explain the orientation tuning of this second tyw of complex cell. Those hypercomplex cells which resemble simple cells when stimulated with short bars (Dreher, 1972: Henry et al.. 1974a) were considered by Henry er al. (1974b) to have a receptive field plan similar to that of simple ceils, but with inhibition filling in the endzones. ALTERNATIVE PROPOSALS The role of rhe subliminul

zones

In experiments reported elsewhere (Rose, 1977) a single bar of light at the optimal orientation was moved across the receptive field. and the bar’s length was varied symmetrically about the midline through the discharge field. When the bar was extended beyond the discharge field (called in that paper the “centre”) into what were called the “flanks” of the receptive field. the cell’s firing was often influenced profoundly, being either suppressed or au_mented. It was suggested that the flanks of each cell could have mixed suppressive and augmentatory influences (in various ratios) on the responses to stimulation of the centre, and that they may perhaps encircle the centre completely. The findings were the same for simple and complex cells. which were also alike in the average sizes of their receptive field centres and flanks. Stimulation of the Ranks alone did not affect the cell’s spontaneous firing, and it therefore seems likely that these flanks are parts of the subliminal zones which have been described by Blakemore and Tobin (1972). Maffei and Fiorentini (1976) and Nelson and Frost (1978). Nelson and Frost have shown that these zones are larger than the inhibitory side-bands discovered by Bishop, Henry and co-workers (see above).” (The side-bands may be part of the “centre” complex of mechanisms, and their function may be to improve stimulus localization, binocular disparity selectivity or spatial frequency specificity.) Gilbert (1977) has recently presented evidence that the suppressive and augmentatory influences from the flanks predominate in different layers of the cortex: suppressiv-e zones are commonest in layers 2-5, while cells whose responses are facilitated over a wide area are found mainly in layer 6. What mechanisms may underlie the suppressive and augmentatory components of the subliminal ’ More recent work shows simple cells with co-extensive zones? First, there are subcortical processes. When areas of excitatory responsiveness to stationary and mova bar is extended beyond the centre of an LGN receping stimuli (Goodwin. Henry and Bishop, 1975; Fries and tive field, the antagonistic surround depresses the Albus. 1976). It seems therefore that various relationships total spike count (even including the response which are possible between such areas (Bishop rr al.. 1971). is now evoked from the surround) (Dreher and San’ Most of the subliminal zones are orientation-specific. unlike the side-bands. Fries, Albus and Creutzfeidt (1977) derson, 1973). Further extensions may evoke infound that orientation-specific suppression from outside fluences from yet another surround which antagonizes the discharge field originated mostly from the side-bands. the first (Maffei and Fiorentini, 1972: Hammond, The apparent disagreement between Fries er al. and Nelson 1973) and in all cells there is a large, silent suppressive and Frost (1978) may be one of emphasis: Fries et al. did surround (Levick, Cleland and Dubin, 1972; Dreher not exclude some influence (30-40”;) from outside the sideand Sanderson, 1973); this silent surround has the bands. It is likely that the subliminal zones extend right same diameter-about 6’ +-as the suppressive comacross the side-bands and even across the discharge fields. and they may well become stronger towards the centre ponent in the subliminal zones of cortical fields (Mafof the receptive field. The fact that Fries et al. were stimu- fei and Fiorentini. 1976: Rose, 1977). The periphery lating the inhibitory side-bands might explain their failure effect, which extends over tens of degrees (e.g. Cleland. to find any augmentatory influences. Dubin and Levick. 1971). might augment cell re-

535

DAVIDROSE

when gratmg stimuli are used, but it is probably too weak to be of relevance in experiments using only a single bar as the stimulus (as Rose. 1977). It is therefore to be expected that cortical cells will respond to very long bars more weakly than to bars of some shorter. optimal length (just sufficient to acti‘rate maximally the centres of all the LGN cells driving the cortical cell). This will be especially true if those LGN cells are involved which have such strong surrounds that they hardly respond at all to large stimuli {e.g. Cletand c(t LID..1971). It will also apply ii there is some threshold input which must be exceeded in order to drive the cortical cell; the presonce of such a threshold is implied by the much lower spontaneous activity of most cortical cells. On this modet. then. the suppressive zones contained in many cortical receptive &Ids are. at least in part. ~js~cji~r~rory rather than inhibitory. However, further mechanisms may also underlie the subliminal zones. Thus the terminals of geniculocortical fibres are probably all excitatory in function (Carey and Powell, 1971: Toyama er nl., 1974; Singer rr (I/.. 1975) and there is a scatter of up to 6’ in the receptive field locations of fibres entering the cortex at a given point (Creutzfeldt and Ito, 1968). Some bcilitatory or disfacilitatory influences could therefore be reaching the subliminal zones from the terminals of LGN fibres other than those which provide the r,ruin dries to the cell. Within the cortex. there is evidence that ceils within the same functional column faciIitate each other, while inhibiting ceils in neighbouring columns (Blakemore and Tobin, 1972: Szentagothai. 1973; Hess et ‘J/.. 197j: Singer and Lux. 19751.Within a given orientation column. the geometrical centres of the receptive fields may be offset from one another by 2-4” (Hubel and Wiesel. 1962: Creutzfeldt er al., 1974b; Albus, sponsa

’ The orientation-specificity of all the augmentatory and some of the suppressive flanks discovered by Maffei and Fiorentini (1976). Fries et al. (1977) and Nelson and Frost f 1978) also suggests that cortical mechanisms are at work. The non-orientarional suppressive influences which were apparent in other cells could have been cortical (as proposed by MatTei and Fiorentini), or subcortical (in the LGN: see above). The presence of widespread facilitation mainly in cells in layer 6 (Gilbert. 1977) fits with the suggestion of Creuttfeldt. Garey. Kuroda and Wolff (1977) that obliquely descending fibres may spread excitation; but this facilitation may still be tuned to the preferred orientation of the recipient cell (cf. Maffei and Fiorentini, 1976). * In view of the doubts expressed by Creutzfeldt ef al. {lY74a b; 1977) and Iro er ~11.(1977) over the vertical spread of excitation. it should be pointed out that intracolumn facilitation is not an essential requisite for this argument. Nor is it essential for the orientation columns to have discrete boundaries (Albus, 1975b: Lee, Albus, Heggelund, Huime and Creutzfeldt, 1977a). - For brevity, ceils with extremely strong suppressive Banks will be referred to as “hypercomplex” cells (Rose. 1977). The inverted commas indicate that the word hypercomplex is describing an attribute of these cells, not defining a separate class of cells. J Within S-10’ of the visual axis. the centre diameters of LGN fields average about 1’ and do not exceed 3” (Sanderson. 1971: Hoffmann. Stone and Sherman. 1972). For cortical cells with weak or no apparent suppressive flanks, responses continue to increase rapidly with increasing bar length up to 4’ on average (range $9’: Rose, 1977).

197Sa; MafTei and Fiorentini. 1977) and this might explain some facifitatory input from the region surrounding the central discharge field. Also, there are cells very broadly tuned for orientation in nearby columns which would respond even to bars optimalI> oriented for the column under consideration (e.g. Albus. 1975b) and these could contribute to the suppressive zones.5 As a short bar, the same length as the discharge field. is elongated at the optimal orientation to encroach upon the subliminal zones, there will therefore be an increasing amount of facilitation from within the same column, and an increasing amount of inhibition from neighbouring columns (up to a limit). As a simiIar short bar is elongated at off-optimal orientations the same will apply. but the ratio of fac~itation/inhibition will be lower. because the bar is now optimal for a neighbouring column. As the orientation of the bar becomes further and further from the optimal for the cell. inhibition from the subliminal zones will eventually predominate over faci!itation. The orientation tuning curve for the elongated bar will therefore be narrower than for the short bar.6 This argument appiies for moving or stationary bars or edges. The mechanism of the discharge field

In my previous experiments (Rose. 1977, 19751 a large number of parameters of cortical cell behayiour were measured and a cross-correlation analysis between them was performed. Some of the main findings of this study were: (1) There is a continuum in the effect of stimulating the “flanks” (subliminal zones; see above) from profound suppression, to no effect. to clear augmentation of the discharge evoked from the “centre”. (2) Cortical units with strong suppressive flanks have shorter discharge fields than do units with weak suppressive flanks (see Fig. 2). Cortical cells with strong suppressive flanks (“hypercomplex” cells)’ in fact respond best to bars whose length is similar to the diameters of the receptive field centres of LGN cells in the same region of the visual field.* (Note that geniculate ceIIs fire most vigorously to moving bars when the bar’s length is the same as or less than the diameter of the receptive field centre: Dreher and Sanderson, 1973; Rose, 1977.1 (3) Cortical cells with strong suppressive flanks respond well to small spots of light (as also noted by Henry et at, 1974a). This is not true of most other cortical cells, but is true of LGN cells. (4) The stronger the suppressive flanks of cortical cells, the broader the range of orientations of a long bar to which the cells respond (even if relative11 weakly). One expianation for these observations is that they reflect the arrangement of the receptive fields of the LGN cells which drive each cortical cell. This model will first be described, and how it fits the above observations will then be explained. A new model. In essence, this model proposes that the LGN cells which drive simple ati complex ceils in the cortex huce scattered receprice fields (perhaps aligned in a row) whereas those dririny crlls i. is endowed on the cell by its LGN inputs. This model has enabled the results of previous experiments (Rose, 197i. 1978) to be explained. However, a good model should be able to predict the results of further experiments. as well as being compatible with the established facts (e.g. of cortical anatom!). Also. since no two cortical cells are identical. the model must be sufficiently flexible to accommodate the variations between cslls. These issues will now be discussed.

t -8

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0

1 ‘8

X Fig. 4. A. B. At the top (A) is a plan view of 5 LGN receptive fields aligned in a row (thick lines show field centres. thin lines. the surrounds). In B. the profiles of the 5 LGN fields are shown superimposed in alignment with the plan view in A, assuming the profile of Fig. 3B. In A. the centre and surround radii are drawn at a distance of 2.5 x the standard deviation of their respective Gaussian functions from the exact middle of the receptive field. The offset of each receptive field from its neighbour is D, which equals 2!,. 2 in this figure. C. The algebraic sum of the 5 LGN receptive field profiles in B is shown. This is the cortical receptive field profile g(s). It is shown in alignment with A and B. so the s-axis (distance across the receptive field) applies to all parts of the figure. (If D were equal to 1,‘,,‘2. then y(.~) would have a single central peak with a rounded top. and if D = 3’, 2. 5 distinct peaks would be visible.)

tory influence on the cortical cell from the one LGN ceil whose field centre the spot is traversing. The more the LGN field centres overlap, the more likely the cortical cell will be to respond to a spot stimulus. (iv) The more scattered the LGN input fields. the narrower the tuning for orientation should be (if the scatter is along a straight line). This is assuming that orientation-specific lateral inhibition (Blakemore and

Tobin, 1972; Rose and Blakemore, 1973a: Hess er al.. 1975) is added on to cortical cells in amounts which are not correlated with the degree of scatter of the LGN inputs: Thus the model can account for the experimental results (l)-(4) listed above.

I

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5

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X’ Fig. 5. The curves obtained by integrating the cortical field profiles (e.g. Fig. 4C) between .V= --I’ and I = +x’ are plotted here as functions of x’ (as was done for the LGN profiles in Fig. 3D). Panels A. B and C are based on the profiles in Fig. 3.4. B and C respectively. The four curves in each panel are for different offsets between the LGN fields (D in Fig. 4.4): this was nj, 2. and the value of n is displayed alongside each curve. The arrow to the right of panel A represents a threshold for the firing of the cortical cell (see text).

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Fig 6. A. A large cortical cell is shown. displaced vertically (for clarity) above the terminal arborizations of four LGN axons (approximate dimensions from Szentagothai. 1973). Ignoring the partial random scatter of LGN receptive field locations, these axons have fields shown here separated by an amount which assumes that 1 mm in the cortex is equivalent to 1’ in the visual field, a situation which pertains for receptive field eccentricities of about 2 - 4’ (Albus, 1975a: Wilson and Sherman 1976). B. The probability p that a synapse will form between any LGN fibre and the cortical cell is drawn here qualitatively as a function of the location of the LGN cell’s receptive field. The quantitative aspects of this function depend on the amount of dendritic surface available. on the possibility of saturation (p approaching 1.0, which would flatten the curve), on the density of axonal terminals as a function of distance from the parent axon and on the “random” scatter of the receptive fields of the LGN fibres (see above). (A similar approach has been used by Wilson and Sherman, 1976.) a-neuron with long dendrites in layer 4. b-neuron with short dendrites in layer 4. c-neuron with long dendrites away from layer 4. A threshold probability for a significant effect on the firing of the cortical cell (arrow at right) would make the change from a to b or c more pronounced. Some further consequences of the model It has been suggested above that for “hypercomplex” cells: (1) the suppressive flanks are at least in part due to subcortical mechanisms and (2) orientation-specificity depends entirely on intracortical influences, which is not the case for non-“hypercom’ Puzzlingly, their only illustration of orientation tuning in one of these hypercomplex cells during bicuculline application (Fig. 3 of Sillito and Veniani. 1977) shows a response to short stimuli moving in a direction 90” clockwise from the optimal which is equal in magnitude to that at the optimal, but a much smaller response is shown at 90” anticlockwise from optimal. Clearly, further work is required to clarify the exact shape of the orientation tuning curves of these cells under bicuculline. and whether, as Sillito and Versiani suggest, it matches the normal (drugfree) curve of layer 5 corticotectal cells.

plex” cells. The predictions are thus set up that the abolition of cortical inhibition. such as would occur with bicuculline if the inhibition depends on GABA (Sillito, 1975a). will remove “hypercomplex” cell orientation-specificity completely. but will not eliminate length specificity. These predictions have both been verified by Sillito and Versiani (1977). Hypercomplex cells in layers 2 and 3 became only slightly more responsive to long bars during microiontophoretic application of bicuculline, but they did come to respond to short bars equally at the optimal orientation and at 90” from the optimal. Some cells responded to short stimuli moving in any direction, in full verification of the above predictions. However, most of Sillito and Versiani’s cells still did not respond to short stimuli moving in a direction 180’ from the optimal, i.e. direction selectivity was not reduced by bicuculline.’ The suggestion that layer 2

Receptive field properties of neurons in cat visual cortex and 3 hypercomplex cells are driven by layer 5 corticotectal cells (Sillito and Versiani, 1977; Sillito, 1977b) could account for this observation, but as Sillito and Versiani pointed out, it is not a perfect explanation (not even with the addition of widespread, GABAmediated inhibition coming to these dk from complex cells: Sillito, 1977b).i” Sillito and Versiani went on to suggest that hypercomplex cells may have other excitatory inputs in addition to corticotectal cells: if these include LGN cells, this might resolve the apparent conflict of their data with the proposals put forward in the present paper. However, direct evidence as to whether or not hypercomplex cells receive bicuculline-resistant directional inhibition (such as is received by corticotectal cells: Sillito, 1977a) should be sought. and the effects of bicuculline on cells with hypercomplex properties outside layers 2 and 3 (Gilbert, 1977) should also be investigated, before defmitive conclusions are drawn. Four out of five cells studied in each eye in previous experiments (Rose, 1977) were relatively much less responsive to spot stimuli in the non-dominant eye. i.e. ocular dominance was greater for spots than for long bars. These four cells, however, had similar centre and flank lengths in each eye. This implies that their LGN inputs had receptive fields which were scattered over the same total distance (along the line of the optimal bar) in each eye. The cortical cell’s receptive field in the dominant eye probably has more LGN inputs than that in the other eye (which is why it is dominant). If these assumptions are true, the LGN inputs in the dominant eye have field centres which overlap one another more than they do in the other eye [see explanation (iii), above]. Modifications and qualijcations

A few variations on the basic proposals have already been considered (see (ii) and (iii) above). Some others will now be discussed. Some complex cells lose their orientation-specificity completely when bicuculline is applied by microiontophoresis (Sillito, 1975b) which argues against their being driven by LGN cells with their fields in a row or by simple cells in the same column only. They may instead be driven by LGN Y cells with superimposed fields, since Y cells have larger fields and weaker surrounds than X cells (Hoffmann er al., 1972; Hammond, 1973). (W cells also have large fields, but strong suppressive surrounds: Cleland, Levick, Morstyn and Wagner. 1976; Wilson, Rowe and Stone, 1976). Alternatively, the LGN inputs to these complex cells may have their fields arranged in some other non-linear pattern or even in a rectangular matrix for Wilson and Sherman (1976) have found that the rvidrh of a complex cell’s field is about twice the aver” Corticotectal cells respond more weakly to short stimuli at 90’ from the optimal than at the optimal, their spontaneous activity is usually inhibited by stimuli moving at 180’ from the optimal direction, they often respond to optimally-oriented long bars as strongly as to small spots of light. and their receptive field lengths and widths are very large (Palmer and Rosenauist. 1974: Gilbert. 1977: Silhto. 1977a; Siilito and Versiadi, 1977; Rose, 1978). None of these observations fits Sillito and Versiani’s model for hypercomplex cells exactly.

541

age diameter of LGN field centres. near the visual axis (supported qualitatively by Lee er al.. 1977b). The presence of cells which are completely non-orientational for small spot stimuli though tightly tuned for the orientation of long bars (e.g. Fig. 7 of Rose. 1977) is also most easily explained by a direct. non-orientational LGN input to these cells. The broader orientation tuning of complex cells overall compared to simple cells (Rose and Blakemore, 1974b: Henry et al., 1974b; Ikeda and Wright, 1975; Singer et al., 1975; Wilson and Sherman. 1976) is also compatible with the above suggestions. If some complex cells receive LGN inputs which are scattered across the width of their receptive fields, then an analysis similar to that of Figs 3-5 can be performed with x and x’ representing dtstances across the width rather than the length of the cortical receptive field. This would lead to the prediction that preferred bar width increases for these cells in proportion to the amount of scatter of their inputs. just as occurs for bar length (Fig. 5). Experimental results are, however, confusing. Hubel and Wiesel (1962) and Toyama, Maekawa and Takeda (1973) found that simple and complex cells respond best to bars of similar width, despite the much wider fields of complex cells compared to simple. MatTei and Fiorentini (1977). however, reported that for all cortical cells the field width is closely related to the preferred spatial frequency (another measure of bar width). (The “field widths” measured by the above workers were plotted with stationary flashing bars for simple and some complex cells). On the other hand, the complex cells studied by Sherman er al. (1976) did not have a clear preferred width of stimulus, but responded equally well over a range of bar widths. It has been proposed that summation may not be symmetrical across the length and width of some cortical receptive fields (Hubel and Wiesel, 1962; Rose, 1977). but in view of the experimental results cited above it is not clear yet whether a special mechanism must be postulated to account for this. The discussion so far has dealt only with the model’s ability to explain orientation and length tuning. It should be pointed out that there are other properties of cortical cells which the model as it stands does not account for, such as direction specificity, the spatial pattern of responsiveness to stationary flashing stimuli, the presence of inhibitory sidebands in simple cell receptive fields and binocular disparity specificity. There is evidence that additional mechanisms are responsible for at least some of these properties. For instance, the degree of direction specificity of a cell is not correlated with its orientation or length tuning (Rose, 1978), the directionality of the discharge field(s) is not necessarily the same as that of the subliminal zones (Fries et al, 1977; Nelson and Frost, 1978), and local application of bicuculline can eliminate directionality in some cells (Sillito, 1977a). Bicuculline can also abolish the segregation of -on” and “off” areas across the width of simple cell receptive fields (Sillito, 1975b). The relationship between the inhibitory side-bands and “on” and “off” areas,’ and selectivity for bar width or spatial frequency, require further clarification before their underlying mechanisms can be understood. Much of the discussion above has also been con-

fined to cortical cells driven directly by LGN affersnts. At the moment. the proportion of cortical cells which are driven mainly and directly by LGN afferents has not been established with certainty. It has been assumed that “hypercomplex” cells are-included m this category (see also Hoffmann and Stone. 1971). .Mhough previous work suggested that “hypercomplex” cell bodies lie mainly in cortical layers 2 and 3. away from the main band of LGN terminal boutons (Kelly and Van Essen. 19711. cells with “hypercomplex” properties have recently been shown to occur in ull layers. including layer 4 (Gilbert. 1977). Also. some LGN terminals can be found at almost every level throughout the depth of area 17 (LeVay and Gilbert. 1976). The extent to which “hypercomplex” ceil dendrites cross laminar boundaries is unknown. as is the relative effectiveness of the many sources of synapses onto a cortical neuron. The model proposed m this paper was derived initially from correlations (between flank strength, field centre length and orientation selectivity) observed only among cells with overall suppressive flanks (Rose. 1977. 1978). This. together with Gilbert‘s (1977) study showing that suppressive and augmentatory inHuences from around the field centre may concentrate on cells in particular layers in the cortex. casts doubt on the idea that cortical cells are all equally likely to receive suppressive and augmentatory influences. both to any degree of strength. Instead, the au_qnentatory influences at least may be directed more selectively within the cortex. In the Introduction it was suggested that the consideration of overall trends is a better strategy than the exposition of hard-set models of so-called “typical” cells, For example. the narrower orientation tuning of individual cells for long bars than for short bars can be explained in terms of.the general principles that inhibition spreads laterally. and excitation vertically, wtthin the cortex. It must, however. be noted that many of the other proposals I have presented in this paper contain a number of over-simplications which make them seem more rigid than they should be. For instance. divisions have been made between the discharge field, side-bands and subliminal zones, the primary drive to the cell and any secondary inputs, and cells driven directly by LGN afferents and those driven only by other cortical cells: these divisions are probably all not as clear-cut as has been assumed. Also. there may be several mechanisms underlying the subliminal zones (i.e. there may be several types of zone), and the model I have proposed for the receptive field only incorporates two of these mechanisms: the suppresstve surrounds of LGN fields and cortical orientational inhibition. Even within the basic model the complexity of the situation is such that a few cells which deviate from the general pattern may be expected (‘*uncommon” cells: Tyner. 1975). Further mechanisms such as those responsible for augmentatory subliminal zones might overlay the general pattern (especially in certain cortical layers). The relationships between the many mechanisms which may influence a cortical cell (their relative strengths and spatial extents, and the linearity of their integration). and their role in generating or modulating the selectivity of the cell for visual stimuli. are

just some of the complexities of the cat’s visual cortex for future research to unravel. .-lc~no~vf~tfyemenrs-I would like to thank C. Blakemore and M. A. Georgeson for their helpful comments on earlier versions of the manuscript. A. 51. Sillito and J. I. Nelson for much useful discussion of particular topics and A. Featherstone and D. Ellis for photographic and secretarial assistance. The experimental work was supported by a M.R.C. scholarship to the author and M.R.C. grant No. G972,463 B to C. Blakemore. and the computer was provided by the S.R.C. REFERESCES .4lbus K. (1975aj .4 quantitative study of the projection area of the central and paracentral visual field in area 17 of the cat. I. The precision of the topography. E.~pl B~in Rrs. 21. 159-179. Albus K. (1975b) .4 quantitative study of the proJection area of the central and paracentral visual field in area 17 of the cat. II. The spatial organization of the orientation domain. Espl Lhin Ra. 24, 151-202. Bishop P. 0.. Coombs J. S. and Henr)- G. H. (1971) Response to visual contours: spatio-temporal aspects of excitation in the receptive fields of simple striate neurons. J. PhIsiol.. Lotk 219. 625-657. Bishoo P. 0.. Coombs J. S. and Henry G. H. (19731 Receotive fields of simple cells in the ‘cat striate Physid.. Lontl. 231, 3 I-60.

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%Iaffei L. and Fiorentini .A. (1977) Spatial frequency rows in the striate visual cortex. Vision Rrs. 17. 257-264. Movshon J. A. (19751 The velocity tuning of single units in cat striate cortex. J. Ph.tsiol.. Land. 219. UC468. Nelson J. 1. and Frost B. J. (1978) Orientation-selective inhibition from beyond the classic receptive tield. Bmin Res. 139, 359-365. Palmer L. A. and Rosenquist A. C. I 1974) Visual receptive fields of single striate cortical units projecting to the superior colliculus in the cat. Brain Rex 67. 27-42. Pettigrew J. D., Nikara T. and Bishop P. 0. 11968) Responses to moving slits by single units in cat striate cortex. Espl Bruin Rrs. 6, 373-390. Rose D. (1974) The hypercomplex cell classilication in the cat’s striate cortex. J. PhJsiol.. Lund. 242. 123-l25P. Rose D. (1977) Responses of single units in cat v-isual cortex to moving bars of light as a function of bar length. J. Ph.rsiol.. Lo&. 271. l-23. Rose D. (1978) Functional interactions in the visual cortex Ph.D. thesis. University of Cambridge. Rose D. and Blakemore C. 1197-ta) Effects of bicuculline on functions of inhibition in visual cortex. Surnrr. Lomb. 249. 375-377. 869. Rose D. and Blakemore C. (1971b) An analysis of orientation selectivity in the cat‘s visual cortex. Ezp[ Brclirt Rrs. 20. l-17. Rowe M. H. and Stone J. (1977) Naming of ncurones. Classification and namine of cat retinal ganglion cells. Brain Brhur. Ecol. 11. 183-216. Sanderson K. J. (1971) Visual projection columns and magnification factors in the lateral geniculate nucleus of the cat. Expl Brain Res. 13. 159-177. Sherman S. M.. Watkins D. W. and Wilson J. R. (1976) Further differences in receptive field properties of simple and complex cells in cat striate cortex. Vision Res. 16. 919927. Sillito A. M. (19758) The effectiveness of bicuculline as an antagonist of GABA and vtsually evoked inhibition in the cat’s striate cortex. J. Ph.rsio/.. Lord. 250. 387-304. Sillito A. M (1975b) The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat. J. Ph.rsiol.. Loci. 250. 305-329. Stllito A. IM. (1977a) Inhibitory processes underlying the directional specificity of simple. complex and hypercomplex cells in the cat’s visual cortex. J. Pl~~siol.. Land. 271, 699-720. Sillito A. M. (1977b1 The spatial extent of excitatory and inhibitory zones in the receptive field of superficial layer hypercomplex cells. J. Ph.rsio/.. Lontl. 273, 791-803. Sillito A. M. and Versiani V. (1977) The contribution of excitatory and inhibitory inputs to the length preference of hypercomplex cells in layers II and III of the cat’s striate cortex. J. Phrsiol.. Lond. 273, 775-790. Singer W. and Creutzfeldt 0. D. (1970) Reciprocal lateral inhibition of on- and off-center neurons in the lateral geniculate body of the cat. E.xnl Brain Res. 10, 31 l-330. Singer W. and Lux H. D. (1975) Extracellular potassium gradients and visual receptive fields in the cat striate cortex. Brain Res. 96, 378-383. Singer W.. Pijppel E. and Creutzfeldt 0. (1973) Inhibitory interaction in the cat’s lateral geniculate nucleus. E.xpl Brain Res. 14, 210-226. Singer W.. Tretter F. and Cynader M. (1975) Organization of cat striate cortex: a correlation of receptive-field properties with afferent and efferent connections. J. Neuropltrsiol. 38, 1080-1098. Stone J. and Dreher B. (1973) Projection of X- and Y-cells of the cat’s lateral geniculate nucleus to areas 17 and 18 of visual cortex. J. Neurophysiol. 36, jjl-567. Szentagothai J. (19731 Synaptology of the visual cortex. In Handbook of Sensory Physiology (edited by Jung, R.t. Vol. VI1,3, part B. pp. 269-324. Springer. Berlin.

DAVID ROSE

‘4-l

Tobama K.. Maekawa K. and Takeda T. t 19731 .An anal>5iS of neuronal circuirr) for two types of visual cortical neuroncs classified on the basis of their responses to photic stimuli. Bruin Rts 61. 3Y5-3YY. fokama K.. Vatsunami Ii.. Ohno T. and fokashiki S. 1197-t) An intr~~ilulsr stud) of neuronal organization in the visual cortex. E.Ypl Bruin Rus. 21. 15-66. Tyner C. F. (19751 The naming of neurons: applications of taxonomic theory fo the study of cellular populations. Bruin B&r. Erui. 11. 75-96. Wilson J. R. and Sherman S. M. (19761 Receptive field characteristics of neurons in cat striate cortex: changes with visual field eccentricity. J. Xrttroph~siol. 39. 512-533. Wilson P. D.. Rowe M. H. and Stone J. (19761 Properties of relay cells in cat’s lateral geniculatr nucleus: a comparison of %‘-cells with Y- and Y-cells. J. .Vertrophmiol. 39, 1193-109. APPE%DIX

Only moving bars at the opritnd orirnmion ior the cortical cell are considered. The profile of a receprire field along the fine of such a bar retltcts the responsiveness of the cell to a stimulus moving (perpendicularly to the bar) across the corresponding part of the receptive field. so that the response of the ceil to a bar depends on the arm under the relevant part of the receptive field profile. Thus the response of a cell is assumed to be independent of the receptive field width and dependent only on the lengrhs of the bar and the field. (The width of a cortical discharge field as estimated from the PSTH is only weakly related to the response ma@tude-own unpublished results). Two types of prohle for LGN receptive fields have been generated. The tirst assumes that the centre and the surround each have Gaussian profiles, taken through the exact mid-point of the field. (It is assumed that each mechanism is either excitatory or inhibitory. e.g. the LGN centre mechanism is excitatory and any centre-inhibition in the LGN merely acts to attenuate the centre-excitation without altering the shape of its profile.) The standard de-

b~:ion of the surround 1s three times that of the centre. and the surround is subtracted linearly from the centrc. The centre has simply been given the iorm ~‘(sI = exp I -.r’t. where .Y is the distance from the mid-point of the field. and the surround is therefore K.rxp I -_I: 91.uhers .k is LIconstant. The integral of exp 1 -.Y’) from .Y = - x to - i. is , z: uhen R = 1 6, the integral across ths whole LGS receptive field profile becomes i, n. and when K = 1 4. f, x. These forms of the receptive field profile are shown in Fig. 3A and 3. The second type of LGN protile assumes that the surround as well as the centre is driven directly and independently bq retinal ganglion cells (Singer and Creutzfeldt. 1970: Maffei and Fiorzntini. 192: Hammond. 1973). The retinal inputs have been taken to have profiies similar to that described above for LGN cells with K = 1’6 (Fig. 3A) so the drive to the LGS centre has the form exp( --?(‘I - II 6\.cup ( -.Y’ 9). uhile that -L.[expt-ts 1. c)‘) - (I 6l.exp to the surround is I--,X L c1’~9,3. where t and c are constants. Setting L = i 4 snd assuming that the LGN Reid profile IS derived from the retinal input to the centre plus two inputs to the surround (one on each side of the centre). then the integral across the whole field is no* $, :: (Fig. ~DI. The constant c determines the offset of the inputs to ths surround from that to the centre. and was set to ~3 i 2. i.c. 3 times the standard deviation of exp (--1’). QuAtatibelv similar results were obtained using c = 2 \ 1 or 4 ..I!.) The resultant LGN profile is shown in Fig. 3C. The integrals from the centrs of the tizld outward iin both directions simultaneousiy) are shown in Fig. 30 for each of the three profiles in Fig. 3&C. (Again, linearit> is assumed in the Integration process.) Using each profile in Fig. 3A-C in turn. 5 LGN prdtiles were generated for each test and these aere offset from one another by D = n.\ 2. where n = 0. 1. 2. 3... Ifig. 441. The linear sum g(x) of the 5 waveforms {Fig. 421 was then integrated from I = 0 outwards in both directtons. Thus the plots in Fig. 5 show the integral from .Y = -..y’ to x = +.Y’ as a function of I’. Panels ‘4-C in Fig. 5 use the corr~ponding LGN profiles shoun In Fig. 3.4-C. and the four curves on each panel correspond to offsets ID in Fie. 4) of n,‘\ 2 with n = 0. I. Z and 3. These curves (Fig. -5) are the simulated cortical length tuning curves.