The binocular organization of simple cells in the cat's visual cortex

We have studied the manner by which inputs from the two eyes are combined in simple cells of the cat's visual cortex. The stimuli for this study are drifting sinusoidal gratings, shown dichoptically at optimal spatial frequency and orientation. The relative spatial phase (disparity) between the gratings for left and right eyes is varied over 360 degrees. Most simple cells show phase-specific binocular interaction such that response amplitudes and phases vary depending on the relative spatial phase. At one phase, response is greater than either of the monocular responses and often greater than the sum of the two. At the phase 180 degrees away from the optimal, the cell's responses are strongly inhibited and often completely suppressed. Phase-specific binocular interaction disappears when the gratings presented to one eye are made orthogonal to the optimal orientation. The degree of binocular interaction does not depend critically on the ocular dominance of the cells. Simple cells that are nearly equally dominated by each eye always exhibit strong phase-specific interaction. The majority of cells that are strongly dominated by one eye, and even those that appear monocular, show phase-dependent changes in responses. We examined the extent of binocular interaction for cells with preferred orientations near vertical compared with those tuned to other optimal orientations. If these cells are conveying information about depth, one might expect a greater degree of binocular phase-specificity for units preferring nearly vertical orientations, which would then be processing horizontal disparities. We find no evidence for this. Predictions of simple-cell responses are derived from a linear model of binocular convergence in which light-evoked neural signals from each eye are summed linearly to determine cell responses. Data from cells generally follow the prediction of the model for both response amplitude and phase. Deviations from predictions of the linear model are found for a minority of cells. This deviation may be accounted for by a threshold mechanism that comes into play after the linear binocular summation. A small proportion of simple cells that appear monocular by alternate tests of each eye show a purely inhibitory influence from the silent eye. This inhibition is not generally dependent on the relative phase of the gratings. We conclude that most binocular interaction in striate simple cells may be accounted for by linear summation of neural signals from each eye.(ABSTRACT TRUNCATED AT 400 WORDS)     

Stimulus specificity of binocular cells in the cat's visual cortex: ocular dominance and the matching of left and right eyes

Summary Most cells in the striate cortex respond to visual stimulation through either eye. We have examined quantitatively the matching of response specificity for the two eyes. Our intention was to determine the degree to which this matching depends on ocular dominance. We used standard single cell recording techniques and studied responses to sinusoidal gratings of different spatial frequencies, orientations, and contrasts. For all tests, stimuli were randomly interleaved both with respect to the value of each parameter, and the eye which was stimulated. After estimating ocular dominance qualitatively and quantitatively, we measured: response modulation (to help identify whether a cell was simple or complex), orientation and spatial frequency tuning, and contrast response functions (to estimate contrast thresholds). Results show that: (1) Response modulation is well matched between the two eyes, but there is a slight tendency for the dominant eye to respond with less modulation. (2) Optimal orientation and spatial frequency and their respective tuning widths were similar for the two eyes. In general, tuning functions for the two eyes differed mainly in slope. However, in each case, there was a tendency for the dominant eye to have broader tuning widths. (3) In most cases, contrast response functions for the two eyes differed mainly in their slopes. Extrapolation to spontaneous levels suggests that estimated contrast thresholds are relatively independent of ocular dominance although, again, there was a tendency for the dominant eye to exhibit slightly lower estimated thresholds. These findings demonstrate that response characteristics between the two eyes are generally well matched regardless of relative response strength. There are, however, small but clear differences between the two eyes for all parameters we measured which are related to and demonstrate that ocular dominance influences the degree of matching between the two eyes.     

Functional organization in the cat's pulvinar complex

Summary The responses of 192 single units in the cat's pulvinar-complex, comprising the inferior, medial and lateral pulvinar nuclei, were studied in paralysed cats, lightly anaesthetized with N₂O/O₂ supplemented with pentobarbitone. About 60% of the cells were visually driven and their receptive fields classified as either diffuse, concentric, movement sensitive, direction sensitive or orientation sensitive. The response fields of such cells were commonly large. Response field maps for the movement and direction sensitive cells formed a heterogenous population with uniform on-off fields to more complex arrangements with on- or off-centres, often with only partial surrounds; other cells responded exclusively to moving stimuli.A dual representation of the visual field was found in the pulvinar-complex corresponding to the striate and tectal recipient zones described anatomically by others. The representation in the striate recipient zone comprised an oblique column running medio-laterally and rostrocaudally through the inferior pulvinar and lateral margin of the medial pulvinar. The peripheral visual field was represented laterally and the vertical meridian medially; the upper visual field was represented dorso-laterally in the medial pulvinar and the lower visual field caudo-ventrally within the inferior pulvinar. That this visuotopic organization corresponded to the striate recipient zone was established by tracing the retrograde transport of HRP. Medial to the striate zone evidence for a second visual field representation was found, apparently more randomly organized than the striate zone, corresponding to the presumed tectal recipient zone. These results support the assertion that cytoarchitectural boundaries do not necessarily delineate functional (visuotopically organized) regions. These observations suggest caution when comparing cytoarchitecturally defined regions between species; rather, functionally equivalent regions should be compared.Formerly the Research Department of Communication     

Internal spatial organization of receptive fields of complex cells in the early visual cortex

The receptive fields of complex cells in the early visual cortex are economically modeled by combining outputs of a quadrature pair of linear filters. For actual complex cells, such a minimal model may be insufficient because many more simple cells are thought to make up a complex cell receptive field. To examine the minimalist model physiologically, we analyzed spatial relationships between the internal structure (subunits) and the overall receptive fields of individual complex cells by a two-stimulus interaction technique. The receptive fields of complex cells are more circular and only slightly larger than their subunits in size. In addition, complex cell subunits occupy spatial extents similar to those of simple cell receptive fields. Therefore in these respects, the minimalist schema is a fair approximation to actual complex cells. However, there are violations against the minimal model. Simple cell receptive fields have significantly fewer subregions than complex cell subunits and, in general, simple cell receptive fields are elongated more horizontally than vertically. This bias is absent in complex cell subunits and receptive fields. Thus simple cells cannot be equated to individual complex cell subunits and spatial pooling of simple cells may occur anisotropically to constitute a complex cell subunit. Moreover, when linear filters for complex cell subunits are examined separately for bright and dark responses, there are significant imbalances and position displacements between them. This suggests that actual complex cell receptive fields are constructed by a richer combination of linear filters than proposed by the minimalist model.     

Inhibitory processes underlying the directional specificity of simple, complex and hypercomplex cells in the cat's visual cortex

1. The iontophoretic application of bicuculline, an antagonist of GABA, the putative inhibitory transmitter in the visual cortex, has been used to examine the contribution of post-synaptic inhibitory processes to the directional selectivity of simple, complex and hypercomplex cells in the cat's striate cortex.

2. The directional selectivity of simple cells was significantly reduced or eliminated during the iontophoretic application of bicuculline. This supports the view that the selectivity is derived from the action of a GABA-mediated post-synaptic inhibitory input modifying their response to a non-directionally specific excitatory input.

3. Complex cells were subdivided into three categories on the basis of the action of iontophoretically applied bicuculline on their directional selectivity, receptive field characteristics and distribution in terms of cortical layer. They are referred to as type `1', `2' and `3' complex cells.

4. The directional specificity of type `1' complex cells was eliminated during the iontophoretic application of bicuculline. It seems likely, therefore, that they receive a non-directionally specific excitatory input and that, as for simple cells, the directional specificity derives from the action of a GABA-mediated post-synaptic inhibitory input. No type `1' complex cells were recorded below layer IV.

5. The directional specificity of type `2' complex cells was unaffected by the iontophoretic application of bicuculline, despite increases in response magnitude, a block of the action of iontophoretically applied GABA and, in some cases, changes in other receptive field properties. It is suggested that these cells receive a directionally specific excitatory input. The type `2' complex cells were found both superficial and deep to layer IV with the majority in layer V.

6. Type `3' complex cells appear to have very similar receptive field properties to those of the cells described by other workers as projecting to the superior colliculus. They were found predominantly in layer V. Their directional specificity was not eliminated by the iontophoretic application of bicuculline. However, they exhibited a powerful suppression of the resting discharge in response to stimulus motion in the non-preferred direction. Iontophoretic application of ammonium ions revealed a small excitatory response in place of the suppression. It appears from these observations that the directional specificity of the type `3' complex cells could be determined, at least in part, by an inhibitory process which is not GABA-mediated.

7. The directional specificity of hypercomplex cells found in layers II and III was unaffected by the iontophoretic application of bicuculline, and they showed no suppression of their background discharge level in response to stimulus motion in the non-preferred direction. This evidence is consistent with the view that they receive a directionally specific excitatory input.

     

Localization of NPY-immunoreactivity in the cat's visual cortex

Summary Using a polyclonal antiserum against neuropeptide Y (NPY; J.M. Allen et al. 1983a) immunohistochemistry was carried out using the PAP method. Neurones displaying NPY-like immunoreactivity are seen mainly in cortical layers V/ VI, adjacent white matter and corona radiata. Only few neurones occur in superficial layers II/III. Neurones are multipolar to bitufted with spineless dendrites; somata are either round (layers V, II/III) or spindle-like (layer VI, white matter) with diameters between 16 and 20 m. Axones were identified by their initial smoother profiles, which are smaller in diameter than principal dendrites, by their typical branching pattern and the occurrence of terminal portions. It was found, that the degree of axonal ramification in proximal parts of axones is rather poor. Most NPY-neurones seem to project intracortically or even locally, except neurones in layers VI and the white matter. The latter neurones have ascending axonal branches terminating in layer VI and V, thus contributing to the dense NPY-plexus in these layers, whereas some layer VI neurones have axonal branches descending into the white matter. The axonal plexus in upper cortical layers is most probably fed by the ascending axones of layer V neurones, passing layer IVc in a strictly vertical direction. Fine smooth fibers of unknown origin which ascend from the white matter in a vertical direction through the grey matter also contribute to the plexus in layer II/III. In semithin sectioned material three terminal types were identified. Firstly, en passant boutons on immunnegative pyramidal neurones, secondly, perisomatically arranged, basket-like terminals, bending around unstained non-pyramidal neurones, and thirdly, about 60 m long vertically oriented rows of boutons exclusively on apical dendrites of layer II/III pyramidal neurones. Due to the unconspicious axonal pattern and the frequently observed basket-like terminal form, we conclude that most NPY-ir neurones can be regarded as a class of unspecific local field basket cells; the origin of the vertically arranged bouton rows has been yet to determined.     

The representation of three-dimensional visual space in the cat's striate cortex

1. Binocularly driven single units were recorded in the cat's striate cortex. For each neurone the two monocular receptive fields were stimulated simultaneously in order to assess the optimal positioning of the image in both eyes to give the best binocular response.2. The electrode was driven perpendicular to the surface of the brain to explore cortical columns, all the cells of which are known to have the same preferred target orientation.3. All orientation columns were found to fit into one of two classes according to their binocular organization.4. In a constant depth column the receptive fields of binocular neurones cover a small retinal area and they are laid out in almost identical arrays in the two eyes. Consequently, the horizontal disparity is practically the same for all the units. The depth column as a whole is viewing a thin sheet of visual space, a few degrees wide, floating at some distance from the cat. There may be about 0.6 degrees disparity difference between neighbouring depth columns.5. In a constant direction column the binocular units' fields are all super-imposed on the retina contralateral to the hemisphere containing the column. In the ipsilateral eye they are more scattered horizontally. Therefore the horizontal disparity varies enormously from cell to cell and the column as a whole is viewing a cylinder of visual space directed towards the contralateral eye. Neighbouring direction columns may vary by about 4 degrees in their oculocentric visual direction.6. This columnar arrangement is probably important for space perception in the cat. Activity in only one depth and one direction column would specify the orientation and the three-dimensional locus of an object in space.7. The two types of column may be involved in the control of disjunctive and conjugate eye movements.     

Differential responsiveness of cells in the visual zones of the cat's LP-pulvinar complex to visual stimuli

Summary Multiple visual field representations are contained within the feline LP-pulvinar complex; regions differentiated by their afferent and efferent connectivity patterns as the striate-, tecto- and retino-recipient zones. Cell responses from these visuotopic zones were investigated in immobilized cats under N₂O/O₂ supplemented with pentobarbitone or Althesin, using spot, bar and textured stimuli.Response fields recorded within the LP-pulvinar complex were classified as diffuse, concentric, movement-, direction- or orientation-sensitive. Concentric receptive fields were further classified as sustained (X), transient (Y) or tonic/phasic W-cells. Direction-and movement-sensitive cells predominated in the striate- and tecto-recipient zones, respectively. Motion of noise fields, or noise bars against an identical stationary noise background elicited vigorous responses from cells in the striate zone, many showing a preference for noise stimuli. In contrast, cells from the tectal zone and other divisions of the LP-pulvinar complex were insensitive to noise. The retino-recipient zone at the lateral margin of the pulvinar nucleus was characterized by cells with concentric receptive fields, the majority exhibiting properties similar to W-cells in the LGNd. The evidence supports the notion of functional subdivision within the LP-pulvinar complex corresponding to the visuotopically organized regions defined by their connectivity patterns. Consideration of the retino-recipient zone as an extension of the LGNd-MIN complex is discussed.Supported by the MRC (Grant No. 976/64/N)     

Orientation tuning of cells in areas 17 and 18 of the cat's visual cortex

Summary Sharpness and symmetry of orientation tuning were quantitatively investigated and compared in ninety-seven cells from areas 17 and 18 of the lightly-anaesthetised feline visual cortex.Halfwidths of orientation tuning at half-height ranged between 5 ° and 73 ° for long stimuli, with an extreme exception at 111 ° (excluding untuned cells).There was a tendency for cells in area 18 to be more broadly tuned than those in area 17, due largely to the relatively sharp tuning of area 17 simple cells. Confirming previous work, simple cells were more sharply tuned than complex cells in area 17. In area 18, there was no clear distinction in sharpness of tuning between complex type 1 cells (equated with area 17 simple cells), complex type 2 cells (equated with area 17 complex cells), or hypercomplex cells.Approximately 60% of cells in both areas were asymmetrically tuned for orientation: ratios of half-widths to either side of the optimal orientation ranged from 1.0–3.0, exceptionally 5.8. Asymmetry of tuning was more marked in area 18 than in area 17, except that area 18 complex type 2 cells as a group were relatively symmetrically tuned for orientation.Occasional cells with different preferred orientations for opposite directions of motion, for each peak of a bimodal response to a single direction, or for each half of the receptive field were also observed. The latter are described in the following paper (Hammond and Andrews, 1978b).     

Monocular and binocular response properties of cells in the striate-recipient zone of the cat's lateral posterior-pulvinar complex

1. We have studied response properties of single cells in the striate-recipient zone of the cat's lateral posterior-pulvinar (LP-P) complex. This zone is in the lateral section of the lateral posterior nucleus (LP1). Our purpose was to determine basic response characteristics of these cells and to investigate the possibility that the LP-P complex is a center of integration that is dominated by input from visual cortex. 2. The majority (72%) of cells in the striate-recipient zone respond to drifting sinusoidal gratings with unmodulated discharge. 3. Cells in the LP1 are selective to the orientation of gratings, and tuning functions have a mean bandwidth of 31 degrees. More than one-half of these units are direction-selective. The preferred orientation and the tuning widths for the two eyes are generally well matched. However, a few cells exhibited the interesting property of opposite preferred directions for the two eyes. Orientation tuning for a small group of cells was different for the mean discharge and first harmonic components, suggesting a convergence from different inputs to these cells. 4. Two-thirds of LP1 cells are tuned to low spatial frequencies (less than 0.5 c/deg). The tuning is broad with a mean bandwidth of 2.2 octaves. The remaining one-third of the units are low-pass because they show no attenuation of their responses to low spatial frequencies. Both eyes exhibit the same spatial frequency preference and the same spatial frequency tuning. There is a high correlation between spatial frequency and orientation selectivities. 5. All cells tested are tuned for temporal frequency with a sharp attenuation for low frequencies. The optimal values range between 4 and 8 Hz, and the mean bandwidth is 2.2 octaves. 6. Cells in LP1 are mostly binocular. When monocular, cells are almost always contralaterally driven. Dichoptic presentation of gratings reveals the presence of strong binocular interaction. In almost all cases, these interactions are phase specific. The cell's discharge is facilitated at particular phases and inhibited at phases 180 degrees away. These binocular interactions are orientation dependent. 7. Twenty-five percent of the cells with phase-specific binocular facilitation appear to be monocular when each eye is tested separately. For three cells, we observed a non-phase-specific inhibitory effect of the silent eye. 8. Our findings indicate that LP1 cells form a relatively homogeneous group, suggesting a high degree of integration of multiple cortical inputs.(ABSTRACT TRUNCATED AT 400 WORDS)