We investigated the spatial organization of surround suppression in primate primary visual cortex (V1). We utilized drifting stimuli, configured to extend either from within the classical receptive field (CRF) to surrounding visual space, or from surrounding visual space into the CRF or subdivided to generate direction contrast, to make a detailed examination of the strength, spatial organization, direction dependence, mechanisms, and laminar distribution of surround suppression. Most cells (99/105, 94%) through all cortical layers, exhibited suppression (mean reduction 67%) to uniform stimuli exceeding the CRF, and 43% exhibited a more than 70% reduction. Testing with an annulus revealed two different patterns of surround influence. Some cells (37% of cells), classical surround suppression (CSS) cells exhibited responses to an annulus encroaching on the CRF that were less than the plateau in the spatial summation curve. The majority (63%), center-gated surround suppression (CGSS) cells, showed responses to annuli that equaled or exceeded the plateau in the spatial summation curve. Analysis suggested the CSS mechanism was implemented in all cells while the CGSS mechanism was implemented in varying strength across the sample with the extreme reflected in cells that gave larger responses to annuli than to a center stimulus. Reversing the direction of motion of the portion of the stimulus surrounding the CRF revealed four different patterns of effect: no reduction in the degree of suppression (22% of cells), a reduction in surround suppression (41%), a facilitation of the response above the level to the inner stimulus alone (37%), and a facilitation of the response above that to the inner stimulus alone that also exceeded the values associated with an optimal inner stimulus. The facilitatory effects were only seen for reverse direction interfaces between the central and surrounding stimulus at diameters equal to or more than the CRF size. The zones driving the suppressive influences and the direction contrast facilitation were often spatially heterogeneous and for a number of cells bore strong comparison with the class of behavior reported for surround mechanisms in MT. This suggests a potential role, for example, in extracting information about motion contrast in the representation of the three dimensional structure of moving objects.

We have examined the responses of 141 layer VI cells in the feline visual cortex. Within this group we compared the responses of a subpopulation of cells checked for connectivity by electrical stimulation in the dLGN and the visual claustrum. The antidromically identified corticogeniculate projecting cells had relatively short receptive fields, as judged from length response curves, measured quantitatively, and were located at the “short” end of the receptive field length spectrum seen in the general population. Of the 17 corticogeniculate projecting cells, 71% were S type cells, which were typically monocular and directionally selective, with relatively long latencies following electrical stimulation. The remaining 29% were C type cells, also directionally selective, but with a wider spread of ocular dominance preferences and shorter latencies following electrical stimulation. S and C type subpopulations did not differ in their receptive field lengths. The mean receptive field length for this subpopulation was 2.2 degrees +/- 0.27, the shortest field being 1 degrees and the longest 5 degrees. The five layer VI cells activated by electrical stimulation from electrodes within the dorsocaudal (visual) claustrum all had much longer receptive field lengths than the corticogeniculate population, often 10 degrees or longer and were monocular and directionally selective S type cells. These data indicate that the information carried in the corticogeniculate stream (and that from layer VI directly to layer IV carried by axon collaterals) is relatively tightly focused in spatial terms whilst the less spatially focused, long receptive field output from layer VI projects to the claustrum.

These experiments examine the effect of blockade of layer VI of the cat striate cortex on the length tuning of hypercomplex cells in the overlying layers II, III and IV. It has previously been suggested that local inactivation of layer VI results in the complete loss of length selectivity in all hypercomplex cells in layers II, III and IV above the blocked region, by removal of an inhibitory mechanism within layer IV, driven from layer VI. However, we have found that, using iontophoretic application of the inhibitory substance GABA to block the activity of layer VI, 29% of hypercomplex cells were unaffected by blockade of the underlying layer VI. The predominant effect on hypercomplex cells was a reduction in visual responsiveness, seen in 71% of cells, with responses reduced on average by 43%. In 50% of these cells (35% of the population) this reduction was apparently specific to responses to the optimum bar length; responses to longer stimuli were unaffected. Iontophoretic application of the potent GABAA analogue muscimol in layer VI showed a similar spectrum of effects on hypercomplex cells. In these cases, however, the cortical blockade was slowly increased to encompass the recorded cell. In each case, any decreases in length selectivity were also the result of a decreased visual responsiveness. Thus, decreases in length selectivity seen when using either GABA or muscimol were almost exclusively the result of decreased responsiveness to the optimal length of bar stimulus, rather than an increase in response to non-optimal, long stimuli. This suggests the loss of a facilitatory influence from layer VI to layer IV, rather than the loss of inhibition.

Layer VI of the visual cortex has been considered to be dominated by cells with very long receptive fields, typically summing to 8 degrees or more. We have re-examined this issue in a series of experiments in which the length tuning profiles of layer VI cells in the cat visual cortex have been quantitatively determined. Responses were assessed to optimally oriented bars of light of varying length drifted over the receptive field. The lengths were varied on a randomised interleaved sequence. Although our data confirm the presence of long field cells in layer VI, only 24% of a population of 119 cells had fields greater than 6 degrees in length. Fields greater than 8 degrees were only seen in 17% of cells. 61% of the population of cells had fields showing summation to 4 degrees or less with a mean length of 2.8 degrees (+/-0.15 sem). In this "short field" group, 18% had fields of 1 degrees or less. We observed 7 cells with rapid initial spatial summation up to 1 degree, followed by clear end zone inhibition. It has been recently suggested on the basis of localised inactivation experiments, that layer VI cells with long (greater than 8 degrees) fields may provide the drive to inhibitory interneurones in layer IV generating hypercomplex cell end zone inhibition. This observation is difficult to equate with evidence indicating that hypercomplex cell end zone inhibition reflects a mechanism showing maximal summation at lengths in the region of 2.8 degrees.(ABSTRACT TRUNCATED AT 250 WORDS)

1. Vasoactive intestinal polypeptide (VIP) was iontophoretically applied to a population of 90 single cells in the primary visual cortex (area 17) of the cat. Response magnitude, response selectivity, spontaneous activity, and the ratio between the visual response and spontaneous activity (signal-to-noise ratio) of the cells were assessed quantitatively before and during drug application. 2. VIP had little effect in the absence of visual stimulation, with only 29/90 (32%) of the cells showing a change of even 1 sp/s in their spontaneous activity. In contrast it had a clear effect on the visual responses of the majority (73/90, 81%) of the cells tested. 3. VIP produced a substantial change (i.e., > or = 40%) in optimal response magnitude for 57 of the affected cells. Of these 65% were facilitated, usually with no change or an improvement in signal-to-noise ratio and direction selectivity. The remaining cells were inhibited, with more variable effects on their visual response characteristics, and were found predominantly in the superficial laminae. 4. The effects of VIP bore a remarkable resemblance to those reported previously for the muscarinic action of acetylcholine (ACh). VIP and a muscarinic cholinergic agonist, either ACh or acetyl-beta-methacholine (MeCh), were therefore applied in turn to a group of 40 cells. In 23 cases VIP and the muscarinic agonist were also applied simultaneously. 5. The effects of VIP and the cholinergic agonist matched in 92% of the cases where both drugs were effective. That is to say, cells that were facilitated by VIP were facilitated also by ACh or MeCh, and vice versa. In many instances there was a clear similarity in the pattern as well as the direction of the effects produced by the two substances. The result of simultaneous application was generally additive. 6. These data suggest that VIP and ACh activate very similar postsynaptic mechanisms, and share a closely related function at the level of individual cortical cells. Thus VIP may facilitate the responses of both the excitatory and the inhibitory components of the cortical circuit, leading to an overall increase in responsiveness and selectivity. In contrast to the cholinergic input from the basal forebrain, however, the VIP-positive cortical cells are likely to exert a very localized influence, over a circumscribed region of the cortex, in response to the presence of an effective visual stimulus.