We can claim that we know what the visual system does once we can predict neural responses to arbitrary stimuli, including those seen in nature. In the early visual system, models based on one or more linear receptive fields hold promise to achieve this goal as long as the models include nonlinear mechanisms that control responsiveness, based on stimulus context and history, and take into account the nonlinearity of spike generation. These linear and nonlinear mechanisms might be the only essential determinants of the response, or alternatively, there may be additional fundamental determinants yet to be identified. Research is progressing with the goals of defining a single "standard model" for each stage of the visual pathway and testing the predictive power of these models on the responses to movies of natural scenes. These predictive models represent, at a given stage of the visual pathway, a compact description of visual computation. They would be an invaluable guide for understanding the underlying biophysical and anatomical mechanisms and relating neural responses to visual perception.

https://www.jneurosci.org/content/jneuro/25/46/10577.full.pdf

Do we know what the early visual system does

A central question in visual neuroscience is what circuits generate the responses of neurons in the primary visual cortex (V1). V1 neurons respond best to oriented stimuli of optimal size within their receptive field (RF) center. This size tuning is contrast dependent, i.e. a neuron's optimal stimulus size measured at high contrast (the high-contrast summation RF, or hsRF) is smaller than when measured using low-contrast stimuli (the low-contrast summation RF, or lsRF). Responses to stimuli in the RF center are usually suppressed by iso-oriented stimuli in the extra-classical RF surround. Iso-orientation surround suppression is fast and long range, extending well beyond the size of V1 cells' lsRF. Geniculocortical feedforward (FF), V1 lateral and extrastriate feedback (FB) connections to V1 could all contribute to generating the RF center and surround of V1 neurons. Studies on the spatio-temporal properties and functional organization of these connections can help disclose their specific contributions to the responses of V1 cells. These studies, reviewed in this chapter, have shown that FF afferents to V1 integrate signals within the hsRF of V1 cells; V1 lateral connections are commensurate with the size of the lsRF and may, thus, underlie contrast-dependent changes in spatial summation, and modulatory effects arising from the surround region closer to the RF center (the "near" surround). The spatial and temporal properties of lateral connections cannot account for the dimensions and onset latency of modulation arising from more distant regions of the surround (the "far" surround). Inter-areal FB connections to V1, instead, are commensurate with the full spatial range of center and surround responses, and show fast conduction velocity consistent with the short onset latency of modulation arising from the "far" surround. We review data showing that a subset of FB connections terminate in a patchy fashion in V1, and show modular and orientation specificity, consistent with their proposed role in orientation-specific center-surround interactions. We propose specific mechanisms by which each connection type contributes to the RF center and surround of V1 neurons, and implement these hypotheses into a recurrent network model. We show physiological data in support of the model's predictions, revealing that modulation from the "far" surround is not always suppressive, but can be facilitatory under specific stimulus conditions.

Contribution of feedforward, lateral and feedback connections to the classical receptive field center and extra-classical receptive field surround of primate V1 neurons

Inhibitory Stabilization of the Cortical Network Underlies Visual Surround Suppression

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.

/pdf/surround-suppression-in-primate-v1-q45batgg81.pdf

Surround suppression in primate V1

Always returning: feedback and sensory processing in visual cortex and thalamus

We have compared the spatial summation characteristics of cells in the primary visual cortex with those of cells in the dorsal lateral geniculate nucleus (LGN) that provide the input to the cortex. We explored the influence of varying the diameter of a patch of grating centred over the receptive field and quantitatively determined the optimal summation diameter and the degree of surround suppression for cells at both levels of the visual system using the same stimulus parameters. The mean optimal summation size for LGN cells (0.90°) was much smaller than that of cortical cells (3.58°). Virtually all LGN cells exhibited strong surround suppression with a mean value of 74%±1.61% SEM for the population as a whole. This potent surround suppression in the cells providing the input to the cortex suggests that cortical cells must integrate their much larger summation fields from the low firing rates associated with the suppression plateau of the LGN cell responses. Our data suggest that the strongest input to cortical cells will arise from geniculate cells representing areas of visual space located at the borders of a visual stimulus. We suggest that analysis of response properties by patterns centred over the receptive fields of cells may give a misleading impression of the process of the representation. Analysis of pattern terminations or salient borders over the receptive field may provide much more insight into the processing algorithms involved in stimulus representation.

Nicola M. Oakely

Papers

Spatial summation in lateral geniculate nucleus and visual cortex.