Circuits and Mechanisms for Surround Modulation in Visual Cortex

Abstract

Surround modulation (SM) is a fundamental property of sensory neurons in many species and sensory modalities. SM is the ability of stimuli in the surround of a neuron’s receptive field (RF) to modulate (typically suppress) the neuron’s response to stimuli simultaneously presented inside the RF, a property thought to underlie optimal coding of sensory information and important perceptual functions. Understanding the circuit and mechanisms for SM can reveal fundamental principles of computations in sensory cortices, from mouse to human. Current debate is centered over whether feedforward or intracortical circuits generate SM, and whether this results from increased inhibition or reduced excitation. Here we present a working hypothesis, based on theoretical and experimental evidence, that SM results from feedforward, horizontal, and feedback interactions with local recurrent connections, via synaptic mechanisms involving both increased inhibition and reduced recurrent excitation. In particular, strong and balanced recurrent excitatory and inhibitory circuits play a crucial role in the computation of SM.

Distinct spatiotemporal mechanisms underlie extra-classical receptive field modulation in macaque V1 microcircuits

“…Layer 2/3 suppression peaked at times quite delayed compared to facilitation. Both the orientation selectivity and delayed emergence of this tuned suppression are consistent with it arising as a result of cortico-cortical lateral interactions, as often postulated before (reviewed in Angelucci et al, 2017). We found that this suppressive component arises from extended spatial scales, with most of it generated by the activity of V1 neurons with receptive fields more than 2 x CRF radius away from the recorded neuron.…”

“…Long-distance V1 lateral connections must be in some way selective for the orientation of their targets in order to support such long-range tuned suppression. If instead this suppression is caused in part by extra-striate feedback (Angelucci et al, 2002(Angelucci et al, , 2017Nassi et al, 2013), then those feedback circuits must also be matched in orientation selectivity to their V1 targets. Tuned suppression is also present in layer 4B but it differs quantitatively from that of layers 2/3.…”

“…Many issues about the eCRF mechanisms and their computations are unresolved. There is considerable debate to what extent the eCRF produces facilitation or suppression (Angelucci et al, 2017) and thus whether it involves feature integration or differentiation. Furthermore, it remains unclear whether eCRF modulation arises from a single or multiple mechanisms.…”

Weaker neural suppression in autism

“…To assess suppressive modulatory mechanisms in humans with ASD, we measured visual spatial suppression, a phenomenon in which larger moving stimuli are more difficult to perceive 28 . This mirrors a well-known neural phenomenon; when stimuli extend beyond a neuron's spatial receptive field, neural responses in visual cortex are suppressed through a combination of feed-forward, lateral, and feedback interactions 18,19,29 . Based on work in both humans 1,30,31 and non-human primates [32][33][34][35] , it is thought that neural surround suppression within the motion-selective visual area MT plays an important role in the perceptual phenomenon of spatial suppression during motion discrimination.…”

“…This alternative account predicts that weaker suppression in ASD may not be widespread and would manifest only under specific circumstances. For example, in the visual system, suppressive modulatory mechanisms are engaged when a stimulus extends beyond the spatial receptive field of a given neuron 18,19 . Although it has been suggested that suppressive visual surround modulation reflects neural inhibition 20 , work from our group and others has recently called this assumption into question 1,21,22 .…”