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

Christopher A Henry,Michael J Hawken,Robert M Shapley,Mehrdad Jazayeri

doi:10.7554/elife.54264

Abstract

Complex scene perception depends upon the interaction between signals from the classical receptive field (CRF) and the extra-classical receptive field (eCRF) in primary visual cortex (V1) neurons. Although much is known about V1 eCRF properties, we do not yet know how the underlying mechanisms map onto the cortical microcircuit. We probed the spatio-temporal dynamics of eCRF modulation using a reverse correlation paradigm, and found three principal eCRF mechanisms: tuned-facilitation, untuned-suppression, and tuned-suppression. Each mechanism had a distinct timing and spatial profile. Laminar analysis showed that the timing, orientation-tuning, and strength of eCRF mechanisms had distinct signatures within magnocellular and parvocellular processing streams in the V1 microcircuit. The existence of multiple eCRF mechanisms provides new insights into how V1 responds to spatial context. Modeling revealed that the differences in timing and scale of these mechanisms predicted distinct patterns of net modulation, reconciling many previous disparate physiological and psychophysical findings.

Highlights

Object vision relies on integrating and differentiating local image features to form a representation of the visual input
The results describe the components of extra-classical receptive field (eCRF) modulation across the population and how response dynamics varied with neurons' laminar locations
Neurons in different cortical laminae had distinct patterns of eCRF modulation that partially segregated with input layer processing streams, and were elaborated along distinct corticocortical output pathways

Summary

Introduction

Object vision relies on integrating and differentiating local image features to form a representation of the visual input. There is considerable debate to what extent the eCRF produces facilitation or suppression (Angelucci et al, 2017) – and whether it involves feature integration or differentiation. It remains unclear whether eCRF modulation arises from a single or multiple mechanisms. The extent to which the eCRF mechanisms are inherited or emerge via computations within the cortical microcircuit is unclear. How eCRF properties differ across the laminar architecture in V1 may strongly impact how context information is relayed along distinct cortical output pathways

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Conclusion