Top-down feedback controls spatial summation and response amplitude in primate visual cortex

Lauri Nurminen,Maryam Bijanzadeh,Alessandra Angelucci,Frederick Federer,Sam Merlin

doi:10.1038/s41467-018-04500-5

Abstract

Sensory information travels along feedforward connections through a hierarchy of cortical areas, which, in turn, send feedback connections to lower-order areas. Feedback has been implicated in attention, expectation, and sensory context, but the mechanisms underlying these diverse feedback functions are unknown. Using specific optogenetic inactivation of feedback connections from the secondary visual area (V2), we show how feedback affects neural responses in the primate primary visual cortex (V1). Reducing feedback activity increases V1 cells’ receptive field (RF) size, decreases their responses to stimuli confined to the RF, and increases their responses to stimuli extending into the proximal surround, therefore reducing surround suppression. Moreover, stronger reduction of V2 feedback activity leads to progressive increase in RF size and decrease in response amplitude, an effect predicted by a recurrent network model. Our results indicate that feedback modulates RF size, surround suppression and response amplitude, similar to the modulatory effects of visual spatial attention.

Highlights

Sensory information travels along feedforward connections through a hierarchy of cortical areas, which, in turn, send feedback connections to lower-order areas
Reducing V2 feedback activity increased summation RF (sRF) size, decreased V1 cell’s responses to stimuli confined to their sRF, and increased their responses to stimuli extending into the proximal surround, weakening surround suppression
The magnitude of these effects depended on the degree of feedback inactivation, so that stronger reduction of V2 feedback activity led to greater increase in sRF size and progressive decrease in response amplitude

Summary

Introduction

Sensory information travels along feedforward connections through a hierarchy of cortical areas, which, in turn, send feedback connections to lower-order areas. To determine the cellular mechanisms underlying the influence of cortical feedback on sensory processing, we asked whether inactivating feedback from the secondary visual area (V2) alters RF size, surround suppression and response gain in the primary visual cortex (V1). Surround suppression is the property of V1 neurons to reduce their response to stimuli inside their RF when presented with large stimuli extending into the RF surround[10,11,12,13,14,15,16,17,18] This is a fundamental computation throughout the visual cortex, thought to increase the neurons’ coding efficiency[19,20,21,22], to contribute to segmentation of objects boundaries[21], and to be generated by feedback connections[5,6]. As several forms of top-down influences in sensory processing have been shown to affect neuronal responses in the same way as we have shown here for feedback from V2, our study suggests that feedback connections can support a large variety of top-down effects observed in vivo

Methods

Results

Conclusion