Surround modulation is predominantly orientation-unspecific in macaque V1

Abstract

Surround modulation is a fundamental property of V1 neurons, playing critical roles in stimulus integration and segregation. It is believed to be orientation-specific, as neurons’ responses at preferred orientations are suppressed more by iso-oriented surrounds than by cross-oriented surrounds. Here, we investigated an alternative hypothesis that surround modulation is primarily orientation-unspecific, in that the observed “orientation-specific” surround effects actually reflect overall gain changes that affect neurons tuned to all orientations. We employed two-photon calcium imaging to compare V1 population orientation tuning functions under iso- and cross-surround modulation in awake, fixating macaques. While confirming “orientation-specific” surround suppression in individual neurons, our analysis of the population orientation tuning functions revealed that iso-surrounds induce a general orientation-unspecific suppression across all orientation-tuned neurons, plus weak orientation-specific suppression to neurons tuned to the center stimulus orientation. Furthermore, cross-surrounds mainly reduce orientation-unspecific suppression by scaling up responses of all orientation-tuned neurons. These findings suggest a model of population gain control where surround stimuli mostly scale the responses of the neuronal population. Further population coding analyses supported this conclusion, demonstrating that surround suppression leads to degraded target orientation information at least partially due to a reduced number of contributing neurons with diverse orientation preferences.