Binocular flash suppression in the primary visual cortex of anesthetized and awake macaques.

Georgios A Keliris,Yusuke Murayama,Hamed Bahmani,Nikos K Logothetis,Samuel G Solomon

doi:10.1371/journal.pone.0107628

Abstract

Primary visual cortex (V1) was implicated as an important candidate for the site of perceptual suppression in numerous psychophysical and imaging studies. However, neurophysiological results in awake monkeys provided evidence for competition mainly between neurons in areas beyond V1. In particular, only a moderate percentage of neurons in V1 were found to modulate in parallel with perception with magnitude substantially smaller than the physical preference of these neurons. It is yet unclear whether these small modulations are rooted from local circuits in V1 or influenced by higher cognitive states. To address this question we recorded multi-unit spiking activity and local field potentials in area V1 of awake and anesthetized macaque monkeys during the paradigm of binocular flash suppression. We found that a small but significant modulation was present in both the anesthetized and awake states during the flash suppression presentation. Furthermore, the relative amplitudes of the perceptual modulations were not significantly different in the two states. We suggest that these early effects of perceptual suppression might occur locally in V1, in prior processing stages or within early visual cortical areas in the absence of top-down feedback from higher cognitive stages that are suppressed under anesthesia.

Highlights

Visual information is processed across a distributed network of interconnected visual areas [1]
Perceptual modulation of multi-unit activity We recorded neural activity from V1 of four macaques being either under general anesthesia (B01 and D01), or awake, passively fixating (D98 and F03). This allows the comparison of neural activity in the anesthetized and awake brains during the binocular flash suppression (BFS) task, which in awake conditions, ensures robust perceptual suppression of a monocular stimulus upon asynchronous presentation of a second stimulus to the other eye
During the dichoptic phase, this difference was significant in only 4 recording sites of one of the animals (B03). These results indicate that perceptual modulations of the lower band of the local field potentials (LFPs) in V1 are essentially absent in anesthetized conditions, similar to the awake passively fixating animals reported previously [37]

Summary

Introduction

Visual information is processed across a distributed network of interconnected visual areas [1]. The use of visual stimuli that induce ambiguous perception has been established as a classical paradigm to identify the neural circuits subserving subjective perception [14,15,16,17,18]. Under these conditions, a single interpretation of the external world cannot be unambiguously achieved. When the brain is presented with such stimuli, typically only one possible interpretation is perceived at a time and after a few seconds the percept switches abruptly to another [18] Such perceptual alternations occur while the sensory input is kept constant, offering a clear dissociation of sensory stimulation and subjective awareness [9,11,14,19,20,21]. Studies using functional magnetic resonance imaging (fMRI) in humans found that V1 is modulated to a large extent by the subjective percept [12,13,38,39,40]

Methods

Results

Conclusion