Rivalry-Like Neural Activity in Primary Visual Cortex in Anesthetized Monkeys

J Neurosci. 2016 Mar 16;36(11):3231-42. doi: 10.1523/JNEUROSCI.3660-15.2016.

Abstract

Two incongruent images viewed by the two eyes cause binocular rivalry, during which observers perceive continuous alternations between these two visual images. Previous studies in both humans and monkeys have shown that the primary visual cortex (V1) plays a critical role in the rivalry perception. However, it is unclear whether the rivalry activity observed in V1 relies on conscious influences. Here, we examine the responses of V1 in monkeys under general anesthesia. With intrinsic signal optical imaging and single-trial analysis, alternating activation of ocular dominance columns in V1 was observed during binocularly incongruent stimulation. Left- and right-eye columns exhibited counterphase activation, which were modulated by stimulus features in ways similar to those found in conscious human observers. These observations indicated that binocular rivalry occurs in V1 without consciousness, suggesting that the low-level automatic mechanisms play a more important role than previously believed in handling visual ambiguities.

Significance statement: When visual input is ambiguous, for example, in viewing bistable images, human subjects normally perceive one of the interpretations at a particular moment. Previous studies have shown that both low-level visual processing and high-level attention contribute to the establishment of the final visual perception. However, it is not clear whether attention is indispensable in such a process. Here we show that rivalry-like neural activity persisted in monkey V1 when the monkeys were anesthetized and viewed binocularly incongruent stimuli. Such activity has many key features similar to those observed in conscious human subjects. These findings indicate that low-level visual processes play a critical role in solving visual ambiguity such as binocular rivalry.

Keywords: anesthetized; attention; binocular rivalry; ocular dominance; optical imaging; striate cortex.

Publication types

  • Research Support, Non-U.S. Gov't
  • Video-Audio Media

MeSH terms

  • Action Potentials / physiology
  • Anesthesia, General
  • Animals
  • Brain Mapping*
  • Dominance, Ocular
  • Macaca fascicularis
  • Macaca mulatta
  • Male
  • Optical Imaging
  • Photic Stimulation
  • Spectrum Analysis
  • Time Factors
  • Vision, Binocular / physiology*
  • Visual Cortex / cytology*
  • Visual Cortex / drug effects
  • Visual Cortex / physiology*
  • Visual Pathways / physiology
  • Visual Perception / physiology*