A circuit for saccadic suppression in the primate brain

J Neurophysiol. 2017 Apr 1;117(4):1720-1735. doi: 10.1152/jn.00679.2016. Epub 2016 Dec 21.

Abstract

Saccades should cause us to see a blur as the eyes sweep across a visual scene. Specific brain mechanisms prevent this by producing suppression during saccades. Neuronal correlates of such suppression were first established in the visual superficial layers of the superior colliculus (SC) and subsequently have been observed in cortical visual areas, including the middle temporal visual area (MT). In this study, we investigated suppression in a recently identified circuit linking visual SC (SCs) to MT through the inferior pulvinar (PI). We examined responses to visual stimuli presented just before saccades to reveal a neuronal correlate of suppression driven by a copy of the saccade command, referred to as a corollary discharge. We found that visual responses were similarly suppressed in SCs, PI, and MT. Within each region, suppression of visual responses occurred with saccades into both visual hemifields, but only in the contralateral hemifield did this suppression consistently begin before the saccade (~100 ms). The consistency of the signal along the circuit led us to hypothesize that the suppression in MT was influenced by input from the SC. We tested this hypothesis in one monkey by inactivating neurons within the SC and found evidence that suppression in MT depends on corollary discharge signals from motor SC (SCi). Combining these results with recent findings in rodents, we propose a complete circuit originating with corollary discharge signals in SCi that produces suppression in visual SCs, PI, and ultimately, MT cortex.NEW & NOTEWORTHY A fundamental puzzle in visual neuroscience is that we frequently make rapid eye movements (saccades) but seldom perceive the visual blur accompanying each movement. We investigated neuronal correlates of this saccadic suppression by recording from and perturbing a recently identified circuit from brainstem to cortex. We found suppression at each stage, with evidence that it was driven by an internally generated signal. We conclude that this circuit contributes to neuronal suppression of visual signals during eye movements.

Keywords: corollary discharge; macaque; suppression.

Publication types

  • Research Support, N.I.H., Intramural

MeSH terms

  • Action Potentials / physiology
  • Animals
  • Brain / cytology*
  • Brain / physiology*
  • Fixation, Ocular
  • Functional Laterality
  • Macaca mulatta
  • Male
  • Movement / physiology
  • Neural Inhibition / physiology*
  • Neurons / physiology*
  • Photic Stimulation
  • Reaction Time / physiology
  • Saccades / physiology*
  • Visual Fields / physiology
  • Visual Pathways / physiology*