A Neural Locus for Spatial-Frequency Specific Saccadic Suppression in Visual-Motor Neurons of the Primate Superior Colliculus

J Neurophysiol. 2017 Apr 1;117(4):1657-1673. doi: 10.1152/jn.00911.2016. Epub 2017 Jan 18.

Abstract

Saccades cause rapid retinal-image shifts that go perceptually unnoticed several times per second. The mechanisms for saccadic suppression have been controversial, in part because of sparse understanding of neural substrates. In this study we uncovered an unexpectedly specific neural locus for spatial frequency-specific saccadic suppression in the superior colliculus (SC). We first developed a sensitive behavioral measure of suppression in two macaque monkeys, demonstrating selectivity to low spatial frequencies similar to that observed in earlier behavioral studies. We then investigated visual responses in either purely visual SC neurons or anatomically deeper visual motor neurons, which are also involved in saccade generation commands. Surprisingly, visual motor neurons showed the strongest visual suppression, and the suppression was dependent on spatial frequency, as in behavior. Most importantly, suppression selectivity for spatial frequency in visual motor neurons was highly predictive of behavioral suppression effects in each individual animal, with our recorded population explaining up to ~74% of behavioral variance even on completely different experimental sessions. Visual SC neurons had mild suppression, which was unselective for spatial frequency and thus only explained up to ~48% of behavioral variance. In terms of spatial frequency-specific saccadic suppression, our results run contrary to predictions that may be associated with a hypothesized SC saccadic suppression mechanism, in which a motor command in the visual motor and motor neurons is first relayed to the more superficial purely visual neurons, to suppress them and to then potentially be fed back to cortex. Instead, an extraretinal modulatory signal mediating spatial-frequency-specific suppression may already be established in visual motor neurons.NEW & NOTEWORTHY Saccades, which repeatedly realign the line of sight, introduce spurious signals in retinal images that normally go unnoticed. In part, this happens because of perisaccadic suppression of visual sensitivity, which is known to depend on spatial frequency. We discovered that a specific subtype of superior colliculus (SC) neurons demonstrates spatial-frequency-dependent suppression. Curiously, it is the neurons that help mediate the saccadic command itself that exhibit such suppression, and not the purely visual ones.

Keywords: microsaccades; perceptual stability; saccades; saccadic suppression; superior colliculus.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / physiology
  • Animals
  • Evoked Potentials / physiology
  • Macaca mulatta
  • Male
  • Neural Inhibition / physiology*
  • Neurons / classification
  • Neurons / physiology*
  • Photic Stimulation
  • Reaction Time / physiology
  • Saccades / physiology*
  • Statistics as Topic
  • Statistics, Nonparametric
  • Superior Colliculi / cytology*
  • Superior Colliculi / physiology*
  • Time Factors
  • Visual Perception / physiology*