Dynamic Structure of Neural Variability in the Cortical Representation of Speech Sounds

J Neurosci. 2016 Jul 13;36(28):7453-63. doi: 10.1523/JNEUROSCI.0156-16.2016.

Abstract

Accurate sensory discrimination is commonly believed to require precise representations in the nervous system; however, neural stimulus responses can be highly variable, even to identical stimuli. Recent studies suggest that cortical response variability decreases during stimulus processing, but the implications of such effects on stimulus discrimination are unclear. To address this, we examined electrocorticographic cortical field potential recordings from the human nonprimary auditory cortex (superior temporal gyrus) while subjects listened to speech syllables. Compared with a prestimulus baseline, activation variability decreased upon stimulus onset, similar to findings from microelectrode recordings in animal studies. We found that this decrease was simultaneous with encoding and spatially specific for those electrodes that most strongly discriminated speech sounds. We also found that variability was predominantly reduced in a correlated subspace across electrodes. We then compared signal and variability (noise) correlations and found that noise correlations reduce more for electrodes with strong signal correlations. Furthermore, we found that this decrease in variability is strongest in the high gamma band, which correlates with firing rate response. Together, these findings indicate that the structure of single-trial response variability is shaped to enhance discriminability despite non-stimulus-related noise.

Significance statement: Cortical responses can be highly variable to auditory speech sounds. Despite this, sensory perception can be remarkably stable. Here, we recorded from the human superior temporal gyrus, a high-order auditory cortex, and studied the changes in the cortical representation of speech stimuli across multiple repetitions. We found that neural variability is reduced upon stimulus onset across electrodes that encode speech sounds.

Keywords: ECoG; encoding; noise correlations; speech; superior temporal gyrus; variability.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Acoustic Stimulation
  • Brain Mapping*
  • Electrocorticography
  • Evoked Potentials, Auditory / physiology*
  • Factor Analysis, Statistical
  • Female
  • Fourier Analysis
  • Humans
  • Male
  • Nonlinear Dynamics*
  • Speech Perception / physiology*
  • Temporal Lobe / physiology*
  • Time Factors