Concurrent temporal channels for auditory processing: Oscillatory neural entrainment reveals segregation of function at different scales

PLoS Biol. 2017 Nov 2;15(11):e2000812. doi: 10.1371/journal.pbio.2000812. eCollection 2017 Nov.

Abstract

Natural sounds convey perceptually relevant information over multiple timescales, and the necessary extraction of multi-timescale information requires the auditory system to work over distinct ranges. The simplest hypothesis suggests that temporal modulations are encoded in an equivalent manner within a reasonable intermediate range. We show that the human auditory system selectively and preferentially tracks acoustic dynamics concurrently at 2 timescales corresponding to the neurophysiological theta band (4-7 Hz) and gamma band ranges (31-45 Hz) but, contrary to expectation, not at the timescale corresponding to alpha (8-12 Hz), which has also been found to be related to auditory perception. Listeners heard synthetic acoustic stimuli with temporally modulated structures at 3 timescales (approximately 190-, approximately 100-, and approximately 30-ms modulation periods) and identified the stimuli while undergoing magnetoencephalography recording. There was strong intertrial phase coherence in the theta band for stimuli of all modulation rates and in the gamma band for stimuli with corresponding modulation rates. The alpha band did not respond in a similar manner. Classification analyses also revealed that oscillatory phase reliably tracked temporal dynamics but not equivalently across rates. Finally, mutual information analyses quantifying the relation between phase and cochlear-scaled correlations also showed preferential processing in 2 distinct regimes, with the alpha range again yielding different patterns. The results support the hypothesis that the human auditory system employs (at least) a 2-timescale processing mode, in which lower and higher perceptual sampling scales are segregated by an intermediate temporal regime in the alpha band that likely reflects different underlying computations.

MeSH terms

  • Acoustic Stimulation*
  • Auditory Perception / physiology*
  • Behavior
  • Biomarkers / metabolism
  • Electroencephalography
  • Evoked Potentials, Auditory / physiology
  • Female
  • Gamma Rhythm / physiology
  • Humans
  • Male
  • Nervous System Physiological Phenomena*
  • Theta Rhythm / physiology
  • Time Factors
  • Young Adult

Substances

  • Biomarkers