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Sequence learning modulates neural responses and oscillatory coupling in human and monkey auditory cortex
Journal article   Open access

Sequence learning modulates neural responses and oscillatory coupling in human and monkey auditory cortex

Yukiko Kikuchi, Adam Attaheri, Benjamin Wilson, Ariane E Rhone, Kirill V Nourski, Phillip E Gander, Christopher K Kovach, Hiroto Kawasaki, Timothy D Griffiths, Matthew A Howard III, …
PLoS biology, Vol.15(4), pp.e2000219-e2000219
04/2017
DOI: 10.1371/journal.pbio.2000219
PMCID: PMC5404755
PMID: 28441393
url
https://doi.org/10.1371/journal.pbio.2000219View
Published (Version of record) Open Access

Abstract

Learning complex ordering relationships between sensory events in a sequence is fundamental for animal perception and human communication. While it is known that rhythmic sensory events can entrain brain oscillations at different frequencies, how learning and prior experience with sequencing relationships affect neocortical oscillations and neuronal responses is poorly understood. We used an implicit sequence learning paradigm (an "artificial grammar") in which humans and monkeys were exposed to sequences of nonsense words with regularities in the ordering relationships between the words. We then recorded neural responses directly from the auditory cortex in both species in response to novel legal sequences or ones violating specific ordering relationships. Neural oscillations in both monkeys and humans in response to the nonsense word sequences show strikingly similar hierarchically nested low-frequency phase and high-gamma amplitude coupling, establishing this form of oscillatory coupling-previously associated with speech processing in the human auditory cortex-as an evolutionarily conserved biological process. Moreover, learned ordering relationships modulate the observed form of neural oscillatory coupling in both species, with temporally distinct neural oscillatory effects that appear to coordinate neuronal responses in the monkeys. This study identifies the conserved auditory cortical neural signatures involved in monitoring learned sequencing operations, evident as modulations of transient coupling and neuronal responses to temporally structured sensory input.
 Magnetic Resonance Imaging Auditory Cortex - diagnostic imaging Species Specificity Verbal Learning Neurovascular Coupling Humans Male Neural Conduction Reaction Time Macaca mulatta Auditory Cortex - physiology Biological Evolution Animals Auditory Pathways - physiology Functional Neuroimaging Audiometry, Evoked Response Neurons - physiology Brain Mapping Adult Auditory Pathways - diagnostic imaging Female Models, Neurological Speech Perception Task Performance and Analysis

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