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

Lookup NU author(s): Dr Yuki Kikuchi, Adam Attaheri, Dr Ben Wilson, Professor Tim Griffiths, Professor Christopher Petkov

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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.


Publication metadata

Author(s): Kikuchi Y, Attaheri A, Wilson B, Rhone AE, Nourski KV, Gander PE, Kovach CK, Kawasaki H, Griffiths TD, Howard MA, Petkov CI

Publication type: Article

Journal: PLoS Biology

Year: 2017

Volume: 15

Issue: 4

Pages: e2000219

Online publication date: 25/04/2017

Acceptance date: 20/03/2017

ISSN (electronic): 1932-6203

Publisher: Public Library of Science

URL: https://doi.org/10.1371/journal.pbio.2000219

DOI: 10.1371/journal.pbio.2000219

PubMed id: 28441393


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