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Research Articles, Behavioral/Cognitive

Neural signatures of auditory perceptual bistability revealed by large-scale human intracranial recordings

Rodica Curtu, Xiayi Wang, Bingni W. Brunton and Kirill V. Nourski
Journal of Neuroscience 12 June 2019, 0655-18; DOI: https://doi.org/10.1523/JNEUROSCI.0655-18.2019
Rodica Curtu
1Department of Mathematics, The University of Iowa, Iowa City, IA 52242, USA
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Xiayi Wang
1Department of Mathematics, The University of Iowa, Iowa City, IA 52242, USA
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Bingni W. Brunton
2Department of Biology, University of Washington, Seattle, WA 98195, USA
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Kirill V. Nourski
3Department of Neurosurgery, The University of Iowa, Iowa City, IA 52242, USA
4Iowa Neuroscience Institute, The University of Iowa, Iowa City, IA 52242, USA
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Abstract

A key challenge in neuroscience is understanding how sensory stimuli give rise to perception, especially when the process is supported by neural activity from an extended network of brain areas. Perception is inherently subjective, so interrogating its neural signatures requires, ideally, a combination of three factors: behavioral tasks that separate stimulus-driven activity from perception per se; human subjects who self-report their percepts while performing those tasks; concurrent neural recordings acquired at high spatial and temporal resolution. In this study, we analyzed human electrocorticographic recordings obtained during an auditory task which supported mutually exclusive perceptual interpretations. Eight neurosurgical patients (5 male; 3 female) listened to sequences of repeated triplets where tones were separated in frequency by several semitones. Subjects reported spontaneous alternations between two auditory perceptual states, 1-stream and 2-stream, by pressing a button. We compared averaged auditory evoked potentials (AEPs) associated with 1-stream and 2-stream percepts and identified significant differences between them in primary and non-primary auditory cortex, surrounding auditory-related temporoparietal cortex, and frontal areas. We developed classifiers to identify spatial maps of percept-related differences in the AEP, corroborating findings from statistical analysis. We employed one-dimensional embedding spaces to perform the group-level analysis. Our data illustrate exemplar high temporal resolution AEP waveforms in auditory core region; explain inconsistencies in perceptual effects within auditory cortex, reported across non-invasive studies of streaming of triplets; show percept-related changes in frontoparietal areas previously highlighted by studies that focused on perceptual transitions; and demonstrate that auditory cortex encodes maintenance of percepts and switches between them.

SIGNIFICANCE STATEMENT

The human brain has the remarkable ability to discern complex and ambiguous stimuli from the external world by parsing mixed inputs into interpretable segments. However, one's perception can deviate from objective reality. But how do perceptual discrepancies occur? What are their anatomical substrates? To address these questions, we performed intracranial recordings in neurosurgical patients as they reported their perception of sounds associated with two mutually exclusive interpretations. We identified signatures of subjective percepts as distinct from sound-driven brain activity in core and non-core auditory cortex and frontoparietal cortex. These findings were compared to previous studies of auditory bistable perception and suggested that perceptual transitions and maintenance of perceptual states were supported by common neural substrates.

Footnotes

  • The authors declare no competing financial interests.

  • This work was supported by grants NSF CRCNS-1515678, NIH R01 DC04290, NIH UL1RR024979, and by the Simons Foundation, Alfred P. Sloan Foundation, and Washington Research Foundation. The authors thank Haiming Chen, Phillip Gander, Matthew Howard, Hiroto Kawasaki, Christopher Kovach, Ariane Rhone and Beau Snoad for help with data acquisition and pre-processing.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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Neural signatures of auditory perceptual bistability revealed by large-scale human intracranial recordings
Rodica Curtu, Xiayi Wang, Bingni W. Brunton, Kirill V. Nourski
Journal of Neuroscience 12 June 2019, 0655-18; DOI: 10.1523/JNEUROSCI.0655-18.2019

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Neural signatures of auditory perceptual bistability revealed by large-scale human intracranial recordings
Rodica Curtu, Xiayi Wang, Bingni W. Brunton, Kirill V. Nourski
Journal of Neuroscience 12 June 2019, 0655-18; DOI: 10.1523/JNEUROSCI.0655-18.2019
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