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Broadband Dynamics Rather than Frequency-Specific Rhythms Underlie Prediction Error in the Primate Auditory Cortex

View ORCID ProfileAndrés Canales-Johnson, View ORCID ProfileAna Filipa Teixeira Borges, View ORCID ProfileMisako Komatsu, Naotaka Fujii, View ORCID ProfileJohannes J. Fahrenfort, View ORCID ProfileKai J. Miller, Valdas Noreika
doi: https://doi.org/10.1101/821942
Andrés Canales-Johnson
1Consciousness and Cognition Lab, Department of Psychology, University of Cambridge, Cambridge, United Kingdom
2Vicerrectoría de Investigación y Posgrado, Universidad Católica del Maule, Talca, Chile
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  • For correspondence: afc37@cam.ac.uk v.noreika@qmul.ac.uk
Ana Filipa Teixeira Borges
3Department of Integrative Neurophysiology, Center for Neurogenomics and Cognitive Research, VU University Amsterdam, Amsterdam, The Netherlands
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Misako Komatsu
4Laboratory for Adaptive Intelligence, RIKEN Brain Science Institute, Wako, Saitama, Japan
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Naotaka Fujii
4Laboratory for Adaptive Intelligence, RIKEN Brain Science Institute, Wako, Saitama, Japan
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Johannes J. Fahrenfort
5Department of Psychology, University of Amsterdam, Amsterdam, The Netherlands
6Department of Experimental and Applied Psychology, Vrije Universiteit, Amsterdam, The Netherlands
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Kai J. Miller
7Department of Neurosurgery, Mayo Clinic, Rochester, United States of America
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Valdas Noreika
8Department of Biological and Experimental Psychology, School of Biological and Behavioural Sciences, Queen Mary University of London, London, United Kingdom
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  • For correspondence: afc37@cam.ac.uk v.noreika@qmul.ac.uk
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Abstract

Detection of statistical irregularities, measured as a prediction error response, is fundamental to the perceptual monitoring of the environment. We studied whether prediction error response is associated with neural oscillations or asynchronous broadband activity. Electrocorticography (ECoG) was carried out in three male monkeys, who passively listened to the auditory roving oddball stimuli. Local field potentials (LFP) recorded over the auditory cortex underwent spectral principal component analysis, which decoupled broadband and rhythmic components of the LFP signal. We found that the broadband component captured the prediction error response, whereas none of the rhythmic components were associated with statistical irregularities of sounds. The broadband component displayed more stochastic, asymmetrical multifractal properties than the rhythmic components, which revealed more self-similar dynamics. We thus conclude that the prediction error response is captured by neuronal populations generating asynchronous broadband activity, defined by irregular dynamical states which, unlike oscillatory rhythms, appear to enable the neural representation of auditory prediction error response.

Significance Statement This study aimed to examine the contribution of oscillatory and asynchronous components of auditory local field potentials in the generation of prediction error responses to sensory irregularities, as this has not been directly addressed in the previous studies. Here, we show that mismatch negativity – an auditory prediction error response – is driven by the asynchronous broadband component of potentials recorded in the auditory cortex. This finding highlights the importance of non-oscillatory neural processes in the predictive monitoring of the environment. At a more general level, the study demonstrates that stochastic neural processes, which are often disregarded as neural noise, do have a functional role in the processing of sensory information.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • http://neurotycho.org/

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license.
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Posted September 21, 2021.
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Broadband Dynamics Rather than Frequency-Specific Rhythms Underlie Prediction Error in the Primate Auditory Cortex
Andrés Canales-Johnson, Ana Filipa Teixeira Borges, Misako Komatsu, Naotaka Fujii, Johannes J. Fahrenfort, Kai J. Miller, Valdas Noreika
bioRxiv 821942; doi: https://doi.org/10.1101/821942
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Broadband Dynamics Rather than Frequency-Specific Rhythms Underlie Prediction Error in the Primate Auditory Cortex
Andrés Canales-Johnson, Ana Filipa Teixeira Borges, Misako Komatsu, Naotaka Fujii, Johannes J. Fahrenfort, Kai J. Miller, Valdas Noreika
bioRxiv 821942; doi: https://doi.org/10.1101/821942

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