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Decoding violated sensory expectations from the auditory cortex of anaesthetised mice: Hierarchical recurrent neural network depicts separate ‘danger’ and ‘safety’ units

The ability to respond appropriately to sensory information received from the external environment is among the most fundamental capabilities of central nervous systems. In the auditory domain, processes underlying this behaviour are studied by measuring auditory‐evoked electrophysiology during sequ...

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Autores principales: O'Reilly, Jamie A., Angsuwatanakul, Thanate, Wehrman, Jordan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9545291/
https://www.ncbi.nlm.nih.gov/pubmed/35695993
http://dx.doi.org/10.1111/ejn.15736
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author O'Reilly, Jamie A.
Angsuwatanakul, Thanate
Wehrman, Jordan
author_facet O'Reilly, Jamie A.
Angsuwatanakul, Thanate
Wehrman, Jordan
author_sort O'Reilly, Jamie A.
collection PubMed
description The ability to respond appropriately to sensory information received from the external environment is among the most fundamental capabilities of central nervous systems. In the auditory domain, processes underlying this behaviour are studied by measuring auditory‐evoked electrophysiology during sequences of sounds with predetermined regularities. Identifying neural correlates of ensuing auditory novelty responses is supported by research in experimental animals. In the present study, we reanalysed epidural field potential recordings from the auditory cortex of anaesthetised mice during frequency and intensity oddball stimulation. Multivariate pattern analysis (MVPA) and hierarchical recurrent neural network (RNN) modelling were adopted to explore these data with greater resolution than previously considered using conventional methods. Time‐wise and generalised temporal decoding MVPA approaches revealed previously underestimated asymmetry between responses to sound‐level transitions in the intensity oddball paradigm, in contrast with tone frequency changes. After training, the cross‐validated RNN model architecture with four hidden layers produced output waveforms in response to simulated auditory inputs that were strongly correlated with grand‐average auditory‐evoked potential waveforms (r (2) > .9). Units in hidden layers were classified based on their temporal response properties and characterised using principal component analysis and sample entropy. These demonstrated spontaneous alpha rhythms, sound onset and offset responses and putative ‘safety’ and ‘danger’ units activated by relatively inconspicuous and salient changes in auditory inputs, respectively. The hypothesised existence of corresponding biological neural sources is naturally derived from this model. If proven, this could have significant implications for prevailing theories of auditory processing.
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spelling pubmed-95452912022-10-14 Decoding violated sensory expectations from the auditory cortex of anaesthetised mice: Hierarchical recurrent neural network depicts separate ‘danger’ and ‘safety’ units O'Reilly, Jamie A. Angsuwatanakul, Thanate Wehrman, Jordan Eur J Neurosci Systems Neuroscience The ability to respond appropriately to sensory information received from the external environment is among the most fundamental capabilities of central nervous systems. In the auditory domain, processes underlying this behaviour are studied by measuring auditory‐evoked electrophysiology during sequences of sounds with predetermined regularities. Identifying neural correlates of ensuing auditory novelty responses is supported by research in experimental animals. In the present study, we reanalysed epidural field potential recordings from the auditory cortex of anaesthetised mice during frequency and intensity oddball stimulation. Multivariate pattern analysis (MVPA) and hierarchical recurrent neural network (RNN) modelling were adopted to explore these data with greater resolution than previously considered using conventional methods. Time‐wise and generalised temporal decoding MVPA approaches revealed previously underestimated asymmetry between responses to sound‐level transitions in the intensity oddball paradigm, in contrast with tone frequency changes. After training, the cross‐validated RNN model architecture with four hidden layers produced output waveforms in response to simulated auditory inputs that were strongly correlated with grand‐average auditory‐evoked potential waveforms (r (2) > .9). Units in hidden layers were classified based on their temporal response properties and characterised using principal component analysis and sample entropy. These demonstrated spontaneous alpha rhythms, sound onset and offset responses and putative ‘safety’ and ‘danger’ units activated by relatively inconspicuous and salient changes in auditory inputs, respectively. The hypothesised existence of corresponding biological neural sources is naturally derived from this model. If proven, this could have significant implications for prevailing theories of auditory processing. John Wiley and Sons Inc. 2022-06-22 2022-08 /pmc/articles/PMC9545291/ /pubmed/35695993 http://dx.doi.org/10.1111/ejn.15736 Text en © 2022 The Authors. European Journal of Neuroscience published by Federation of European Neuroscience Societies and John Wiley & Sons Ltd. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Systems Neuroscience
O'Reilly, Jamie A.
Angsuwatanakul, Thanate
Wehrman, Jordan
Decoding violated sensory expectations from the auditory cortex of anaesthetised mice: Hierarchical recurrent neural network depicts separate ‘danger’ and ‘safety’ units
title Decoding violated sensory expectations from the auditory cortex of anaesthetised mice: Hierarchical recurrent neural network depicts separate ‘danger’ and ‘safety’ units
title_full Decoding violated sensory expectations from the auditory cortex of anaesthetised mice: Hierarchical recurrent neural network depicts separate ‘danger’ and ‘safety’ units
title_fullStr Decoding violated sensory expectations from the auditory cortex of anaesthetised mice: Hierarchical recurrent neural network depicts separate ‘danger’ and ‘safety’ units
title_full_unstemmed Decoding violated sensory expectations from the auditory cortex of anaesthetised mice: Hierarchical recurrent neural network depicts separate ‘danger’ and ‘safety’ units
title_short Decoding violated sensory expectations from the auditory cortex of anaesthetised mice: Hierarchical recurrent neural network depicts separate ‘danger’ and ‘safety’ units
title_sort decoding violated sensory expectations from the auditory cortex of anaesthetised mice: hierarchical recurrent neural network depicts separate ‘danger’ and ‘safety’ units
topic Systems Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9545291/
https://www.ncbi.nlm.nih.gov/pubmed/35695993
http://dx.doi.org/10.1111/ejn.15736
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