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Spatiotemporal dynamics of auditory information processing in the insular cortex: an intracranial EEG study using an oddball paradigm

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Abstract

Functional neuroimaging studies using auditory stimuli consistently show activation of the insular cortex. However, due to the limited temporal resolution of non-invasive neuroimaging techniques, the role(s) of the insula in auditory processing remains unclear. As the anterior insula (aI) and the posterior insula (pI) have different connections and are thought to be functionally distinct, it is likely that these two areas contribute differently to auditory processing. Our study examines the spatiotemporal dynamics of auditory processing in the insula using intracranial electroencephalography (EEG). Eight epileptic patients completed two passive listening tasks and one three-stimulus auditory oddball detection task during the intracranial EEG monitoring of their drug-resistant seizures. Recordings were obtained from depth electrodes implanted in 11 insulae. Event-related potentials (ERPs) were analyzed using permutation analyses during the N100 and the P300 intervals, and modulations of alpha, theta, and gamma band responses were compared using Wilcoxon/Mann–Whitney analyses. N100 responses to auditory stimuli were mostly observed in the pI and were little affected by task conditions. Auditory target detection was associated with P300 ERPs, and alpha, theta, high- and low-gamma responses, preferentially at aI contacts. Results suggest that the aI is involved in voluntary attentional processing of task-relevant information, whereas the pI is involved in automatic auditory processing.

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Acknowledgements

We are grateful to the patients who were involved in this study. We also want to thank the staff of the neuro-epilepsy unit at Centre Hospitalier de l’Université de Montréal for their technical assistance.

Funding

This work was supported by the Canadian Institutes of Health Research (148563 to DKN, FL, OB, and MFE-115520 to OB) and by the Natural Sciences and Engineering Research Council of Canada (RGPIN-2016-05216 to DKN, FL, KJ). DKN holds the Canada Research Chair in Epilepsy and Functional Anatomy of the Human Brain.

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Authors and Affiliations

  1. Centre de Recherche du Centre Hospitalier de l’Université de Montreal (CHUM), Montreal, QC, Canada

    Daphné Citherlet, Olivier Boucher, Manon Robert & Dang Khoa Nguyen

  2. Département de Neurosciences, Université de Montréal, Montreal, Canada

    Daphné Citherlet & Dang Khoa Nguyen

  3. Département de Psychologie, Université de Montréal, Montreal, Canada

    Olivier Boucher, Anne Gallagher & Franco Lepore

  4. Service de Psychologie, CHUM, Montreal, QC, Canada

    Olivier Boucher

  5. Centre de Recherche du CHU Sainte-Justine, Montreal, Canada

    Julie Tremblay & Anne Gallagher

  6. Service de Neurochirurgie, CHUM, Montreal, QC, Canada

    Alain Bouthillier

  7. Service de Neurologie, Centre Hospitalier de l’Université de Montréal (CHUM), 900 rue Saint-Denis, Montreal, QC, H2X 0A9, Canada

    Dang Khoa Nguyen

Authors
  1. Daphné Citherlet
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  2. Olivier Boucher
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  3. Julie Tremblay
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  4. Manon Robert
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  5. Anne Gallagher
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  6. Alain Bouthillier
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  7. Franco Lepore
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  8. Dang Khoa Nguyen
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Correspondence to Dang Khoa Nguyen.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee (Comité d'éthique de la recherche, Centre de recherche du CHUM, 2016-5966, CE 15.018–CA) and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

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Informed consent was obtained from all individual participants included in the study.

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Citherlet, D., Boucher, O., Tremblay, J. et al. Spatiotemporal dynamics of auditory information processing in the insular cortex: an intracranial EEG study using an oddball paradigm. Brain Struct Funct 225, 1537–1559 (2020). https://doi.org/10.1007/s00429-020-02072-z

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  • DOI: https://doi.org/10.1007/s00429-020-02072-z

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