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Auditory prediction hierarchy in the human hippocampus and amygdala

View ORCID ProfileAthina Tzovara, Tommaso Fedele, Johannes Sarnthein, Debora Ledergerber, Jack J. Lin, Robert T. Knight
doi: https://doi.org/10.1101/2022.11.16.516768
Athina Tzovara
1Helen Wills Neuroscience Institute, University of California, Berkeley, USA
2Institute of Computer Science, University of Bern, Switzerland
3Center for Experimental Neurology - Sleep Wake Epilepsy Center | NeuroTec, Department of Neurology, Inselspital, Bern University Hospital, University of Bern, Switzerland
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  • ORCID record for Athina Tzovara
  • For correspondence: athina.tzovara@unibe.ch
Tommaso Fedele
4Neurosurgery Department, University Hospital Zurich, Switzerland
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Johannes Sarnthein
4Neurosurgery Department, University Hospital Zurich, Switzerland
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Debora Ledergerber
5Swiss Epilepsy Center, Klinik Lengg, Zurich, Switzerland
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Jack J. Lin
6Department of Neurology, University of California, Davis, Davis, USA
7The Center of Mind and Brain, University of California, Davis, Davis, USA
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Robert T. Knight
1Helen Wills Neuroscience Institute, University of California, Berkeley, USA
8Department of Psychology, University of California, Berkeley, USA
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Abstract

Our brains can extract structure from the environment and form predictions given past sensory experience. Predictive circuits have been identified in wide-spread cortical regions. However, the contribution of subcortical areas, such as the hippocampus and amygdala in the formation of predictions remains under-explored. Here, we hypothesized that the hippocampus would be sensitive to predictability in sound sequences, while the amygdala would be sensitive to unexpected violations of auditory rules. We presented epileptic patients undergoing presurgical monitoring with standard and deviant sounds, in a predictable or unpredictable context. Onsets of auditory responses and unpredictable deviance effects were detected at earlier latencies in the temporal cortex compared to the amygdala and hippocampus. Deviance effects in 1-20 Hz local field potentials were detected in the lateral temporal cortex, irrespective of predictability. The amygdala showed stronger deviance responses in the unpredictable context. Additionally, low frequency deviance responses in the hippocampus (1-8 Hz) were observed in the predictable but not in the unpredictable context. Our results reveal a distributed cortical-subcortical network underlying the generation of auditory predictions, comprising temporal cortex and the hippocampus and amygdala, and suggest that the neural basis of sensory predictions and prediction error signals needs to be extended to subcortical regions.

Competing Interest Statement

The authors have declared no competing interest.

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 4.0 International license.
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Posted November 16, 2022.
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Auditory prediction hierarchy in the human hippocampus and amygdala
Athina Tzovara, Tommaso Fedele, Johannes Sarnthein, Debora Ledergerber, Jack J. Lin, Robert T. Knight
bioRxiv 2022.11.16.516768; doi: https://doi.org/10.1101/2022.11.16.516768
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Auditory prediction hierarchy in the human hippocampus and amygdala
Athina Tzovara, Tommaso Fedele, Johannes Sarnthein, Debora Ledergerber, Jack J. Lin, Robert T. Knight
bioRxiv 2022.11.16.516768; doi: https://doi.org/10.1101/2022.11.16.516768

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