Parallel mechanisms signal a hierarchy of sequence structure violations in the auditory cortex
The brain predicts regularities in sensory inputs at multiple complexity levels, with neuronal mechanisms that remain elusive. Here, we monitored auditory cortex activity during the local-global paradigm, a protocol nesting different regularity levels in sound sequences. We observed that mice encode...
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2024-12-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/102702 |
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| _version_ | 1846139249964875776 |
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| author | Sara Jamali Sophie Bagur Enora Bremont Timo Van Kerkoerle Stanislas Dehaene Brice Bathellier |
| author_facet | Sara Jamali Sophie Bagur Enora Bremont Timo Van Kerkoerle Stanislas Dehaene Brice Bathellier |
| author_sort | Sara Jamali |
| collection | DOAJ |
| description | The brain predicts regularities in sensory inputs at multiple complexity levels, with neuronal mechanisms that remain elusive. Here, we monitored auditory cortex activity during the local-global paradigm, a protocol nesting different regularity levels in sound sequences. We observed that mice encode local predictions based on stimulus occurrence and stimulus transition probabilities, because auditory responses are boosted upon prediction violation. This boosting was due to both short-term adaptation and an adaptation-independent surprise mechanism resisting anesthesia. In parallel, and only in wakefulness, VIP interneurons responded to the omission of the locally expected sound repeat at the sequence ending, thus providing a chunking signal potentially useful for establishing global sequence structure. When this global structure was violated, by either shortening the sequence or ending it with a locally expected but globally unexpected sound transition, activity slightly increased in VIP and PV neurons, respectively. Hence, distinct cellular mechanisms predict different regularity levels in sound sequences. |
| format | Article |
| id | doaj-art-44a26f48b8aa43a886ce1bde2db5e4a5 |
| institution | Kabale University |
| issn | 2050-084X |
| language | English |
| publishDate | 2024-12-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj-art-44a26f48b8aa43a886ce1bde2db5e4a52024-12-06T11:17:52ZengeLife Sciences Publications LtdeLife2050-084X2024-12-011310.7554/eLife.102702Parallel mechanisms signal a hierarchy of sequence structure violations in the auditory cortexSara Jamali0https://orcid.org/0000-0003-4933-3167Sophie Bagur1https://orcid.org/0000-0002-4375-1838Enora Bremont2Timo Van Kerkoerle3https://orcid.org/0000-0003-1935-8216Stanislas Dehaene4Brice Bathellier5https://orcid.org/0000-0001-9211-1960Université Paris Cité, Institut Pasteur, AP-HP, Inserm, Fondation Pour l'Audition, Institut de l’Audition, IHU reConnect, Paris, FranceUniversité Paris Cité, Institut Pasteur, AP-HP, Inserm, Fondation Pour l'Audition, Institut de l’Audition, IHU reConnect, Paris, FranceUniversité Paris Cité, Institut Pasteur, AP-HP, Inserm, Fondation Pour l'Audition, Institut de l’Audition, IHU reConnect, Paris, FranceUniversité Paris Saclay, INSERM, CEA, Cognitive Neuroimaging Unit, NeuroSpin Center, Paris, France; Collège de France, PSL University, Paris, FranceUniversité Paris Saclay, INSERM, CEA, Cognitive Neuroimaging Unit, NeuroSpin Center, Paris, France; Collège de France, PSL University, Paris, FranceUniversité Paris Cité, Institut Pasteur, AP-HP, Inserm, Fondation Pour l'Audition, Institut de l’Audition, IHU reConnect, Paris, FranceThe brain predicts regularities in sensory inputs at multiple complexity levels, with neuronal mechanisms that remain elusive. Here, we monitored auditory cortex activity during the local-global paradigm, a protocol nesting different regularity levels in sound sequences. We observed that mice encode local predictions based on stimulus occurrence and stimulus transition probabilities, because auditory responses are boosted upon prediction violation. This boosting was due to both short-term adaptation and an adaptation-independent surprise mechanism resisting anesthesia. In parallel, and only in wakefulness, VIP interneurons responded to the omission of the locally expected sound repeat at the sequence ending, thus providing a chunking signal potentially useful for establishing global sequence structure. When this global structure was violated, by either shortening the sequence or ending it with a locally expected but globally unexpected sound transition, activity slightly increased in VIP and PV neurons, respectively. Hence, distinct cellular mechanisms predict different regularity levels in sound sequences.https://elifesciences.org/articles/102702auditory cortexpredictive codingsequence predictionadaptationomission responsesglobal violations |
| spellingShingle | Sara Jamali Sophie Bagur Enora Bremont Timo Van Kerkoerle Stanislas Dehaene Brice Bathellier Parallel mechanisms signal a hierarchy of sequence structure violations in the auditory cortex eLife auditory cortex predictive coding sequence prediction adaptation omission responses global violations |
| title | Parallel mechanisms signal a hierarchy of sequence structure violations in the auditory cortex |
| title_full | Parallel mechanisms signal a hierarchy of sequence structure violations in the auditory cortex |
| title_fullStr | Parallel mechanisms signal a hierarchy of sequence structure violations in the auditory cortex |
| title_full_unstemmed | Parallel mechanisms signal a hierarchy of sequence structure violations in the auditory cortex |
| title_short | Parallel mechanisms signal a hierarchy of sequence structure violations in the auditory cortex |
| title_sort | parallel mechanisms signal a hierarchy of sequence structure violations in the auditory cortex |
| topic | auditory cortex predictive coding sequence prediction adaptation omission responses global violations |
| url | https://elifesciences.org/articles/102702 |
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