Inhibitory control of frontal metastability sets the temporal signature of cognition
- Inserm, France
- Sorbonne Université, CNRS, France
- Icahn School of Medicine at Mount Sinai, United States
Abstract
Cortical dynamics are organized over multiple anatomical and temporal scales. The mechanistic origin of the temporal organization and its contribution to cognition remain unknown. Here we demonstrate the cause of this organization by studying a specific temporal signature (time constant and latency) of neural activity. In monkey frontal areas, recorded during flexible decisions, temporal signatures display specific area-dependent ranges, as well as anatomical and cell-type distributions. Moreover, temporal signatures are functionally adapted to behaviorally relevant timescales. Fine-grained biophysical network models, constrained to account for experimentally observed temporal signatures, reveal that after-hyperpolarization potassium and inhibitory GABA-B conductances critically determine areas’ specificity. They mechanistically account for temporal signatures by organizing activity into metastable states, with inhibition controlling state stability and transitions. As predicted by models, state durations non-linearly scale with temporal signatures in monkey, matching behavioral timescales. Thus, local inhibitory-controlled metastability constitutes the dynamical core specifying the temporal organization of cognitive functions in frontal areas.
Data availability
All spike time series from monkey recordings, scripts for temporal signatures extraction and scripts of computational models are freely accessible on the Zenodo repository (https://doi.org/10.5281/zenodo.5707884).
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Code for spike analyses and biophysical modelling for 'Inhibitory control of frontal metastability sets the temporal signature of cognition"Zenodo repository,doi.org/10.5281/zenodo.5707884.
Article and author information
Author details
Funding
Fondation pour la Recherche Médicale (DEQ20160334905)
- Emmanuel Procyk
Agence Nationale de la Recherche (ANR-10-SVSE4-1441)
- Emmanuel Procyk
Agence Nationale de la Recherche (ANR-16-NEUC-0006-01)
- Bruno Delord
Agence Nationale de la Recherche (ANR-11-LABX-0042)
- Emmanuel Procyk
Fondation pour la Recherche Médicale (FDT201904008187)
- Vincent Fontanier
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: All procedures followed the European Community Council Directive (2010) (Ministère de l'Agriculture et de la Forêt, Commission nationale de l'expérimentation animale) and were approved by the localethical committee (Comité d'Ethique Lyonnais pour les Neurosciences Expérimentales, CELYNE, C2EA683 #42)
Copyright
© 2022, Fontanier et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Inhibitory control of frontal metastability sets the temporal signature of cognition
eLife 11:e63795.
https://doi.org/10.7554/eLife.63795
