Article (Scientific journals)
An increase of inhibition drives the developmental decorrelation of neural activity.
Chini, Mattia; Pfeffer, Thomas; Hanganu-Opatz, Ileana
2022In eLife, 11
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Keywords :
E-I ratio; decorrelation; development; electrophysiology; human; mouse; neural network models; neuroscience; Animals; Brain; Humans; Inhibition, Psychological; Mice; Neural Inhibition; Neurodevelopmental Disorders; Prefrontal Cortex/physiology; Prefrontal Cortex; Neuroscience (all); Medicine (all); Biochemistry, Genetics and Molecular Biology (all); Immunology and Microbiology (all)
Abstract :
[en] Throughout development, the brain transits from early highly synchronous activity patterns to a mature state with sparse and decorrelated neural activity, yet the mechanisms underlying this process are poorly understood. The developmental transition has important functional consequences, as the latter state is thought to allow for more efficient storage, retrieval, and processing of information. Here, we show that, in the mouse medial prefrontal cortex (mPFC), neural activity during the first two postnatal weeks decorrelates following specific spatial patterns. This process is accompanied by a concomitant tilting of excitation-inhibition (E-I) ratio toward inhibition. Using optogenetic manipulations and neural network modeling, we show that the two phenomena are mechanistically linked, and that a relative increase of inhibition drives the decorrelation of neural activity. Accordingly, in mice mimicking the etiology of neurodevelopmental disorders, subtle alterations in E-I ratio are associated with specific impairments in the correlational structure of spike trains. Finally, capitalizing on EEG data from newborn babies, we show that an analogous developmental transition takes place also in the human brain. Thus, changes in E-I ratio control the (de)correlation of neural activity and, by these means, its developmental imbalance might contribute to the pathogenesis of neurodevelopmental disorders.
Disciplines :
Life sciences: Multidisciplinary, general & others
Author, co-author :
Chini, Mattia  ;  Institute of Developmental Neurophysiology, Center for Molecular Neurobiology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
Pfeffer, Thomas ;  Center for Brain and Cognition, Computational Neuroscience Group, Universitat Pompeu Fabra, Barcelona, Spain
Hanganu-Opatz, Ileana ;  Institute of Developmental Neurophysiology, Center for Molecular Neurobiology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
Language :
English
Title :
An increase of inhibition drives the developmental decorrelation of neural activity.
Publication date :
17 August 2022
Journal title :
eLife
eISSN :
2050-084X
Publisher :
eLife Sciences Publications Ltd, England
Volume :
11
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
ERC - European Research Council
Marie Skłodowska-Curie Actions
EU - European Union
DFG - Deutsche Forschungsgemeinschaft
AvH - Alexander von Humboldt Foundation
Funding text :
We thank Amit Marmelshtein, Stefano Panzeri, Giulio Bondanelli, Sebastian Bitzenhofer, Johanna Kostka, Jastyn P\u00F6pplau, and Lingzhen Song for valuable discussions and feedback on the manu-script, and P Putthoff, A Marquardt, and A Dahlmann for excellent technical assistance. This work was funded by grants from the European Research Council (ERC-2015-CoG 681577 to ILH-O), Marie Curie Training Network euSNN (MSCA-ITN-H2020-860563 to ILH-O), Horizon 2020 DEEPER 101016787, the German Research Foundation (437610067, 178316478, and 302153259 to ILH-O) and Landesforschungsf\u00F6rderung Hamburg (LFF76, LFF73 to ILH-O).We thank Amit Marmelshtein, Stefano Panzeri, Giulio Bondanelli, Sebastian Bitzenhofer, Johanna Kostka, Jastyn P\u00F6pplau, and Lingzhen Song for valuable discussions and feedback on the manuscript, and P Putthoff, A Marquardt, and A Dahlmann for excellent technical assistance. This work was funded by grants from the European Research Council (ERC-2015-CoG 681577 to ILH-O), Marie Curie Training Network euSNN (MSCA-ITN-H2020-860563 to ILH-O), Horizon2020 DEEPER 101016787, the German Research Foundation (437610067, 178316478, and 302153259 to ILH-O) and Landes-forschungsf\u00F6rderung Hamburg (LFF76, LFF73 to ILH-O).
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