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Published March 27, 2023 | Submitted + Supplemental Material
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Unsupervised Restoration of a Complex Learned Behavior After Large-Scale Neuronal Perturbation

Abstract

Reliable execution of behaviors requires that brain circuits correct for variations in neuronal dynamics. Genetic perturbation of the majority of excitatory neurons in a brain region involved in song production in adult songbirds with stereotypical songs triggered severe degradation of their songs. The song fully recovered within two weeks, and substantial improvement occurred even when animals were prevented from singing during the recovery period, indicating that offline mechanisms enable recovery in an unsupervised manner. Song restoration was accompanied by increased excitatory synaptic inputs to unmanipulated neurons in the same region. A model inspired by the behavioral and electrophysiological findings suggests that a combination of unsupervised single-cell and population-level homeostatic plasticity rules can support the observed functional restoration after large-scale disruption of networks implementing sequential dynamics. In the model the sequence is restored through a parallel homeostatic process, rather than regrown serially, and predicts that sequences should recover in a saltatory fashion. Correspondingly, we observed such recovery in the songs of manipulated animals, with syllables that rapidly alternate between abnormal and normal durations from rendition to rendition until eventually they permanently settled into their original length. These observations indicate the existence of cellular and systems-level restorative mechanisms that ensure behavioral resilience.

Additional Information

The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. Author contributions: All authors contributed to the conceptualization, methodology, and writing of the paper. Investigation - Experiments: BW, ZT, SW, TV, CL Investigation - Computational: AD, DB Visualization: BW, ZT , AD, DB Funding acquisition & Supervision: AF, CL Data and materials availability. All derived data in this study are included in this article. Raw datasets and computer codes are available from the corresponding authors on reasonable request. The authors have declared no competing interest.

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Submitted - 2022.09.09.507372v1.full.pdf

Supplemental Material - media-1.pdf

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Additional details

Created:
August 20, 2023
Modified:
October 18, 2023