An emergent neural coactivity code for dynamic memory

Mohamady El-Gaby*, Hayley M. Reeve, Vítor Lopes-dos-Santos, Natalia Campo-Urriza, Pavel V. Perestenko, Alexander Morley, Lauren A.M. Strickland, István P. Lukács, Ole Paulsen, David Dupret

*Corresponding author for this work

Research output: Contribution to journalArticle (Academic Journal)peer-review

1 Citation (Scopus)

Abstract

Neural correlates of external variables provide potential internal codes that guide an animal’s behavior. Notably, first-order features of neural activity, such as single-neuron firing rates, have been implicated in encoding information. However, the extent to which higher-order features, such as multineuron coactivity, play primary roles in encoding information or secondary roles in supporting single-neuron codes remains unclear. Here, we show that millisecond-timescale coactivity among hippocampal CA1 neurons discriminates distinct, short-lived behavioral contingencies. This contingency discrimination was unrelated to the tuning of individual neurons, but was instead an emergent property of their coactivity. Contingency-discriminating patterns were reactivated offline after learning, and their reinstatement predicted trial-by-trial memory performance. Moreover, optogenetic suppression of inputs from the upstream CA3 region during learning impaired coactivity-based contingency information in the CA1 and subsequent dynamic memory retrieval. These findings identify millisecond-timescale coactivity as a primary feature of neural firing that encodes behaviorally relevant variables and supports memory retrieval.

Original languageEnglish
Pages (from-to)694-704
Number of pages11
JournalNature Neuroscience
Volume24
Issue number5
Early online date29 Mar 2021
DOIs
Publication statusPublished - May 2021

Bibliographical note

Funding Information:
We thank D. Bannerman and S. McHugh for helpful advice when designing the behavioral protocol, J. Westcott and B. Micklem for technical support, W. Podlaski and T. Vogels for useful discussions on neural coding models, A.J. Quinn for developing the EMD toolbox and S. Trouche, H. Barron and all the members of the Dupret laboratory for useful discussions. This work was supported by the Biotechnology and Biological Sciences Research Council UK (BB/N00597X/1 to D.D. and BB/N006836/1 to O.P.) and the Medical Research Council UK (MC_UU_12024/3 and MC_UU_00003/4 to D.D.).

Publisher Copyright:
© 2021, The Author(s), under exclusive licence to Springer Nature America, Inc.

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