Preexisting hippocampal network dynamics constrain optogenetically induced place fields

Sam McKenzie, Roman Huszár, Daniel F. English, Kanghwan Kim, Fletcher Christensen, Euisik Yoon, György Buzsáki

Research output: Contribution to journalArticlepeer-review

37 Citations (Scopus)

Abstract

Memory models often emphasize the need to encode novel patterns of neural activity imposed by sensory drive. Prior learning and innate architecture likely restrict neural plasticity, however. Here, we test how the incorporation of synthetic hippocampal signals is constrained by preexisting circuit dynamics. We optogenetically stimulated small groups of CA1 neurons as mice traversed a chosen segment of a linear track, mimicking the emergence of place fields. Stimulation induced persistent place field remapping in stimulated and non-stimulated neurons. The emergence of place fields could be predicted from sporadic firing in the new place field location and the temporal relationship to peer neurons before the optogenetic perturbation. Circuit modification was reflected by altered spike transmission between connected pyramidal cells and inhibitory interneurons, which persisted during post-experience sleep. We hypothesize that optogenetic perturbation unmasked sub-threshold place fields. Plasticity in recurrent/lateral inhibition may drive learning through the rapid association of existing states.

Original languageEnglish
Pages (from-to)1040-1054.e7
JournalNeuron
Volume109
Issue number6
DOIs
Publication statusPublished - 2021 Mar 17

Bibliographical note

Funding Information:
We would like to thank Zachary Saccomano and Abed Ghanbari for providing software used in the present study and Yunchang Zhang and Sinan Kokuuslu for their help with data collection. We would like to thank Manuel Valero, Thomas Hainmueller, Antonio Fernández-Ruiz, and Shy Shoham for useful feedback on the manuscript before publication. This work was supported by NIMH K99MH118423, NIMH R00MH118423, NIH MH 122391, and NSF PIRE grant (no. 1545858), U19 NS107616, and U19 NS104590. S.M. and R.H. collected and analyzed the data. D.F.E. prepared the experimental subjects. K.K. and E.Y. provided the μLED probes. G.B. supervised all aspects of the experiment. F.C. assisted with the statistical analyses. S.M. R.H. and G.B designed the experiments and wrote the manuscript. The authors declare no competing interests.

Funding Information:
We would like to thank Zachary Saccomano and Abed Ghanbari for providing software used in the present study and Yunchang Zhang and Sinan Kokuuslu for their help with data collection. We would like to thank Manuel Valero, Thomas Hainmueller, Antonio Fernández-Ruiz, and Shy Shoham for useful feedback on the manuscript before publication. This work was supported by NIMH K99MH118423 , NIMH R00MH118423 , NIH MH 122391 , and NSF PIRE grant (no. 1545858 ), U19 NS107616 , and U19 NS104590 .

Publisher Copyright:
© 2021 Elsevier Inc.

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)

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