Differential Emergence and Stability of Sensory and Temporal Representations in Context-Specific Hippocampal Sequences

Jiannis Taxidis; Eftychios A Pnevmatikakis; Conor C Dorian; Apoorva L Mylavarapu; Jagmeet S Arora; Kian D Samadian; Emily A Hoffberg; Peyman Golshani

doi:10.1016/j.neuron.2020.08.028

Differential Emergence and Stability of Sensory and Temporal Representations in Context-Specific Hippocampal Sequences

Neuron. 2020 Dec 9;108(5):984-998.e9. doi: 10.1016/j.neuron.2020.08.028. Epub 2020 Sep 18.

Authors

Jiannis Taxidis¹, Eftychios A Pnevmatikakis², Conor C Dorian³, Apoorva L Mylavarapu³, Jagmeet S Arora³, Kian D Samadian³, Emily A Hoffberg³, Peyman Golshani⁴

Affiliations

¹ Department of Neurology, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA, USA; Integrative Center for Learning and Memory, Brain Research Institute, University of California, Los Angeles, Los Angeles, CA, USA. Electronic address: jtaxidis@ucla.edu.
² Center for Computational Mathematics, Flatiron Institute, New York, NY, USA.
³ Department of Neurology, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA, USA.
⁴ Department of Neurology, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA, USA; Integrative Center for Learning and Memory, Brain Research Institute, University of California, Los Angeles, Los Angeles, CA, USA; Semel Institute for Neuroscience and Human Behavior, University of California, Los Angeles, Los Angeles, CA, USA; West Los Angeles Veteran Affairs Medical Center, Los Angeles, CA, USA; Intellectual and Developmental Disabilities Research Center, University of California, Los Angeles, Los Angeles, CA, USA. Electronic address: pgolshani@mednet.ucla.edu.

Abstract

Hippocampal spiking sequences encode external stimuli and spatiotemporal intervals, linking sequential experiences in memory, but the dynamics controlling the emergence and stability of such diverse representations remain unclear. Using two-photon calcium imaging in CA1 while mice performed an olfactory working-memory task, we recorded stimulus-specific sequences of "odor-cells" encoding olfactory stimuli followed by "time-cells" encoding time points in the ensuing delay. Odor-cells were reliably activated and retained stable fields during changes in trial structure and across days. Time-cells exhibited sparse and dynamic fields that remapped in both cases. During task training, but not in untrained task exposure, time-cell ensembles increased in size, whereas odor-cell numbers remained stable. Over days, sequences drifted to new populations with cell activity progressively converging to a field and then diverging from it. Therefore, CA1 employs distinct regimes to encode external cues versus their variable temporal relationships, which may be necessary to construct maps of sequential experiences.

Keywords: CA1; Hippocampus; calcium imaging; drift; learning; odor; population dynamics; sequences; stability; time.

Published by Elsevier Inc.

Publication types

Research Support, N.I.H., Extramural
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Action Potentials
Animals
CA1 Region, Hippocampal / chemistry
CA1 Region, Hippocampal / cytology
CA1 Region, Hippocampal / physiology*
Cues*
Male
Memory, Short-Term / drug effects
Memory, Short-Term / physiology*
Mice
Mice, 129 Strain
Mice, Inbred C57BL
Mice, Transgenic
Microscopy, Fluorescence, Multiphoton / methods
Odorants*
Smell / drug effects
Smell / physiology*
Time Factors

Abstract

Publication types

MeSH terms

Grants and funding