Sequential activity of CA1 hippocampal cells constitutes a temporal memory map for associative learning in mice

Ming Ma; Fabio Simoes de Souza; Gregory L Futia; Sean R Anderson; Jose Riguero; Daniel Tollin; Arianna Gentile-Polese; Jonathan P Platt; Kira Steinke; Naoki Hiratani; Emily A Gibson; Diego Restrepo

doi:10.1016/j.cub.2024.01.021

Sequential activity of CA1 hippocampal cells constitutes a temporal memory map for associative learning in mice

Curr Biol. 2024 Feb 26;34(4):841-854.e4. doi: 10.1016/j.cub.2024.01.021. Epub 2024 Feb 6.

Authors

Affiliations

¹ Department of Cell and Developmental Biology, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USA.
² Department of Cell and Developmental Biology, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USA; Center for Mathematics, Computation and Cognition, Federal University of ABC, Sao Bernardo do Campo 09606-045, SP, Brazil.
³ Department of Bioengineering, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USA.
⁴ Department of Physiology and Biophysics, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USA.
⁵ Department of Physiology and Biophysics, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USA; Neuroscience Graduate Program, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USA.
⁶ Department of Neurosurgery, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USA.
⁷ Integrated Physiology Graduate Program, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USA.
⁸ Department of Neuroscience, Washington University, St. Louis, MO 63110, USA.
⁹ Department of Bioengineering, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USA; Neuroscience Graduate Program, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USA.
¹⁰ Department of Cell and Developmental Biology, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USA; Neuroscience Graduate Program, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USA. Electronic address: diego.restrepo@cuanschutz.edu.

PMID: 38325376
DOI: 10.1016/j.cub.2024.01.021

Abstract

Sequential neural dynamics encoded by time cells play a crucial role in hippocampal function. However, the role of hippocampal sequential neural dynamics in associative learning is an open question. We used two-photon Ca²⁺ imaging of dorsal CA1 (dCA1) neurons in the stratum pyramidale (SP) in head-fixed mice performing a go-no go associative learning task to investigate how odor valence is temporally encoded in this area of the brain. We found that SP cells responded differentially to the rewarded or unrewarded odor. The stimuli were decoded accurately from the activity of the neuronal ensemble, and accuracy increased substantially as the animal learned to differentiate the stimuli. Decoding the stimulus from individual SP cells responding differentially revealed that decision-making took place at discrete times after stimulus presentation. Lick prediction decoded from the ensemble activity of cells in dCA1 correlated linearly with lick behavior. Our findings indicate that sequential activity of SP cells in dCA1 constitutes a temporal memory map used for decision-making in associative learning. VIDEO ABSTRACT.

Keywords: CA1; associative learning; decision-making; decoding; go-no go; hippocampus; olfactory; time cells.

Publication types

Video-Audio Media

MeSH terms

Animals
CA1 Region, Hippocampal* / physiology
Conditioning, Classical
Hippocampus*
Learning
Mice
Neurons / physiology