Increased flexibility of CA3 memory representations following environmental enrichment

Silvia Ventura; Stephen Duncan; James A Ainge

doi:10.1016/j.cub.2024.03.054

Increased flexibility of CA3 memory representations following environmental enrichment

Curr Biol. 2024 May 6;34(9):2011-2019.e7. doi: 10.1016/j.cub.2024.03.054. Epub 2024 Apr 17.

Authors

Silvia Ventura¹, Stephen Duncan², James A Ainge³

Affiliations

¹ School of Psychology & Neuroscience, University of St. Andrews, St. Mary's Quad, South Street, St. Andrews, Fife, Scotland KY16 9JP, UK.
² School of Psychology & Neuroscience, University of St. Andrews, St. Mary's Quad, South Street, St. Andrews, Fife, Scotland KY16 9JP, UK; School of Psychological & Brain Sciences, Indiana University, 1101 E 10th Street, Bloomington, IN 47405, USA.
³ School of Psychology & Neuroscience, University of St. Andrews, St. Mary's Quad, South Street, St. Andrews, Fife, Scotland KY16 9JP, UK. Electronic address: jaa7@st-andrews.ac.uk.

PMID: 38636511
DOI: 10.1016/j.cub.2024.03.054

Abstract

Environmental enrichment (EE) improves memory, particularly the ability to discriminate similar past experiences.¹^,²^,³^,⁴^,⁵^,⁶ The hippocampus supports this ability via pattern separation, the encoding of similar events using dissimilar memory representations.⁷ This is carried out in the dentate gyrus (DG) and CA3 subfields.⁸^,⁹^,¹⁰^,¹¹^,¹² Upregulation of adult neurogenesis in the DG improves memory through enhanced pattern separation.¹^,²^,³^,⁴^,⁵^,⁶^,¹¹^,¹³^,¹⁴^,¹⁵^,¹⁶ Adult-born granule cells (abGCs) in DG are suggested to contribute to pattern separation by driving inhibition in regions such as CA3,¹³^,¹⁴^,¹⁵^,¹⁶^,¹⁷^,¹⁸ leading to sparser, nonoverlapping representations of similar events (although a role for abGCs in driving excitation in the hippocampus has also been reported¹⁶). Place cells in the hippocampus contribute to pattern separation by remapping to spatial and contextual alterations to the environment.¹⁹^,²⁰^,²¹^,²²^,²³^,²⁴^,²⁵^,²⁶^,²⁷ How spatial responses in CA3 are affected by EE and input from increased numbers of abGCs in DG is, however, unknown. Here, we investigate the neural mechanisms facilitating improved memory following EE using associative recognition memory tasks that model the automatic and integrative nature of episodic memory. We find that EE-dependent improvements in difficult discriminations are related to increased neurogenesis and sparser memory representations across the hippocampus. Additionally, we report for the first time that EE changes how CA3 place cells discriminate similar contexts. CA3 place cells of enriched rats show greater spatial tuning, increased firing rates, and enhanced remapping to contextual changes. These findings point to more precise and flexible CA3 memory representations in enriched rats, which provides a putative mechanism for EE-dependent improvements in fine memory discrimination.

Keywords: context; dentate gyrus; episodic memory; hippocampus; neurogenesis; object recognition; pattern separation; place cell; rat; remapping.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
CA3 Region, Hippocampal* / physiology
Dentate Gyrus / physiology
Environment*
Male
Memory / physiology
Neurogenesis / physiology
Rats
Rats, Long-Evans