Specific exercise patterns generate an epigenetic molecular memory window that drives long-term memory formation and identifies ACVR1C as a bidirectional regulator of memory in mice

Ashley A. Keiser, Tri N. Dong, Enikö A. Kramár, Christopher W. Butler, Siwei Chen, Dina P. Matheos, Jacob S. Rounds, Alyssa Rodriguez, Joy H. Beardwood, Agatha S. Augustynski, Ameer Al-Shammari, Yasaman Alaghband, Vanessa Alizo Vera, Nicole C. Berchtold, Sharmin Shanur, Pierre Baldi, Carl W. Cotman and Marcelo A. Wood ()
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Ashley A. Keiser: University of California Irvine
Tri N. Dong: University of California Irvine
Enikö A. Kramár: University of California Irvine
Christopher W. Butler: University of California, Irvine
Siwei Chen: University of California, Irvine
Dina P. Matheos: University of California Irvine
Jacob S. Rounds: University of California Irvine
Alyssa Rodriguez: University of California Irvine
Joy H. Beardwood: University of California Irvine
Agatha S. Augustynski: University of California Irvine
Ameer Al-Shammari: University of California Irvine
Yasaman Alaghband: University of California Irvine
Vanessa Alizo Vera: University of California Irvine
Nicole C. Berchtold: University of California, Irvine
Sharmin Shanur: University of California Irvine
Pierre Baldi: University of California, Irvine
Carl W. Cotman: University of California, Irvine
Marcelo A. Wood: University of California Irvine

Nature Communications, 2024, vol. 15, issue 1, 1-16

Abstract: Abstract Exercise has beneficial effects on cognition throughout the lifespan. Here, we demonstrate that specific exercise patterns transform insufficient, subthreshold training into long-term memory in mice. Our findings reveal a potential molecular memory window such that subthreshold training within this window enables long-term memory formation. We performed RNA-seq on dorsal hippocampus and identify genes whose expression correlate with conditions in which exercise enables long-term memory formation. Among these genes we found Acvr1c, a member of the TGF ß family. We find that exercise, in any amount, alleviates epigenetic repression at the Acvr1c promoter during consolidation. Additionally, we find that ACVR1C can bidirectionally regulate synaptic plasticity and long-term memory in mice. Furthermore, Acvr1c expression is impaired in the aging human and mouse brain, as well as in the 5xFAD mouse model, and over-expression of Acvr1c enables learning and facilitates plasticity in mice. These data suggest that promoting ACVR1C may protect against cognitive impairment.

Date: 2024
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DOI: 10.1038/s41467-024-47996-w

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