A hypothalamic novelty signal modulates hippocampal memory

Shuo Chen (), Linmeng He, Arthur J. Y. Huang, Roman Boehringer, Vincent Robert, Marie E. Wintzer, Denis Polygalov, Adam Z. Weitemier, Yanqiu Tao, Mingxiao Gu, Steven J. Middleton, Kana Namiki, Hiroshi Hama, Ludivine Therreau, Vivien Chevaleyre, Hiroyuki Hioki, Atsushi Miyawaki, Rebecca A. Piskorowski and Thomas J. McHugh ()
Additional contact information
Shuo Chen: RIKEN Center for Brain Science
Linmeng He: RIKEN Center for Brain Science
Arthur J. Y. Huang: RIKEN Center for Brain Science
Roman Boehringer: RIKEN Center for Brain Science
Vincent Robert: Université de Paris, INSERM UMRS1266
Marie E. Wintzer: RIKEN Center for Brain Science
Denis Polygalov: RIKEN Center for Brain Science
Adam Z. Weitemier: RIKEN Center for Brain Science
Yanqiu Tao: RIKEN Center for Brain Science
Mingxiao Gu: RIKEN Center for Brain Science
Steven J. Middleton: RIKEN Center for Brain Science
Kana Namiki: RIKEN Center for Brain Science
Hiroshi Hama: RIKEN Center for Brain Science
Ludivine Therreau: Université de Paris, INSERM UMRS1266
Vivien Chevaleyre: Université de Paris, INSERM UMRS1266
Hiroyuki Hioki: Juntendo University Graduate School of Medicine
Atsushi Miyawaki: RIKEN Center for Brain Science
Rebecca A. Piskorowski: Université de Paris, INSERM UMRS1266
Thomas J. McHugh: RIKEN Center for Brain Science

Nature, 2020, vol. 586, issue 7828, 270-274

Abstract: Abstract The ability to recognize information that is incongruous with previous experience is critical for survival. Novelty signals have therefore evolved in the mammalian brain to enhance attention, perception and memory1,2. Although the importance of regions such as the ventral tegmental area3,4 and locus coeruleus5 in broadly signalling novelty is well-established, these diffuse monoaminergic transmitters have yet to be shown to convey specific information on the type of stimuli that drive them. Whether distinct types of novelty, such as contextual and social novelty, are differently processed and routed in the brain is unknown. Here we identify the supramammillary nucleus (SuM) as a novelty hub in the hypothalamus6. The SuM region is unique in that it not only responds broadly to novel stimuli, but also segregates and selectively routes different types of information to discrete cortical targets—the dentate gyrus and CA2 fields of the hippocampus—for the modulation of mnemonic processing. Using a new transgenic mouse line, SuM-Cre, we found that SuM neurons that project to the dentate gyrus are activated by contextual novelty, whereas the SuM–CA2 circuit is preferentially activated by novel social encounters. Circuit-based manipulation showed that divergent novelty channelling in these projections modifies hippocampal contextual or social memory. This content-specific routing of novelty signals represents a previously unknown mechanism that enables the hypothalamus to flexibly modulate select components of cognition.

Date: 2020
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DOI: 10.1038/s41586-020-2771-1

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