Awake ripples enhance emotional memory encoding in the human brain

Haoxin Zhang; Ivan Skelin; Shiting Ma; Michelle Paff; Lilit Mnatsakanyan; Michael A Yassa; Robert T Knight; Jack J Lin

doi:10.1038/s41467-023-44295-8

Awake ripples enhance emotional memory encoding in the human brain

Nat Commun. 2024 Jan 3;15(1):215. doi: 10.1038/s41467-023-44295-8.

Authors

Haoxin Zhang^#^{1

2}, Ivan Skelin^#^{3

4}, Shiting Ma⁵, Michelle Paff⁶, Lilit Mnatsakanyan⁵, Michael A Yassa^{5

7

8}, Robert T Knight^{9

10}, Jack J Lin^{11

12}

Affiliations

¹ Department of Neurology, University of California Irvine, Irvine, 92603, CA, USA. haoxinz1@uci.edu.
² Department of Biomedical Engineering, University of California Irvine, Irvine, 92603, CA, USA. haoxinz1@uci.edu.
³ Krembil Brain Institute, Toronto Western Hospital, Toronto, Ontario, M5T 1M8, Canada.
⁴ Department Center for Advancing Neurotechnological Innovation to Application, Toronto, Ontario, M5G 2A2, Canada.
⁵ Department of Neurology, University of California Irvine, Irvine, 92603, CA, USA.
⁶ Department of Neurosurgery, University of California Irvine, Irvine, 92603, CA, USA.
⁷ Department of Neurobiology and Behavior, University of California Irvine, Irvine, 92697, CA, USA.
⁸ Department of Psychiatry and Human Behavior, University of California Irvine, Irvine, 92697, CA, USA.
⁹ Department of Psychology, University of California Berkeley, Berkeley, 94720, CA, USA.
¹⁰ Helen Wills Neuroscience Institute, University of California Berkeley, Berkeley, 94720, CA, USA.
¹¹ Department of Neurology, School of Medicine, University of California Davis, Sacramento, 95817, CA, USA. jajlin@ucdavis.edu.
¹² Center for Mind and Brain, University of California Davis, Davis, 95618, CA, USA. jajlin@ucdavis.edu.

^# Contributed equally.

Abstract

Enhanced memory for emotional experiences is hypothesized to depend on amygdala-hippocampal interactions during memory consolidation. Here we show using intracranial recordings from the human amygdala and the hippocampus during an emotional memory encoding and discrimination task increased awake ripples after encoding of emotional, compared to neutrally-valenced stimuli. Further, post-encoding ripple-locked stimulus similarity is predictive of later memory discrimination. Ripple-locked stimulus similarity appears earlier in the amygdala than in hippocampus and mutual information analysis confirms amygdala influence on hippocampal activity. Finally, the joint ripple-locked stimulus similarity in the amygdala and hippocampus is predictive of correct memory discrimination. These findings provide electrophysiological evidence that post-encoding ripples enhance memory for emotional events.

MeSH terms

Amygdala / physiology
Electrophysiological Phenomena
Emotions
Hippocampus / physiology
Humans
Memory Consolidation* / physiology
Wakefulness* / physiology

Abstract

MeSH terms

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