Multiplexing of Theta and Alpha Rhythms in the Amygdala-Hippocampal Circuit Supports Pattern Separation of Emotional Information

Jie Zheng; Rebecca F Stevenson; Bryce A Mander; Lilit Mnatsakanyan; Frank P K Hsu; Sumeet Vadera; Robert T Knight; Michael A Yassa; Jack J Lin

doi:10.1016/j.neuron.2019.03.025

Multiplexing of Theta and Alpha Rhythms in the Amygdala-Hippocampal Circuit Supports Pattern Separation of Emotional Information

Neuron. 2019 May 22;102(4):887-898.e5. doi: 10.1016/j.neuron.2019.03.025. Epub 2019 Apr 9.

Authors

Jie Zheng¹, Rebecca F Stevenson², Bryce A Mander³, Lilit Mnatsakanyan⁴, Frank P K Hsu⁵, Sumeet Vadera⁵, Robert T Knight⁶, Michael A Yassa⁷, Jack J Lin⁸

Affiliations

¹ Department of Biomedical Engineering, University of California, Irvine, Irvine, CA 92697, USA.
² Department of Neurobiology and Behavior, University of California, Irvine, Irvine, CA 92697, USA; Center for the Neurobiology of Learning and Memory, University of California, Irvine, Irvine, CA 92697, USA.
³ Center for the Neurobiology of Learning and Memory, University of California, Irvine, Irvine, CA 92697, USA; Department of Psychiatry and Human Behavior, University of California, Irvine, Irvine, CA 92697, USA.
⁴ Comprehensive Epilepsy Program, Department of Neurology, University of California, Irvine, Irvine, CA 92868, USA.
⁵ Department of Neurological Surgery, University of California, Irvine, Irvine, CA 92868, USA.
⁶ Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, CA 94720, USA; Department of Psychology, University of California, Berkeley, Berkeley, CA 94720, USA.
⁷ Department of Neurobiology and Behavior, University of California, Irvine, Irvine, CA 92697, USA; Center for the Neurobiology of Learning and Memory, University of California, Irvine, Irvine, CA 92697, USA; Department of Psychiatry and Human Behavior, University of California, Irvine, Irvine, CA 92697, USA. Electronic address: myassa@uci.edu.
⁸ Department of Biomedical Engineering, University of California, Irvine, Irvine, CA 92697, USA; Center for the Neurobiology of Learning and Memory, University of California, Irvine, Irvine, CA 92697, USA; Comprehensive Epilepsy Program, Department of Neurology, University of California, Irvine, Irvine, CA 92868, USA. Electronic address: linjj@uci.edu.

Abstract

How do we remember emotional events? While emotion often leads to vivid recollection, the precision of emotional memories can be degraded, especially when discriminating among overlapping experiences in memory (i.e., pattern separation). Communication between the amygdala and the hippocampus has been proposed to support emotional memory, but the exact neural mechanisms remain unclear. Here, we used intracranial recordings in pre-surgical epilepsy patients to show that successful pattern separation of emotional stimuli is associated with theta band (3-7 Hz)-coordinated bidirectional interactions between the amygdala and the hippocampus. In contrast, discrimination errors (i.e., failure to discriminate similar stimuli) were associated with alpha band (7-13 Hz)-coordinated unidirectional influence from the amygdala to the hippocampus. These findings imply that alpha band synchrony may impair discrimination of similar emotional events via the amygdala-hippocampal directional coupling, which suggests a target for treatments of psychiatric conditions such as post-traumatic stress disorder, in which aversive experiences are often overgeneralized.

Keywords: alpha; amygdala; emotional memory; hippocampus; memory generalization; oscillations; pattern separation; theta.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Adult
Alpha Rhythm / physiology*
Amygdala / physiology*
Discrimination, Psychological
Electrocorticography
Electroencephalography Phase Synchronization
Emotions*
Female
Hippocampus / physiology*
Humans
Male
Memory
Memory, Episodic*
Middle Aged
Neural Pathways / physiology
Theta Rhythm / physiology*
Young Adult

Abstract

Publication types

MeSH terms

Grants and funding