Awake ripples enhance emotional memory encoding in the human brain

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.

Authors:

• Haoxin Zhang

• Ivan Skelin

• Shiting Ma

• Michelle Paff

• Lilit Mnatsakanyan

• Michael A. Yassa

• Robert T. Knight

• Jack J. Lin

Date: 2024

DOI: https://doi.org/10.1038/s41467-023-44295-8

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Bidirectional prefrontal-hippocampal dynamics organize information transfer during sleep in humans

Abstract:

How are memories transferred from short-term to long-term storage? Systems-level memory consolidation is thought to be dependent on the coordinated interplay of cortical slow waves, thalamo-cortical sleep spindles and hippocampal ripple oscillations. However, it is currently unclear how the selective interaction of these cardinal sleep oscillations is organized to support information reactivation and transfer. Here, using human intracranial recordings, we demonstrate that the prefrontal cortex plays a key role in organizing the ripple-mediated information transfer during non-rapid eye movement (NREM) sleep. We reveal a temporally precise form of coupling between prefrontal slow-wave and spindle oscillations, which actively dictates the hippocampal-neocortical dialogue and information transfer. Our results suggest a model of the human sleeping brain in which rapid bidirectional interactions, triggered by the prefrontal cortex, mediate hippocampal activation to optimally time subsequent information transfer to the neocortex during NREM sleep.

Authors:

• Randolph F Helfrich

• Janna D Lendner

• Bryce A Mander

• Heriberto Guillen

• Michelle Paff

• Lilit Mnatsakanyan

• Sumeet Vadera

• Matthew P Walker

• Jack J Lin

• Robert T Knight

Date: 2019

DOI: https://doi.org/10.1038/s41467-019-11444-x

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Hippocampal CA1 gamma power predicts the precision of spatial memory judgments

Abstract:

The hippocampus plays a critical role in spatial memory. However, the exact neural mechanisms underlying high-fidelity spatial memory representations are unknown. We report findings from presurgical epilepsy patients with bilateral hippocampal depth electrodes performing an object-location memory task that provided a broad range of spatial memory precision. During encoding, patients were shown a series of objects along the circumference of an invisible circle. At test, the same objects were shown at the top of the circle (0°), and patients used a dial to move the object to its location shown during encoding. Angular error between the correct location and the indicated location was recorded as a continuous measure of performance. By registering pre- and postimplantation MRI scans, we were able to localize the electrodes to specific hippocampal subfields. We found a correlation between increased gamma power, thought to reflect local excitatory activity, and the precision of spatial memory retrieval in hippocampal CA1 electrodes. Additionally, we found a similar relationship between gamma power and memory precision in the dorsolateral prefrontal cortex and a directional relationship between activity in this region and in the CA1, suggesting that the dorsolateral prefrontal cortex is involved in postretrieval processing. These results indicate that local processing in hippocampal CA1 and dorsolateral prefrontal cortex supports high-fidelity spatial memory representations.

Authors:

• Rebecca F. Stevenson

• Jie Zheng

• Lilit Mnatsakanyan

• Sumeet Vadera

• Robert T. Knight

• Jack J. Lin

• Michael A. Yassa

Date: 2018

DOI: 10.1073/pnas.1805724115

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

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 are not well understood. Here, we used intracranial depth electrode 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, we show that overgeneralization is associated with alpha band (7-13 Hz)-coordinated unidirectional influence from the amygdala to the hippocampus. These findings imply that alpha band synchrony may trigger overgeneralization of similar emotional events via amygdala-hippocampal directional coupling, which suggests a target for the treatment of psychiatric conditions such as post-traumatic stress disorder, where aversive memories are often overgeneralized.

AUTHORS

• 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

Date: 2018

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Amygdala-hippocampal dynamics during salient information processing

ABSTRACT

Recognizing motivationally salient information is critical to guiding behaviour. The amygdala and hippocampus are thought to support this operation, but the circuit-level mechanism of this interaction is unclear. We used direct recordings in the amygdala and hippocampus from human epilepsy patients to examine oscillatory activity during processing of fearful faces compared with neutral landscapes. We report high gamma (70–180 Hz) activation for fearful faces with earlier stimulus evoked onset in the amygdala compared with the hippocampus. Attending to fearful faces compared with neutral landscape stimuli enhances low-frequency coupling between the amygdala and the hippocampus. The interaction between the amygdala and hippocampus is largely unidirectional, with theta/alpha oscillations in the amygdala modulating hippocampal gamma activity. Granger prediction, phase slope index and phase lag analysis corroborate this directional coupling. These results demonstrate that processing emotionally salient events in humans engages an amygdala-hippocampal network, with the amygdala influencing hippocampal dynamics during fear processing.

AUTHORS

• Robert T. Knight

• Avgusta Shestyuk

• Kristopher L. Anderson

• Jie Zheng

• Stephanie L. Leal

• Gultekin Gulsen

• Lilit Mnatsakanyan

• Sumeet Vadera

• Frank P.K. Hsu

• Michael A. Yassa

• Jack J. Lin

Date: 2017

DOI: 10.1038/ncomms14413

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