Coupling between slow-waves and sharp-wave ripples organizes distributed neural activity during sleep in humans

Abstract:

Hippocampal-dependent memory consolidation during sleep is hypothesized to depend on the synchronization of distributed neuronal ensembles, organized by the hippocampal sharp-wave ripples (SWRs, 80-150 Hz) and subcortical/cortical slow-waves (0.5-4 Hz). However, the precise role of SWR-slow-wave interactions in synchronizing subcortical/cortical neuronal activity is unclear. Here, we leverage intracranial electrophysiological recordings from the human hippocampus, amygdala, temporal and frontal cortices, to examine activity modulation and cross-regional coordination during SWRs. Hippocampal SWRs are associated with widespread modulation of high frequency activity (HFA; 70-200 Hz) a measure of local neuronal activation. This peri-SWR HFA modulation is predicted by the coupling between hippocampal SWRs and local subcortical/cortical slow-waves. Finally, local cortical slow-wave phase offsets during SWRs predicted functional connectivity between the frontal and temporal cortex. These findings suggest a selection mechanism wherein hippocampal SWR and cortical slow-wave synchronization governs the transient engagement of distributed neuronal populations supporting hippocampal-dependent memory consolidation.

Authors:

• Ivan Skelin

• Haoxin Zhang

• Jie Zheng

• Shiting Ma

• Bryce A Mander

• Olivia Kim Mcmanus

• Sumeet Vadera

• Robert T Knight

• Bruce L McNaughton

• Jack J Lin

Date: 2020

DOI: https://doi.org/10.1101/2020.05.24.113480

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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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