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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Patients with basal ganglia damage show preserved learning in an economic game

Abstract:

Both basal ganglia (BG) and orbitofrontal cortex (OFC) have been widely implicated in social and non-social decision-making. However, unlike OFC damage, BG pathology is not typically associated with disturbances in social functioning. Here we studied the behavior of patients with focal lesions to either BG or OFC in a multi-strategy competitive game known to engage these regions. We find that whereas OFC patients are significantly impaired, BG patients show intact learning in the economic game. By contrast, when information about the strategic context is absent, both cohorts are significantly impaired. Computational modeling further shows a preserved ability in BG patients to learn by anticipating and responding to the behavior of others using the strategic context. These results suggest that apparently divergent findings on BG contribution to social decision-making may instead reflect a model where higher-order learning processes are dissociable from trial-and-error learning, and can be preserved despite BG damage.

Authors:

• Lusha Zhu

• Yaomin Jiang

• Donatella Scabini

• Robert T. Knight

• Ming Hsu

Date: 2019

DOI: https://doi.org/10.1038/s41467-019-08766-1

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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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Rapid tuning shifts in human auditory cortex enhance speech intelligibility

ABSTRACT

Experience shapes our perception of the world on a moment-to-moment basis. This robust perceptual effect of experience parallels a change in the neural representation of stimulus features, though the nature of this representation and its plasticity are not well-understood. Spectrotemporal receptive field (STRF) mapping describes the neural response to acoustic features, and has been used to study contextual effects on auditory receptive fields in animal models. We performed a STRF plasticity analysis on electrophysiological data from recordings obtained directly from the human auditory cortex. Here, we report rapid, automatic plasticity of the spectrotemporal response of recorded neural ensembles, driven by previous experience with acoustic and linguistic information, and with a neurophysiological effect in the sub-second range. This plasticity reflects increased sensitivity to spectrotemporal features, enhancing the extraction of more speech-like features from a degraded stimulus and providing the physiological basis for the observed ‘perceptual enhancement’ in understanding speech.

AUTHORS

• Chris Holdgraf

• Wendy de Heer

• Brian Pasley

• Jochem W. Rieger

• Nathan E. Crone

• Jack J. Lin

• Robert T. Knight

• Frédéric E. Theunissen

Date: 2016

DOI: 10.1038/ncomms13654

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