Anterior thalamic high frequency band activity is coupled with theta oscillations at rest

ABSTRACT

Cross-frequency coupling (CFC) between slow and fast brain rhythms, in the form of phase–amplitude coupling (PAC), is proposed to enable the coordination of neural oscillatory activity required for cognitive processing. PAC has been identified in the neocortex and mesial temporal regions, varying according to the cognitive task being performed and also at rest. PAC has also been observed in the anterior thalamic nucleus (ATN) during memory processing. The thalamus is active during the resting state and has been proposed to be involved in switching between task-free cognitive states such as rest, in which attention is internally-focused, and externally-focused cognitive states, in which an individual engages with environmental stimuli. It is unknown whether PAC is an ongoing phenomenon during the resting state in the ATN, which is modulated during different cognitive states, or whether it only arises during the performance of specific tasks. We analyzed electrophysiological recordings of ATN activity during rest from seven patients who received thalamic electrodes implanted for treatment of pharmacoresistant focal epilepsy. PAC was identified between theta (4–6 Hz) phase and high frequency band (80–150 Hz) amplitude during rest in all seven patients, which diminished during engagement in tasks involving an external focus of attention. The findings are consistent with the proposal that theta–gamma coupling in the ATN is an ongoing phenomenon, which is modulated by task performance.

AUTHORS

• Catherine M. Sweeney-Reed

• Tino Zauhle

• Jürgen Voges

• Friedhelm Schmitt

• Lars Buentjen

• Viola Borchardt

• Hermann Hinrichs

• Hans-Jochen Heinze

• Michael D. Rugg

• Robert T. Knight

Date: 2017

DOI: 10.3389/fnhum.2017.00358

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Pre-stimulus thalamic theta power predicts human memory formation

ABSTRACT

Pre-stimulus theta (4–8 Hz) power in the hippocampus and neocortex predicts whether a memory for a subsequent event will be formed. Anatomical studies reveal thalamus-hippocampal connectivity, and lesion, neuroimaging, and electrophysiological studies show that memory processing involves the dorsomedial (DMTN) and anterior thalamic nuclei (ATN). The small size and deep location of these nuclei have limited real-time study of their activity, however, and it is unknown whether pre-stimulus theta power predictive of successful memory formation is also found in these subcortical structures. We recorded human electrophysiological data from the DMTN and ATN of 7 patients receiving deep brain stimulation for refractory epilepsy. We found that greater pre-stimulus theta power in the right DMTN was associated with successful memory encoding, predicting both behavioral outcome and post-stimulus correlates of successful memory formation. In particular, significant correlations were observed between right DMTN theta power and both frontal theta and right ATN gamma (32–50 Hz) phase alignment, and frontal-ATN theta-gamma cross-frequency coupling. We draw the following primary conclusions. Our results provide direct electrophysiological evidence in humans of a role for the DMTN as well as the ATN in memory formation. Furthermore, prediction of subsequent memory performance by pre-stimulus thalamic oscillations provides evidence that post-stimulus differences in thalamic activity that index successful and unsuccessful encoding reflect brain processes specifically underpinning memory formation. Finally, the findings broaden the understanding of brain states that facilitate memory encoding to include subcortical as well as cortical structures.

AUTHORS

• Catherine M. Sweeney-Reed

• Tino Zaehle

• Jürgen Voges

• Friedhelm Schmitt

• Lars Buentjen

• Klaus Kopitzki

• Alan Richardson-Klavehn

• Hermann Hinrichs

• Hans-Jochen Heinze

• Robert T. Knight

• Michael D. Rugg

Date: 2016

DOI: 10.1016/j.neuroimage.2016.05.042

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Thalamic theta phase alignment predicts human memory formation and anterior thalamic cross-frequency coupling

Authors:

• Catherine M. Sweeney-Reed

• Tino Zaehle

• Jürgen Voges

• Friedhelm Schmitt

• Lars Buentjen

• Klaus Kopitzki

• Hermann Hinrichs

• Hans-Jochen Heinze

• Michael D. Rugg

• Robert T. Knight

• Alan Richardson-Klavehn

Date: 2015

DOI: 10.7554/eLife.07578

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Abstract:

Previously we reported electrophysiological evidence for a role for the anterior thalamic nucleus (ATN) in human memory formation (Sweeney-Reed et al. 2014). Theta-gamma cross-frequency coupling (CFC) predicted successful memory formation, with the involvement of gamma oscillations suggesting memory-relevant local processing in the ATN. The importance of the theta frequency range in memory processing is well-established, and phase alignment of oscillations is considered to be necessary for synaptic plasticity. We hypothesized that theta phase alignment in the ATN would be necessary for memory encoding. Further analysis of the electrophysiological data reveal that phase alignment in the theta rhythm was greater during successful compared with unsuccessful encoding, and that this alignment was correlated with the CFC. These findings support an active processing role for the ATN during memory formation.

Corticothalamic phase synchrony and cross-frequency coupling predict human memory formation

Authors:

• Catherine M. Sweeney-Reed

• Tino Zaehle

• Jürgen Voges

• Friedhelm Schmitt

• Lars Buentjen

• Klaus Kopitzki

• Christine Esslinger

• Hermann Hinrichs

• Hans-Jochen Heinze

• Robert T. Knight

• Alan Richardson-Klavehn

Date: 2014

DOI: 10.7554/eLife.05352.001

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Abstract:

The anterior thalamic nucleus (ATN) is thought to play an important role in a brain network involving the hippocampus and neocortex, which enables human memories to be formed. However, its small size and location deep within the brain have impeded direct investigation in humans with non-invasive techniques. Here we provide direct evidence for a functional role for the ATN in memory formation from rare simultaneous human intrathalamic and scalp electroencephalogram (EEG) recordings from eight volunteering patients receiving intrathalamic electrodes implanted for the treatment of epilepsy, demonstrating real-time communication between neocortex and ATN during successful memory encoding. Neocortical-ATN theta oscillatory phase synchrony of local field potentials and neocortical-theta-to-ATN-gamma cross-frequency coupling during presentation of complex photographic scenes predicted later memory for the scenes, demonstrating a key role for the ATN in human memory encoding.

Phase-amplitude cross-frequency coupling in the human nucleus acumbens tracks action monitoring during cognitive control

Authors:

• S. Durschmid

• Tino Zaehle

• Klaus Kopitzki

• Jürgen Voges

• Friedhelm Schmitt

• Hans-Jochen Heinze

• Robert T. Knight

• Hermann Hinrichs

Date: 2013

DOI: 10.3389/fnhum.2013.00635

PubMed: 24586885

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Abstract:

The Nucleus Accumbens (NAcc) is an important structure for the transfer of information between cortical and subcortical structures, especially the prefrontal cortex and the hippocampus. However, the mechanism that allows the NAcc to achieve this integration is not well understood. Phase-amplitude cross-frequency coupling (PAC) of oscillations in different frequency bands has been proposed as an effective mechanism to form functional networks to optimize transfer and integration of information. Here we assess PAC between theta and high gamma oscillations as a potential mechanism that facilitates motor adaptation. To address this issue we recorded intracranial field potentials directly from the bilateral human NAcc in three patients while they performed a motor learning task that varied in the level of cognitive control needed to perform the task. As in rodents, PAC was observable in the human NAcc, transiently occurring contralateral to a movement following the motor response. Importantly, PAC correlated with the level of cognitive control needed to monitor the action performed. This functional relation indicates that the NAcc is engaged in action monitoring and supports the evaluation of motor programs during adaptive behavior by means of PAC.