The role of the anterior nuclei of the thalamus in human memory processing

Abstract:

Extensive neuroanatomical connectivity between the anterior thalamic nuclei (ATN) and hippocampus and neocortex renders them well-placed for a role in memory processing, and animal, lesion, and neuroimaging studies support such a notion. The deep location and small size of the ATN have precluded their real-time electrophysiological investigation during human memory processing. However, ATN electrophysiological recordings from patients receiving electrodes implanted for deep brain stimulation for pharmacoresistant focal epilepsy have enabled high temporal resolution study of ATN activity. Theta frequency synchronization of ATN and neocortical oscillations during successful memory encoding, enhanced phase alignment, and coupling between ATN local gamma frequency activity and frontal neocortical and ATN theta oscillations provide evidence of an active role for the ATN in memory encoding, potentially integrating information from widespread neocortical sources. Greater coupling of a broader gamma frequency range with theta oscillations at rest than during memory encoding provides additional support for the hypothesis that the ATN play a role in selecting local, task-relevant high frequency activity associated with particular features of a memory trace.

Authors:

• Catherine M Sweeney-Reed

• Lars Buentjen

• Jürgen Voges

• Friedhelm C Schmitt

• Tino Zaehle

• Julia WY Kam

• Jörn Kaufmann

• Hans-Jochen Heinze

• Hermann Hinrichs

• Robert T Knight

• Michael D Rugg

Date: 2021

DOI: https://doi.org/10.1016/j.neubiorev.2021.02.046

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Frontotemporal Regulation of Subjective Value to Suppress Impulsivity in Intertemporal Choices

Abstract:

Impulsive decisions arise from preferring smaller but sooner rewards compared with larger but later rewards. How neural activity and attention to choice alternatives contribute to reward decisions during temporal discounting is not clear. Here we probed (1) attention to and (2) neural representation of delay and reward information in humans (both sexes) engaged in choices. We studied behavioral and frequency-specific dynamics supporting impulsive decisions on a fine-grained temporal scale using eye tracking and MEG recordings. In one condition, participants had to decide for themselves but pretended to decide for their best friend in a second prosocial condition, which required perspective taking. Hence, conditions varied in the value for themselves versus that pretending to choose for another person. Stronger impulsivity was reliably found across three independent groups for prosocial decisions. Eye tracking revealed a systematic shift of attention from the delay to the reward information and differences in eye tracking between conditions predicted differences in discounting. High-frequency activity (175-250 Hz) distributed over right frontotemporal sensors correlated with delay and reward information in consecutive temporal intervals for high value decisions for oneself but not the friend. Collectively, the results imply that the high-frequency activity recorded over frontotemporal MEG sensors plays a critical role in choice option integration.

Authors:

• Stefan Dürschmid

• Andre Maric

• Marcel S Kehl

• Robert T Knight

• Hermann Hinrichs

• Hans-Jochen Heinze

Date: 2021

DOI: https://doi.org/10.1523/JNEUROSCI.1196-20.2020

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Comparison between a wireless dry electrode EEG system with a conventional wired wet electrode EEG system for clinical applications

Abstract:

Dry electrode electroencephalogram (EEG) recording combined with wireless data transmission offers an alternative tool to conventional wet electrode EEG systems. However, the question remains whether the signal quality of dry electrode recordings is comparable to wet electrode recordings in the clinical context. We recorded the resting state EEG (rsEEG), the visual evoked potentials (VEP) and the visual P300 (P3) from 16 healthy subjects (age range: 26–79 years) and 16 neurological patients who reported subjective memory impairment (age range: 50–83 years). Each subject took part in two recordings on different days, one with 19 dry electrodes and another with 19 wet electrodes. They reported their preferred EEG system. Comparisons of the rsEEG recordings were conducted qualitatively by independent visual evaluation by two neurologists blinded to the EEG system used and quantitatively by spectral analysis of the rsEEG. The P100 visual evoked potential (VEP) and P3 event-related potential (ERP) were compared in terms of latency, amplitude and pre-stimulus noise. The majority of subjects preferred the dry electrode headset. Both neurologists reported that all rsEEG traces were comparable between the wet and dry electrode headsets. Absolute Alpha and Beta power during rest did not statistically differ between the two EEG systems (p > 0.05 in all cases). However, Theta and Delta power was slightly higher with the dry electrodes (p = 0.0004 for Theta and p < 0.0001 for Delta). For ERPs, the mean latencies and amplitudes of the P100 VEP and P3 ERP showed comparable values (p > 0.10 in all cases) with a similar spatial distribution for both wet and dry electrode systems. These results suggest that the signal quality, ease of set-up and portability of the dry electrode EEG headset used in our study comply with the needs of clinical applications.

Authors:

• Hermann Hinrichs

• Michael Scholz

• Anne Katrin Baum

• Julia WY Kam

• Robert T Knight

• Hans-Jochen Heinze

Date: 2020

DOI: https://doi.org/10.1038/s41598-020-62154-0

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Systematic comparison between a wireless EEG system with dry electrodes and a wired EEG system with wet electrodes

Abstract:

Recent advances in dry electrodes technology have facilitated the recording of EEG in situations not previously possible, thanks to the relatively swift electrode preparation and avoidance of applying gel to subject's hair. However, to become a true alternative, these systems should be compared to state-of-the-art wet EEG systems commonly used in clinical or research applications. In our study, we conducted a systematic comparison of electrodes application speed, subject comfort, and most critically electrophysiological signal quality between the conventional and wired Biosemi EEG system using wet active electrodes and the compact and wireless F1 EEG system consisting of dry passive electrodes. All subjects (n = 27) participated in two recording sessions on separate days, one with the wet EEG system and one with the dry EEG system, in which the session order was counterbalanced across subjects. In each session, we recorded their EEG during separate rest periods with eyes open and closed followed by two versions of a serial visual presentation target detection task. Each task component allows for a neural measure reflecting different characteristics of the data, including spectral power in canonical low frequency bands, event-related potential components (specifically, the P3b), and single trial classification based on machine learning. The performance across the two systems was similar in most measures, including the P3b amplitude and topography, as well as low frequency (theta, alpha, and beta) spectral power at rest. Both EEG systems performed well above chance in the classification analysis, with a marginal advantage of the wet system over the dry. Critically, all aforementioned electrophysiological metrics showed significant positive correlations (r = 0.54–0.89) between the two EEG systems. This multitude of measures provides a comprehensive comparison that captures different aspects of EEG data, including temporal precision, frequency domain as well as multivariate patterns of activity. Taken together, our results indicate that the dry EEG system used in this experiment can effectively record electrophysiological measures commonly used across the research and clinical contexts with comparable quality to the conventional wet EEG system.

Authors:

• Julia W.Y. Kam

• Sandon Griffin

• Alan Shen

• Shawn Patel

• Hermann Hinrichs

• Hans-Jochen Heinze

• Leon Y. Deouell

• Robert T. Knight

Date: 2019

DOI: 10.1016/j.neuroimage.2018.09.012

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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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Hierarchy of prediction errors for auditory events in human temporal and frontal cortex

ABSTRACT

Predictive coding theories posit that neural networks learn statistical regularities in the environment for comparison with actual outcomes, signaling a prediction error (PE) when sensory deviation occurs. PE studies in audition have capitalized on low-frequency event-related potentials (LF-ERPs), such as the mismatch negativity. However, local cortical activity is well-indexed by higher-frequency bands [high-γ band (Hγ): 80–150 Hz]. We compared patterns of human Hγ and LF-ERPs in deviance detection using electrocorticographic recordings from subdural electrodes over frontal and temporal cortices. Patients listened to trains of task-irrelevant tones in two conditions differing in the predictability of a deviation from repetitive background stimuli (fully predictable vs. unpredictable deviants). We found deviance-related responses in both frequency bands over lateral temporal and inferior frontal cortex, with an earlier latency for Hγ than for LF-ERPs. Critically, frontal Hγ activity but not LF-ERPs discriminated between fully predictable and unpredictable changes, with frontal cortex sensitive to unpredictable events. The results highlight the role of frontal cortex and Hγ activity in deviance detection and PE generation.

AUTHORS

• S. Durschmid

• Erik Edwards

• Christoph Reichert

• Callum Dewar

• Hermann Hinrichs

• Hans-Jochen Heinze

• Heidi E. Kirsch

• Sarang S. Dalal

• Leon Y. Deouell

• Robert T. Knight

Date: 2016

DOI: 10.1073/pnas.1525030113

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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.

Sensory Deviancy Detection Measured Directly Within the Human Nucleus Accumbens

Authors:

• S. Durschmid

• Tino Zauhle

• Hermann Hinrichs

• Hans-Jochen Heinze

• Jürgen Voges

• Marta Garrido

• Raymond J. Dolan

• Robert T. Knight

Date: 2015

DOI: 10.1093/cercor/bhu304

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Abstract:

Rapid changes in the environment evoke a comparison between expectancy and actual outcome to inform optimal subsequent behavior. The nucleus accumbens (NAcc), a key interface between the hippocampus and neocortical regions, is a candidate region for mediating this comparison. Here, we report event-related potentials obtained from the NAcc using direct intracranial recordings in 5 human participants while they listened to trains of auditory stimuli differing in their degree of deviation from repetitive background stimuli. NAcc recordings revealed an early mismatch signal (50–220 ms) in response to all deviants. NAcc activity in this time window was also sensitive to the statistics of stimulus deviancy, with larger amplitudes as a function of the level of deviancy. Importantly, this NAcc mismatch signal also predicted generation of longer latency scalp potentials (300–400 ms). The results provide direct human evidence that the NAcc is a key component of a network engaged in encoding statistics of the sensory environmental.

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.

Decoding spectrotemporal features of overt and covert speech from the human cortex

Authors:

• Stéphanie Martin

• Peter Brunner

• Chris Holdgraf

• Hans-Jochen Heinze

• Nathan E. Crone

• Jochem W. Rieger

• Gerwin Schalk

• Robert T. Knight

• Brian Pasley

Date: 2014

DOI: 10.3389/fneng.2014.00014

PubMed: 4034498

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Abstract:

Auditory perception and auditory imagery have been shown to activate overlapping brain regions. We hypothesized that these phenomena also share a common underlying neural representation. To assess this, we used electrocorticography intracranial recordings from epileptic patients performing an out loud or a silent reading task. In these tasks, short stories scrolled across a video screen in two conditions: subjects read the same stories both aloud (overt) and silently (covert). In a control condition the subject remained in a resting state. We first built a high gamma (70–150 Hz) neural decoding model to reconstruct spectrotemporal auditory features of self-generated overt speech. We then evaluated whether this same model could reconstruct auditory speech features in the covert speech condition. Two speech models were tested: a spectrogram and a modulation-based feature space. For the overt condition, reconstruction accuracy was evaluated as the correlation between original and predicted speech features, and was significant in each subject (p < 10−5; paired two-sample t-test). For the covert speech condition, dynamic time warping was first used to realign the covert speech reconstruction with the corresponding original speech from the overt condition. Reconstruction accuracy was then evaluated as the correlation between original and reconstructed speech features. Covert reconstruction accuracy was compared to the accuracy obtained from reconstructions in the baseline control condition. Reconstruction accuracy for the covert condition was significantly better than for the control condition (p < 0.005; paired two-sample t-test). The superior temporal gyrus, pre- and post-central gyrus provided the highest reconstruction information. The relationship between overt and covert speech reconstruction depended on anatomy. These results provide evidence that auditory representations of covert speech can be reconstructed from models that are built from an overt speech data set, supporting a partially shared neural substrate.

Hypertension drives parenchymal b -amyloid accumulationin the brain parenchyma

Authors:

• Robert T. Knight

• Hans-Jochen Heinze

• Celine Bueche

• Cheryl Hawkes

• Cornelia Garz

• Stefan Vielhaber

• Johannes Attems

• Klaus Reymann

• Roxana Carare

• Stefanie Schreiber

Date: 2014

DOI: 10.1002/acn3.27

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Abstract:

There is substantial controversy regarding the causative role of amyloid b (Ab)deposition in Alzheimer’s disease (AD). The cerebrovasculature plays an impor-tant role in the elimination of Ab from the brain and hypertension is a well-known risk factor for AD. In spontaneously hypertensive stroke-prone rats(SHRSP), an animal model of chronic arterial hypertension, cerebral small ves-sel disease (CSVD) leads to age-dependent parenchymal Ab accumulation simi-lar to that observed in AD. These data approve the neuropathological linkbetween CSVD and AD, confirm the challenge that parenchymal Ab depositionis a specific marker for AD and disclose the meaning of SHRSP as valid experi-mental model to investigate the association between hypertension, CSVD, and Ab plaques.

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.

Single trial discrimination of individual finger movements on one hand: A combined MEG and EEG study

Authors:

• Fanny Quandt

• Christoph Reichert

• Hermann Hinrichs

• Hans-Jochen Heinze

• Robert T. Knight

• Jochem W. Rieger

Date: 2011

DOI: 10.1016/j.neuroimage.2011.11.053

PubMed: 22155040

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Abstract:

It is crucial to understand what brain signals can be decoded from single trials with different recording techniques for the development of Brain-Machine Interfaces. A specific challenge for non-invasive recording methods are activations confined to small spatial areas on the cortex such as the finger representation of one hand. Here we study the information content of single trial brain activity in non-invasive MEG and EEG recordings elicited by finger movements of one hand. We investigate the feasibility of decoding which of four fingers of one hand performed a slight button press. With MEG we demonstrate reliable discrimination of single button presses performed with the thumb, the index, the middle or the little finger (average over all subjects and fingers 57%, best subject 70%, empirical guessing level: 25.1%). EEG decoding performance was less robust (average over all subjects and fingers 43%, best subject 54%, empirical guessing level 25.1%). Spatiotemporal patterns of amplitude variations in the time series provided best information for discriminating finger movements. Non-phase-locked changes of mu and beta oscillations were less predictive. Movement related high gamma oscillations were observed in average induced oscillation amplitudes in the MEG but did not provide sufficient information about the finger's identity in single trials. Importantly, pre-movement neuronal activity provided information about the preparation of the movement of a specific finger. Our study demonstrates the potential of non-invasive MEG to provide informative features for individual finger control in a Brain-Machine Interface neuroprosthesis.