Grasp-specific high-frequency broadband mirror neuron activity during reach-and-grasp movements in humans

Abstract:

Broadly congruent mirror neurons, responding to any grasp movement, and strictly congruent mirror neurons, responding only to specific grasp movements, have been reported in single-cell studies with primates. Delineating grasp properties in humans is essential to understand the human mirror neuron system with implications for behavior and social cognition. We analyzed electrocorticography data from a natural reach-and-grasp movement observation and delayed imitation task with 3 different natural grasp types of everyday objects. We focused on the classification of grasp types from high-frequency broadband mirror activation patterns found in classic mirror system areas, including sensorimotor, supplementary motor, inferior frontal, and parietal cortices. Classification of grasp types was successful during movement observation and execution intervals but not during movement retention. Our grasp type classification from combined and single mirror electrodes provides evidence for grasp-congruent activity in the human mirror neuron system potentially arising from strictly congruent mirror neurons.

Authros:

• Alexander M. Dreyer

• Leo Michalke

• Anat Perry

• Edward F. Chang

• Jack J. Lin

• Robert T. Knight

• Jochem W. Rieger

Date: 2022

DOI: https://doi.org/10.1093/cercor/bhac504

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Deep brain stimulation of the ventrointermediate nucleus of the thalamus to treat essential tremor improves motor sequence learning

Abstract:

The network of brain structures engaged in motor sequence learning comprises the same structures as those involved in tremor, including basal ganglia, cerebellum, thalamus, and motor cortex. Deep brain stimulation (DBS) of the ventrointermediate nucleus of the thalamus (VIM) reduces tremor, but the effects on motor sequence learning are unknown. We investigated whether VIM stimulation has an impact on motor sequence learning and hypothesized that stimulation effects depend on the laterality of electrode location. Twenty patients (age: 38–81 years; 12 female) withVIM electrodes implanted to treat essential tremor (ET) successfully performed a serial reaction time task, varying whether the stimuli followed a repeating pattern or were selected at random, during which VIM-DBS was either on or off. Analyses of variance were applied to evaluate motor sequence learning performance according to reaction times (RTs) and accuracy. An interaction was observed between whether the sequence was repeated or random and whether VIM-DBS was on or off (F[1,18]=7.89,p=.012). Motor sequence learning, reflected by reduced RTs for repeated sequences, was greater with DBS on than off (T[19]=2.34,p=.031). Stimulation location correlated with the degree of motor learning, with greater motor learning when stimulation targeted the lateral VIM (n=23,ρ=0.46;p=.027).These results demonstrate the beneficial effects of VIM-DBS on motor sequence learning in ET patients, particularly with lateral VIM electrode location, and provide evidence for a role for the VIM in motor sequence learning.

Authors:

• Laila Terzic

• Angela Voegtle

• Amr Farahat

• Nanna Hartong

• Imke Galazky

• Slawomir J. Nasuto

• Adriano de Oliveira Andrade

• Robert T. Knight

• Richard B. Ivry

• Jürgen Voges

• Lars Buentjen

• Catherine M. Sweeney-Reed

Date: 2022

DOI: 10.1002/hbm.25989

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Advances in human intracranial electroencephalography research, guidelines and good practices

Abstract:

Since the second half of the twentieth century, intracranial electroencephalography (iEEG), including both electrocorticography (ECoG) and stereo-electroencephalography (sEEG), has provided an intimate view into the human brain. At the interface between fundamental research and the clinic, iEEG provides both high temporal resolution and high spatial specificity but comes with constraints, such as the individual's tailored sparsity of electrode sampling. Over the years, researchers in neuroscience developed their practices to make the most of the iEEG approach. Here we offer a critical review of iEEG research practices in a didactic framework for newcomers, as well addressing issues encountered by proficient researchers. The scope is threefold: (i) review common practices in iEEG research, (ii) suggest potential guidelines for working with iEEG data and answer frequently asked questions based on the most widespread practices, and (iii) based on current neurophysiological knowledge and methodologies, pave the way to good practice standards in iEEG research. The organization of this paper follows the steps of iEEG data processing. The first section contextualizes iEEG data collection. The second section focuses on localization of intracranial electrodes. The third section highlights the main pre-processing steps. The fourth section presents iEEG signal analysis methods. The fifth section discusses statistical approaches. The sixth section draws some unique perspectives on iEEG research. Finally, to ensure a consistent nomenclature throughout the manuscript and to align with other guidelines, e.g., Brain Imaging Data Structure (BIDS) and the OHBM Committee on Best Practices in Data Analysis and Sharing (COBIDAS), we provide a glossary to disambiguate terms related to iEEG research.

Authors:

• Manuel R. Mercier

• Anne-Sophie Dubarry

• François Tadel

• Pietro Avanzini

• Nikolai Axmacher

• Dillan Cellier

• Maria Del Vecchio

• Liberty S. Hamilton

• Dora Hermes

• Michael J. Kahana

• Robert T. Knight

• Anais Llorens

• Pierre Megevand

• Lucia Melloni

• Kai J. Miller

• Vitória Piai

• Aina Puce

• Nick F. Ramsey

• Caspar M. Schwiedrzik

• Sydney E. Smith

• Arjen Stolk

• Nicole C. Swann

• Mariska J Vansteensel

• Bradley Voytek

• Liang Wang

• Jean-Philippe Lachaux

• Robert Oostenveld

Date: 2022

DOI: https://doi.org/10.1016/j.neuroimage.2022.119438

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Orbitofrontal cortex governs working memory for temporal order

abstract:

How do we think about time? Converging lesion and neuroimaging evidence indicates that orbitofrontal cortex (OFC) supports the encoding and retrieval of temporal context in long-term memory, which may contribute to confabulation in individuals with OFC damage. Here, we reveal that OFC damage diminishes working memory for temporal order, that is, the ability to disentangle the relative recency of events as they unfold. OFC lesions reduced working memory for temporal order but not spatial position, and individual deficits were commensurate with lesion size. Comparable effects were absent in patients with lesions restricted to lateral prefrontal cortex (PFC). Based on these findings, we propose that OFC supports understanding of the order of events. Well-documented behavioral changes in individuals with OFC damage may relate to impaired temporal-order understanding.

authors:

• Elizabeth L Johnson

• William K Chang

• Callum D Dewar

• Donna Sorensen

• Jack J Lin

• Anne-Kristin Solbakk

• Tor Endestad

• Pal G Larsson

• Jugoslav Ivanovic

• Torstein R Meling

• Donatella Scabini

• Robert T Knight

Date: 2022

DOI: https:// doi.org/10.1016/j.cub.2022.03.074.

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Event segmentation reveals working memory forgetting rate

abstract:

We encounter the world as a continuous flow and effortlessly segment sequences of events into episodes. This process of event segmentation engages working memory (WM) for tracking the flow of events and impacts subsequent memory accuracy. WM is limited in how much information (i.e., WM capacity) and for how long the information is retained (i.e., forgetting rate). In this study, across multiple tasks, we estimated participants' WM capacity and forgetting rate in a dynamic context and evaluated their relationship to event segmentation. A U-shaped relationship across tasks shows that individuals who segmented the movie more finely or coarsely than the average have a faster WM forgetting rate. A separate task assessing long-term memory retrieval revealed that the coarse-segmenters have better recognition of temporal order of events compared to the fine-segmenters. These findings show that event segmentation employs dissociable memory strategies and correlates with how long information is retained in WM

authors:

• Anna Jafarpour

• Elizabeth A Buffalo

• Robert T Knight

• Anne GE Collins

Date: 2022

DOI: https://doi.org/10.1016/ j.isci.2022.103902

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Mind-wandering: mechanistic insights from lesion, tDCS, and iEEG

abstract:

Cognitive neuroscience has witnessed a surge of interest in investigating the neural correlates of the mind when it drifts away from an ongoing task and the external environment. To that end, functional neuroimaging research has consistently implicated the default mode network (DMN) and frontoparietal control network (FPCN) in mind-wandering. Yet, it remains unknown which subregions within these networks are necessary and how they facilitate mind-wandering. In this review, we synthesize evidence from lesion, transcranial direct current stimulation (tDCS), and intracranial electroencephalogram (iEEG) studies demonstrating the causal relevance of brain regions, and providing insights into the neuronal mechanism underlying mind-wandering. We propose that the integration of complementary approaches is the optimal strategy to establish a comprehensive understanding of the neural basis of mind-wandering.

Authors:

• Julia WY Kam

• Matthias Mittner

• Robert T Knight

Date: 2022

DOI:

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Left hemisphere dominance for bilateral kinematic encoding in the human brain

Abstract:

Neurophysiological studies in humans and nonhuman primates have revealed movement representations in both the contralateral and ipsilateral hemispheres. Inspired by clinical observations, we ask if this bilateral representation differs for the left and right hemispheres. Electrocorticography was recorded in human participants during an instructed-delay reaching task, with movements produced with either the contralateral or ipsilateral arm. Using a cross-validated kinematic encoding model, we found stronger bilateral encoding in the left hemisphere, an effect that was present during preparation and was amplified during execution. Consistent with this asymmetry, we also observed better across-arm generalization in the left hemisphere, indicating similar neural representations for right and left arm movements. Notably, these left hemisphere electrodes were centered over premotor and parietal regions. The more extensive bilateral encoding in the left hemisphere adds a new perspective to the pervasive neuropsychological finding that the left hemisphere plays a dominant role in praxis.

authors:

• Christina M Merrick

• Tanner C Dixon

• Assaf Breska

• Jack Lin

• Edward F Chang

• David King-Stephens

• Kenneth D Laxer

• Peter B Weber

• Jose Carmena

• Robert Thomas Knight

• Richard B Ivry

Date: 2022

DOI: : https://doi.org/10.7554/eLife.69977

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Consciousness is supported by near-critical slow cortical electrodynamics

Abstract:

Mounting evidence suggests that during conscious states, the electrodynamics of the cortex are poised near a critical point or phase transition and that this near-critical behavior supports the vast flow of information through cortical networks during conscious states. Here, we empirically identify a mathematically specific critical point near which waking cortical oscillatory dynamics operate, which is known as the edge-of-chaos critical point, or the boundary between stability and chaos. We do so by applying the recently developed modified 0-1 chaos test to electrocorticography (ECoG) and magnetoencephalography (MEG) recordings from the cortices of humans and macaques across normal waking, generalized seizure, anesthesia, and psychedelic states. Our evidence suggests that cortical information processing is disrupted during unconscious states because of a transition of low-frequency cortical electric oscillations away from this critical point; conversely, we show that psychedelics may increase the information richness of cortical activity by tuning low-frequency cortical oscillations closer to this critical point. Finally, we analyze clinical electroencephalography (EEG) recordings from patients with disorders of consciousness (DOC) and show that assessing the proximity of slow cortical oscillatory electrodynamics to the edge-of-chaos critical point may be useful as an index of consciousness in the clinical setting.

Authors:

• Daniel Toker

• Ioannis Pappas

• Janna D Lendner

• Joel Frohlich

• Diego M Mateos

• Suresh Muthukumaraswamy

• Robin Carhart-Harris

• Michelle Paff

• Paul M Vespa

• Martin M Monti

• Friedrich T Sommer

• Robert T Knight

• Mark D’Esposito

Date: 2022

DOI: https://doi.org/10.1073/pnas.2024455119

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Encoding and decoding analysis of music perception using intracranial EEG

Abstract:

Music perception engages multiple brain regions, however the neural dynamics of this core human experience remains elusive. We applied predictive models to intracranial EEG data from 29 patients listening to a Pink Floyd song. We investigated the relationship between the song spectrogram and the elicited high-frequency activity (70-150Hz), a marker of local neural activity. Encoding models characterized the spectrotemporal receptive fields (STRFs) of each electrode and decoding models estimated the population-level song representation. Both methods confirmed a crucial role of the right superior temporal gyri (STG) in music perception. A component analysis on STRF coefficients highlighted overlapping neural populations tuned to specific musical elements (vocals, lead guitar, rhythm). An ablation analysis on decoding models revealed the presence of unique musical information concentrated in the right STG and more spatially distributed in the left hemisphere. Lastly, we provided the first song reconstruction decoded from human neural activity.

Authors:

• Ludovic Bellier

• Anaïs Llorens

• Déborah Marciano

• Gerwin Schalk

• Peter Brunner

• Robert T. Knight

• Brian N. Pasley

Date: 2022

DOI: https://doi.org/10.1101/2022.01.27.478085

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Orbitofrontal cortex governs working memory for temporal order

Abstract:

How do we think about time? Converging lesion and neuroimaging evidence indicates that orbitofrontal cortex (OFC) supports the encoding and retrieval of temporal context in long-term memory1, which may contribute to confabulation in individuals with OFC damage2. Here, we reveal that OFC damage diminishes working memory for temporal order, that is, the ability to disentangle the relative recency of events as they unfold. OFC lesions reduced working memory for temporal order but not spatial position, and individual deficits were commensurate with lesion size. Comparable effects were absent in patients with lesions restricted to lateral prefrontal cortex (PFC). Based on these findings, we propose that OFC supports understanding of the order of events. Well-documented behavioral changes in individuals with OFC damage2 may relate to impaired temporal-order understanding.

Authors:

• Elizabeth L. Johnson

• William K. Chang

• Callum D. Dewar

• Donna Sorensen

• Jack J. Lin

• Anne-Kristin Solbakk

• Tor Endestad

• Pal G. Larsson

• Jugoslav Ivanovic

• Torstein R. Meling

• Donatella Scabini

• Robert T. Knight

Date: 2022

DOI: https://doi.org/10.1016/j.cub.2022.03.074

View PDF

Event segmentation reveals working memory forgetting rate

Abstract:

We encounter the world as a continuous flow and effortlessly segment sequences of events into episodes. This process of event segmentation engages working memory (WM) for tracking the flow of events and impacts subsequent memory accuracy. WM is limited in how much information (i.e., WM capacity) and for how long the information is retained (i.e., forgetting rate). In this study, across multiple tasks, we estimated participants’ WM capacity and forgetting rate in a dynamic context and evaluated their relationship to event segmentation. A Ushaped relationship across tasks shows that individuals who segmented the movie more finely or coarsely than the average have a faster WM forgetting rate. A separate task assessing long-term memory retrieval revealed that the coarse-segmenters have better recognition of temporal order of events compared to the fine-segmenters. These findings show that event segmentation employs dissociable memory strategies and correlates with how long information is retained in WM

Authors:

• Anna Jafarpour

• Elizabeth A. Buffalo

• Robert T. Knight

• Anne G.E. Collins

Date: 2022

DOI: https://doi.org/10.1016/j.isci.2022.103902

View PDF

Mind-wandering: mechanistic insights from lesion, tDCS, and iEEG

Abstract:

Cognitive neuroscience has witnessed a surge of interest in investigating the neural correlates of the mind when it drifts away from an ongoing task and the external environment. To that end, functional neuroimaging research has consistently implicated the default mode network (DMN) and frontoparietal control network (FPCN) in mind-wandering. Yet, it remains unknown which subregions within these networks are necessary and how they facilitate mind-wandering. In this review, we synthesize evidence from lesion, transcranial direct current stimulation (tDCS), and intracranial electroencephalogram (iEEG) studies demonstrating the causal relevance of brain regions, and providing insights into the neuronal mechanism underlying mind-wandering. We propose that the integration of complementary approaches is the optimal strategy to establish a comprehensive understanding of the neural basis of mindwandering.

Authors:

• Julia W.Y. Kam

• Matthias Mittner

• Robert T. Knight

Date: 2022

DOI: https://doi.org/10.1016/j.tics.2021.12.005

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Consciousness is supported by near-critical slow cortical electrodynamics

Abstract:

Mounting evidence suggests that during conscious states, the electrodynamics of the cortex are poised near a critical point or phase transition and that this near-critical behavior supports the vast flow of information through cortical networks during conscious states. Here, we empirically identify a mathematically specific critical point near which waking cortical oscillatory dynamics operate, which is known as the edge-of-chaos critical point, or the boundary between stability and chaos. We do so by applying the recently developed modified 0-1 chaos test to electrocorticography (ECoG) and magnetoencephalography (MEG) recordings from the cortices of humans and macaques across normal waking, generalized seizure, anesthesia, and psychedelic states. Our evidence suggests that cortical information processing is disrupted during unconscious states because of a transition of low-frequency cortical electric oscillations away from this critical point; conversely, we show that psychedelics may increase the information richness of cortical activity by tuning low-frequency cortical oscillations closer to this critical point. Finally, we analyze clinical electroencephalography (EEG) recordings from patients with disorders of consciousness (DOC) and show that assessing the proximity of slow cortical oscillatory electrodynamics to the edge-of-chaos critical point may be useful as an index of consciousness in the clinical setting.

Authors:

• Daniel Toker

• Ioannis Pappas

• Janna D. Lendner

• Joel Frohlich

• Diego M. Mateos

• Suresh Muthukumaraswamy

• Robin Carhart-Harris

• Michelle Paff

• Paul M. Vespa

• Martin M. Monti

• Friedrich T. Sommer

• Robert T. Knight

• Mark D’Esposito

Date: 2022

DOI: https://doi.org/10.1073/pnas.2024455119

View PDF

Left hemisphere dominance for bilateral kinematic encoding in the human brain

Abstract:

Neurophysiological studies in humans and nonhuman primates have revealed movement representations in both the contralateral and ipsilateral hemispheres. Inspired by clinical observations, we ask if this bilateral representation differs for the left and right hemispheres. Electrocorticography was recorded in human participants during an instructed-delay reaching task, with movements produced with either the contralateral or ipsilateral arm. Using a cross-validated kinematic encoding model, we found stronger bilateral encoding in the left hemisphere, an effect that was present during preparation and was amplified during execution. Consistent with this asymmetry, we also observed better across-arm generalization in the left hemisphere, indicating similar neural representations for right and left arm movements. Notably, these left hemisphere electrodes were centered over premotor and parietal regions. The more extensive bilateral encoding in the left hemisphere adds a new perspective to the pervasive neuropsychological finding that the left hemisphere plays a dominant role in praxis.

Authors:

• Christina M Merrick

• Tanner C Dixon

• Assaf Breska

• Jack Lin

• Edward F Chang

• David King-Stephens

• Kenneth D Laxer

• Peter B Weber

• Jose Carmena

• Robert Thomas Knight

• Richard B Ivry

Date: 2022

DOI: : https://doi.org/10.7554/eLife.69977

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Imagined speech can be decoded from low- and cross-frequency intracranial EEG features

Abstract:

Reconstructing intended speech from neural activity using brain-computer interfaces holds great promises for people with severe speech production deficits. While decoding overt speech has progressed, decoding imagined speech has met limited success, mainly because the associated neural signals are weak and variable compared to overt speech, hence difficult to decode by learning algorithms. We obtained three electrocorticography datasets from 13 patients, with electrodes implanted for epilepsy evaluation, who performed overt and imagined speech production tasks. Based on recent theories of speech neural processing, we extracted consistent and specific neural features usable for future brain computer interfaces, and assessed their performance to discriminate speech items in articulatory, phonetic, and vocalic representation spaces. While high-frequency activity provided the best signal for overt speech, both low- and higher-frequency power and local cross-frequency contributed to imagined speech decoding, in particular in phonetic and vocalic, i.e. perceptual, spaces. These findings show that low-frequency power and cross-frequency dynamics contain key information for imagined speech decoding.

Authors:

• Timothée Proix

• Jaime Delgado Saa

• Andy Christen

• Stephanie Martin

• Brian N. Pasley

• Robert T. Knight

• Xing Tian

• David Poeppel

• Werner K. Doyle

• Orrin Devinsky

• Luc H. Arnal

• Pierre Mégevand

• Anne-Lise Giraud

Date: 2021

DOI: https://doi.org/10.1038/s41467-021-27725-3

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