Direct electrical stimulation of human cortex evokes high gamma activity that predicts conscious somatosensory perception

Muller, Leah; Rolston, John D.; Fox, Neal P.; Knowlton, Robert C.; Rao, Vikram R.; Chang, Edward F.

doi:10.1088/1741-2552/aa9bf9

Cited by 16 publications

(19 citation statements)

References 62 publications

(81 reference statements)

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“…Chronically implantable devices that stimulate the human brain are clinically approved to treat Parkinson’s disease, essential tremor, dystonia, epilepsy, and obsessive-compulsive disorder and have been investigated for major depressive disorder and Tourette syndrome (Lozano & Lipsman, 2013). Recent human studies have investigated the ability for direct stimulation of cortical and subcortical structures to modulate biomarkers of memory (Ezzyat et al, 2017; Inman et al, 2017), visual perception (Rangarajan et al, 2014; Winawer & Parvizi, 2016), language production (Chang, Kurteff, & Wilson, 2017), somatosensory perception (Muller et al, 2018), sensorimotor function (W. Wang et al, 2013), and subjective experience (Foster & Parvizi, 2017). While neurostimulation is a promising interventional approach to modulate brain state, current practices of calibrating where , when , and how to stimulate the brain are “open-loop” and limited in efficacy—relying on manual and periodic tuning of device parameters to optimize therapy (Morrell, 2011).…”

Section: Introductionmentioning

confidence: 99%

Functional control of electrophysiological network architecture using direct neurostimulation in humans

Khambhati

Kahn

Costantini

et al. 2019

Network Neuroscience

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Chronically implantable neurostimulation devices are becoming a clinically viable option for treating patients with neurological disease and psychiatric disorders. Neurostimulation offers the ability to probe and manipulate distributed networks of interacting brain areas in dysfunctional circuits. Here, we use tools from network control theory to examine the dynamic reconfiguration of functionally interacting neuronal ensembles during targeted neurostimulation of cortical and subcortical brain structures. By integrating multimodal intracranial recordings and diffusion-weighted imaging from patients with drug-resistant epilepsy, we test hypothesized structural and functional rules that predict altered patterns of synchronized local field potentials. We demonstrate the ability to predictably reconfigure functional interactions depending on stimulation strength and location. Stimulation of areas with structurally weak connections largely modulates the functional hubness of downstream areas and concurrently propels the brain towards more difficult-to-reach dynamical states. By using focal perturbations to bridge large-scale structure, function, and markers of behavior, our findings suggest that stimulation may be tuned to influence different scales of network interactions driving cognition.

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Section: Introductionmentioning

confidence: 99%

Functional control of electrophysiological network architecture using direct neurostimulation in humans

Khambhati

Kahn

Costantini

et al. 2019

Network Neuroscience

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“…Researchers have found a correlation between cortical stimulation, perception of sensation, and high gamma activity, pointing to overlap of the OFM and ECS methods. 44…”

Section: Discussionmentioning

confidence: 99%

“…Researchers have found a correlation between cortical stimulation, perception of sensation, and high gamma activity, pointing to overlap of the OFM and ECS methods. 44 A technical area for improvement includes automating display of real-time OFM results. Initially, OFM results were only displayed on grid diagrams (Fig.…”

Section: Limitations and Next Stepsmentioning

confidence: 99%

Novel intraoperative online functional mapping of somatosensory finger representations for targeted stimulating electrode placement

McMullen

Thomas

Fifer

et al. 2020

Preprint

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Defining eloquent cortex intraoperatively, traditionally performed by neurosurgeons to preserve patient function, can now help target electrode implantation for restoring function. Brain-machine interfaces (BMIs) have the potential to restore upper-limb motor control to paralyzed patients but require accurate placement of recording and stimulating electrodes to enable functional control of a prosthetic limb. Beyond motor decoding from recording arrays, precise placement of stimulating electrodes in cortical areas associated with finger and fingertip sensations allows for the delivery of sensory feedback that could improve dexterous control of prosthetic hands. In our study, we demonstrated the use of a novel intraoperative online functional mapping (OFM) technique with high-density electrocorticography (ECoG) to localize finger representations in human primary somatosensory cortex. In conjunction with traditional pre- and intraoperative targeting approaches, this technique enabled accurate implantation of stimulating microelectrodes, which was confirmed by post-implantation intra-cortical stimulation of finger and fingertip sensations. This work demonstrates the utility of intraoperative OFM and will inform future studies of closed-loop BMIs in humans.

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“…The significance of these differences was evaluated in relation to the variability of fluctuations within each time segment. The data features we compared were the fluctuations in HFA (70–150 Hz), shown to be a potential specific biological support of cognitive function (Lachaux, Axmacher, Mormann, Halgren, & Crone, 2012; Muller et al, 2018; Perrone‐Bertolotti et al, 2020). We applied this methodology to assess large‐scale language networks by evaluated DES‐induced language errors and measured HFA modification during these errors in nonstimulated brain regions.…”

Section: Introductionmentioning

confidence: 99%

Probabilistic mapping of language networks from high frequency activity induced by direct electrical stimulation

Perrone‐Bertolotti

Alexandre

Jobb

et al. 2020

Human Brain Mapping

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Direct electrical stimulation (DES) at 50 Hz is used as a gold standard to map cognitive functions but little is known about its ability to map large‐scale networks and specific subnetwork. In the present study, we aim to propose a new methodological approach to evaluate the specific hypothesis suggesting that language errors/dysfunction induced by DES are the result of large‐scale network modification rather than of a single cortical region, which explains that similar language symptoms may be observed after stimulation of different cortical regions belonging to this network. We retrospectively examined 29 patients suffering from focal drug‐resistant epilepsy who benefitted from stereo‐electroencephalographic (SEEG) exploration and exhibited language symptoms during a naming task following 50 Hz DES. We assessed the large‐scale language network correlated with behavioral DES‐induced responses (naming errors) by quantifying DES‐induced changes in high frequency activity (HFA, 70–150 Hz) outside the stimulated cortical region. We developed a probabilistic approach to report the spatial pattern of HFA modulations during DES‐induced language errors. Similarly, we mapped the pattern of after‐discharges (3–35 Hz) occurring after DES. HFA modulations concurrent to language symptoms revealed a brain network similar to our current knowledge of language gathered from standard brain mapping. In addition, specific subnetworks could be identified within the global language network, related to different language processes, generally described in relation to the classical language regions. Spatial patterns of after‐discharges were similar to HFA induced during DES. Our results suggest that this new methodological DES‐HFA mapping is a relevant approach to map functional networks during SEEG explorations, which would allow to shift from “local” to “network” perspectives.

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Direct electrical stimulation of human cortex evokes high gamma activity that predicts conscious somatosensory perception

Abstract: Our findings suggest that high gamma activity is a reliable biomarker for perception evoked by both natural and electrical stimuli.

Cited by 16 publications

References 62 publications

Functional control of electrophysiological network architecture using direct neurostimulation in humans

Functional control of electrophysiological network architecture using direct neurostimulation in humans

Novel intraoperative online functional mapping of somatosensory finger representations for targeted stimulating electrode placement

Probabilistic mapping of language networks from high frequency activity induced by direct electrical stimulation

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