Local and distant cortical responses to single pulse intracranial stimulation in the human brain are differentially modulated by specific stimulation parameters

Paulk, Angelique C.; Zelmann, Rina; Crocker, Britni; Widge, Alik S.; Dougherty, Darin D.; Eskandar, Emad N.; Weisholtz, Daniel S.; Richardson, R. Mark; Cosgrove, G. Rees; Williams, Ziv; Cash, Sydney S.

doi:10.1016/j.brs.2022.02.017

Cited by 35 publications

(58 citation statements)

References 123 publications

(225 reference statements)

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“…Using a power spectral density approach, 74,84,85 we intended to build on previous works that focused on whole-band power metrics like root mean square, 77,79,86 or metrics that rely on cortico-cortical evoked potential waveform morphology which can be difficult to interpret with depth electrodes. 75,[87][88][89][90][91] Overall, when presumably healthy regions were stimulated, the SOZ theta [4-8 Hz] relative band power was markedly decreased from pre-stimulation baseline. Conversely, SOZ beta [13][14][15][16][17][18][19][20][21][22][23][24][25][26][27][28][29][30] and gamma relative band power increased when healthy regions were stimulated.…”

Section: Does Imbalanced Reciprocal Connectivity Indicate Suppression?mentioning

confidence: 97%

The Interictal Suppression Hypothesis in Focal Epilepsy: Electrographic and Structural Evaluation

Johnson

Doss

Morgan

et al. 2022

Preprint

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Why are people with focal epilepsy not constantly seizing? Previous molecular work has implicated gamma-aminobutyric acid balance as integral to seizure generation and termination, but is the high-level distributed brain network involved in suppressing seizures? Recent intracranial electrographic evidence has suggested that seizure onset zones have an increased inward connectivity. Accordingly, we hypothesize that seizure onset zones are actively suppressed by the rest of the brain network during interictal states.We tested this hypothesis on 81 subjects with drug resistant focal epilepsy undergoing presurgical evaluation. We utilized intracranial electrographic resting-state and neurostimulation recordings to evaluate the network connectivity of seizure onset, propagative, and non-involved regions. We then utilized diffusion imaging to acquire estimates of white matter connectivity to evaluate structure-function coupling effects on connectivity findings. Finally, using our observations, we generated a resting-state classification model to assist clinicians in detecting seizure onset and propagative zones without the need for multiple ictal recordings.Our findings indicate that seizure onset and propagative zones demonstrate markedly increased inward connectivity and decreased outward connectivity on both resting-state and neurostimulation analyses. When controlling for distance between regions, the difference between inward vs. outward connectivity remained stable up to 80 mm between brain connections. Structure-function coupling analyses revealed that seizure onset zones exhibit abnormally enhanced coupling (hypercoupling) of surrounding regions compared to presumably healthy tissue. Using these observations, our classification models achieved a maximum held-out testing set accuracy of 92.0±2.2%.These results indicate that seizure onset zones are actively segregated and suppressed by a widespread brain network. Furthermore, this electrographically observed functional suppression is disproportionate to any observed structural connectivity alterations of the seizure onset zones. These findings have implications for the identification of seizure onset zones using only brief resting-sate recordings to reduce patient morbidity and augment the presurgical evaluation of drug resistant epilepsy. Furthermore, testing of the interictal suppression hypothesis can provide insight into potential new resective, ablative, and neuromodulation approaches to improve surgical success rates in those suffering from drug resistant focal epilepsy.

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Section: Does Imbalanced Reciprocal Connectivity Indicate Suppression?mentioning

confidence: 97%

The Interictal Suppression Hypothesis in Focal Epilepsy: Electrographic and Structural Evaluation

Johnson

Doss

Morgan

et al. 2022

Preprint

View full text Add to dashboard Cite

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“…Participants received their typical antiepileptic medications before the stimulation experiment. A subset of the data obtained during the Wake state in the EMU was used in our previous publication (111). Electrodes were implanted exclusively for clinical reasons at the Massachusetts General Hospital (MGH) or Brigham and Women's Hospital (BWH).…”

Section: Human Participants Intracerebral Recordings and Stimulationmentioning

confidence: 99%

“…Multi-focal electrical intracranial stimulation was delivered with a CereStim R96 stimulator while simultaneously acquiring iEEG with a Blackrock Neural Signal Processing system at a 2 kHz sampling rate (Blackrock Microsystems, Salt Lake City, UT, USA). Individual charged-balanced biphasic stimulation pulses were 233ms duration, 7mA intensity, 2-5 s +/-0.25s inter-stimulation interval (34,111). Current injection and return paths used neighboring contacts in a bipolar con guration.…”

Section: Human Participants Intracerebral Recordings and Stimulationmentioning

confidence: 99%

Differential Cortical Network Engagement During States of Un/Consciousness in Humans

Zelmann

Paulk

Tian

et al. 2022

Preprint

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The neural basis of consciousness remains a major unresolved issue in human neuroscience, with theories of consciousness and experimental studies differing concerning which brain regions are necessary for consciousness. Direct experimental evidence to resolve this debate requires identifying the global, network, and regional involvement during different states of consciousness in humans. We utilized multi-region intracranial single-pulse direct electrical stimulation to examine circuit and network interactions during three canonical states of consciousness: wake vs. arousable unconsciousness (sleep) vs. non-arousable unconsciousness (e.g., propofol-induced general anesthesia). Increased variability in cortical responses, reduced information transfer, and reduced complexity characterized states of diminished consciousness. Notably, however, these metrics differed in different brain regions and types of unconscious states.Anesthesia induced more overall changes in brain responses than sleep, but cortical network engagement depended on the kind of unconsciousness. Brain activity changes were largely anatomically uniform during sleep, contrasting with a substantial and selective disconnection of the prefrontal cortices during anesthesia. These results provide direct evidence from human intracranial recordings during the loss of consciousness, suggesting that the obliteration of consciousness during anesthesia results not from just altered overall physiology but from a disconnection between prefrontal areas and other brain areas. Significance What happens in the human brain when we are unconscious? Despite substantial work, we are still unsure which brain regions are involved and how they are impacted when consciousness is disrupted. Using intracranial recordings and direct electrical stimulation, we mapped global, network, and regional involvement during wake vs. arousable unconsciousness (sleep) vs. non-arousable unconsciousness (propofol-induced general anesthesia). Information integration and complex processing were reduced, while variability increased during the loss of consciousness. These changes were more pronounced during anesthesia than sleep. They also involved different cortical engagement; During sleep, changes were mostly uniformly distributed across the brain while during anesthesia the prefrontal cortex was the most disrupted. These findings indicate different neural signatures for different types of unconsciousness. Highlights · Sleep and anesthesia showed decreased complexity, connectivity, and response amplitude with increased response variability compared to wake states in the human brain. · These changes in brain response to stimulation were more pronounced during propofol-induced general anesthesia than during natural sleep. · During sleep, changes were homogeneously distributed across the brain. · During anesthesia, there was a substantial disconnection of the frontal cortices.

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“…Clinical needs also constrained the exploration of physical stimulation parameters to few pulse intensities and two pulse widths. Future studies encompassing multiple intensity and pulse width steps, like the one by Paulk and colleagues [69], will allow for a more systematic comparison between invasive and non-invasive stimulation techniques.…”

Section: Limitationsmentioning

confidence: 99%

Simultaneous stereo-EEG and high-density scalp EEG recordings to study the effects of intracerebral stimulation parameters

et al. 2022

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Local and distant cortical responses to single pulse intracranial stimulation in the human brain are differentially modulated by specific stimulation parameters

Cited by 35 publications

References 123 publications

The Interictal Suppression Hypothesis in Focal Epilepsy: Electrographic and Structural Evaluation

The Interictal Suppression Hypothesis in Focal Epilepsy: Electrographic and Structural Evaluation

Differential Cortical Network Engagement During States of Un/Consciousness in Humans

Simultaneous stereo-EEG and high-density scalp EEG recordings to study the effects of intracerebral stimulation parameters

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