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Intrinsic network architecture predicts the effects elicited by intracranial electrical stimulation of the human brain
Open accessAbstract
Intracranial electrical stimulation (iES) of the human brain has long been known to elicit a remarkable variety of perceptual, motor and cognitive effects, but the functional-anatomical basis of this heterogeneity remains poorly understood. We conducted a whole-brain mapping of iES-elicited effects, collecting first-person reports following iES at 1,537 cortical sites in 67 participants implanted with intracranial electrodes. We found that intrinsic network membership and the principal gradient of functional connectivity strongly predicted the type and frequency of iES-elicited effects in a given brain region. While iES in unimodal brain networks at the base of the cortical hierarchy elicited frequent and simple effects, effects became increasingly rare, heterogeneous and complex in heteromodal and transmodal networks higher in the hierarchy. Our study provides a comprehensive exploration of the relationship between the hierarchical organization of intrinsic functional networks and the causal modulation of human behaviour and experience with iES.
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“And as noted above, a recent study we conducted with a large cohort of iES patients (n = 67) likewise found exclusively null effects in frontopolar cortex (Fox et al., 2020).”
From Does the Prefrontal Cortex Play an Essential Role in Consciousness? Insights from Intracranial Electrical Stimulation of the Human Brain (2021) · cites this paper as Fox et al., 2020
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
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“We are not aware of any past research that reports iESinduced phenomenal changes in these regions (Selimbeyoglu and Parvizi, 2010), and recent work across dozens of patients, from both our own group (Fox et al., 2020) and others (Trevisi et al., 2018), indicates only null results in these areas.”
From Does the Prefrontal Cortex Play an Essential Role in Consciousness? Insights from Intracranial Electrical Stimulation of the Human Brain (2021) · cites this paper as Fox et al., 2020
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Indeed, there is no part of the brain wherein iES is less likely to cause a noticeable change in consciousness than the most anterior regions of the PFC (Fox et al., 2020) (Figs. 2 and 3).”
From Does the Prefrontal Cortex Play an Essential Role in Consciousness? Insights from Intracranial Electrical Stimulation of the Human Brain (2021) · cites this paper as Fox et al., 2020
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“This low elicitation rate (17%) is in marked contrast to unimodal brain regions, where positive response rates can reach 67% (Fox et al., 2020).”
From Does the Prefrontal Cortex Play an Essential Role in Consciousness? Insights from Intracranial Electrical Stimulation of the Human Brain (2021) · cites this paper as Fox et al., 2020
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“Sham stimulation is used to control for demand characteristics, especially when meaningful or intense experiences are reported, and has proven to be a very effective control (Fox and Parvizi, 2021;Fox et al., 2020).”
From Does the Prefrontal Cortex Play an Essential Role in Consciousness? Insights from Intracranial Electrical Stimulation of the Human Brain (2021) · cites this paper as Fox et al., 2020
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“It is also significant that the PFC is not the only region of the brain where iES-elicited effects are rare: other high-level association areas also appear to share this property (e.g., the posterior cingulate cortex) (Foster and Parvizi, 2017), and these trends appear to be driven by the brain's intrinsic network architecture (Fox et al., 2020).”
From Does the Prefrontal Cortex Play an Essential Role in Consciousness? Insights from Intracranial Electrical Stimulation of the Human Brain (2021) · cites this paper as Fox et al., 2020
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“Our prior work has shown that simple neurophysiological attributes, such as myelin concentration or electrical excitability, are unable to explain elicitation rates across the cortical mantle (Fox et al., 2020).”
From Does the Prefrontal Cortex Play an Essential Role in Consciousness? Insights from Intracranial Electrical Stimulation of the Human Brain (2021) · cites this paper as Fox et al., 2020
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“Low rates of iES effects are not unique to prefrontal regions, but appear to be a more general property of brain areas involved in abstract thought and complex cognitive function, although the lowest elicitation rates are nonetheless found in the anterior PFC (Fox et al., 2020;Koch, 2020).”
From Does the Prefrontal Cortex Play an Essential Role in Consciousness? Insights from Intracranial Electrical Stimulation of the Human Brain (2021) · cites this paper as Fox et al., 2020
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In the citing paper
“Therefore, PFC neurons are thought to represent information across larger circuits; hence, the localized nature of iES might result in lower rates of effect elicitation compared with unimodal regions where contiguous neuronal populations code for specific perceptual features (Fox et al., 2020).”
From Does the Prefrontal Cortex Play an Essential Role in Consciousness? Insights from Intracranial Electrical Stimulation of the Human Brain (2021) · cites this paper as Fox et al., 2020
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“One major caveat is that iES to the PFC might still be influencing consciousness, but in subtle ways not noticeable or reportable by patients (Fox et al., 2020).”
From Does the Prefrontal Cortex Play an Essential Role in Consciousness? Insights from Intracranial Electrical Stimulation of the Human Brain (2021) · cites this paper as Fox et al., 2020
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“within NREM sleep, the response to TMS differed according to the subjects’ report upon awakening133. Reports of no dreaming were associated with a larger negative evoked response and shorter phase-locking compared with reports of dreaming.”
From Consciousness and sleep (2024) · cites this paper as [133]
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“the amplitude of the negative peak, presumably reflecting the degree of neuronal bistability, was inversely correlated with the length of the dream report (word count).”
From Consciousness and sleep (2024) · cites this paper as [133]
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“A wide variety of other effects have been reported, including digestive sensations (Mulak et al., 2008), vestibular hallucinations (Kahane et al., 2003), anxiety and physical pain (Kahane et al., 2003;Mulak et al., 2008), and in the pregenual ACC, fear (Fox et al., 2020).”
From Does the Prefrontal Cortex Play an Essential Role in Consciousness? Insights from Intracranial Electrical Stimulation of the Human Brain (2021) · cites this paper as Fox et al., 2020
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Metadata
- Authors
- Fox, K. C. R., Shi, L., Baek, S., Raccah, O., Foster, B. L., Saha, S., Margulies, D. S., Kucyi, A., & Parvizi, J.
- Affiliations
- Stanford Medicine (US)
- Capital Medical University (CN)
- Baylor College of Medicine (US)
- Centre National de la Recherche Scientifique (FR)
- Corresponding author
- Fox, Kieran C. R.
- Parvizi, Josef
- ORCID
- Venue
- Nature Human Behaviour
- Published
- 2020-07-06
- Volume
- 4
- Issue
- 10
- Pages
- 1039-1052
- ISSN
- 2397-3374 (ISSN-L)
- PMC
- PMC7572705
- OpenAlex
- W3039362686
- Cited by
- 133
- References
- 95
- Citations by year
- 2026: 10 · 2025: 22 · 2024: 18 · 2023: 36 · 2022: 20 · 2021: 22 · 2020: 5
- FWCI
- 11.15
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- Nature Human Behaviour (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- HAL (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- China Scholarship Council (201708110057)
- U.S. Department of Health & Human Services | National Institutes of Health (R00MH103479, 1P50MH109429)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Life Sciences › Neuroscience › Neurology › Transcranial Magnetic Stimulation Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neural Engineering
- Keywords
- intracranial electrical stimulation, cortical hierarchy, functional connectivity gradients, network membership, first-person reports, perceptual effects, motor effects, cognitive effects
- MeSH terms
- Drug Resistant Epilepsy, Electrocorticography, Adult, Brain Mapping, Cerebral Cortex, Electric Stimulation, Epilepsies, Partial, Female, Humans, Functional Laterality, Male, Middle Aged, Nerve Net, Connectome
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