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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A recent study with a large cohort of iES patients (n = 67) found exclusively null effects in frontopolar cortex.
“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
The Results report iES data from 67 patients, and the Discussion describes the anterior prefrontal cortex as showing “almost total quiescence.” That supports predominantly null findings in the region, but not the stronger claim that effects were exclusively null. The paper also limits its observations to stimulation during a task-free resting state; page numbers are unavailable in our copy. (LLM, conf=0.86)
Experimental — accuracy not yet measuredRecent work across dozens of patients, from the authors' own group and others, indicates only null results in anteromedial prefrontal regions.
“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
The Methods (Patient characteristics; page unavailable) report a 67-patient sample. The Discussion (page unavailable) says effects in the core medial prefrontal cortex were “almost entirely absent,” supporting a predominantly null finding, but not the claim that results in these areas were only null; the paper also does not say that dozens of patients had stimulation in those specific regions. (LLM, conf=0.88)
Experimental — accuracy not yet measuredThere 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.
“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
The Discussion (page not provided) describes “almost total quiescence” following iES in some regions, especially the anterior prefrontal cortex, supporting the claim that noticeable effects there were particularly rare. But the paper does not establish that it is less likely to elicit an effect than every other part of the brain: its comparisons are primarily across sampled cortical networks, and the Methods say subcortical regions were excluded. (LLM, conf=0.86)
Experimental — accuracy not yet measuredThe low elicitation rate (17%) in OFC is in marked contrast to unimodal brain regions, where positive response rates can reach 67%.
“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
The Results section reports markedly higher elicitation rates in unimodal somatomotor and visual networks than in lower-rate networks, supporting the comparison. It gives rates of 55% and 52% for those unimodal networks, however, and the passages available from our copy do not establish a 67% rate. The paper also does not establish the citing document’s 17% OFC figure in these passages. Page numbers were not provided. (LLM, conf=0.83)
Experimental — accuracy not yet measuredSham stimulation is a very effective control for demand characteristics in iES.
“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
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, and these trends appear to be driven by the brain's intrinsic network architecture.
“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
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.
“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
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.
“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
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.
“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
One major caveat is that iES to the PFC might still be influencing consciousness, but in subtle ways not noticeable or reportable by patients.
“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
Within NREM sleep, the response to TMS differs according to the subjects' report upon awakening: reports of no dreaming were associated with a larger negative evoked response and shorter phase-locking compared with reports of dreaming.
“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]
The Results and Methods (page unavailable) describe intracranial electrical stimulation during task-free resting states, not TMS during NREM sleep. Searches for NREM sleep, dreaming, awakening, negative evoked responses and phase-locking found no passage addressing the claimed comparison. (LLM, conf=0.76)
Experimental — accuracy not yet measuredThe amplitude of the negative peak, presumably reflecting the degree of neuronal bistability, was inversely correlated with the length of the dream report (word count).
“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]
The Results passages concern patients’ reports after intracranial electrical stimulation and correlations involving brain-network characteristics; the Discussion addresses possible under-reporting of stimulation effects. A search for negative-peak amplitude, neuronal bistability, and dream-report length found no passage in our copy addressing the claimed inverse correlation. No page numbers were available for these passages. (LLM, conf=0.76)
Experimental — accuracy not yet measuredA wide variety of other effects have been reported from ACC stimulation, including digestive sensations, vestibular hallucinations, anxiety and physical pain, and fear in the pregenual ACC.
“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
The Discussion says that stimulation of the anterior cingulate sometimes elicited effects, but does not identify fear or the pregenual ACC. Searches for “fear,” “pregenual,” and negative emotional effects found no passage in our copy establishing the specific effect attributed to Fox et al.; the other effects in the citing sentence have separate citations. (LLM, conf=0.73)
Experimental — accuracy not yet measured
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- 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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