Forced conceptual thought induced by electrical stimulation of the left prefrontal gyrus involves widespread neural networks
Open accessAbstract
Background Early accounts of forced thought were reported at the onset of a focal seizure, and characterized as vague, repetitive, and involuntary intellectual auras distinct from perceptual or psychic hallucinations or illusions. Here, we examine the neural underpinnings involved in conceptual thought by presenting a series of 3 patients with epilepsy reporting intrusive thoughts during electrical stimulation of the left lateral prefrontal cortex (PFC) during invasive surgical evaluation. We illustrate the widespread networks involved through two independent brain imaging modalities: resting state functional magnetic resonance imaging (fMRI) (rs-fMRI) and task-based meta-analytic connectivity modeling (MACM). Methods We report the clinical and stimulation characteristics of three patients with left hemispheric language dominance who demonstrate forced thought with functional mapping. To examine the brain networks underlying this phenomenon, we used the regions of interest (ROI) centered at the active electrode pairs. We modeled functional networks using two approaches: (1) rs-fMRI functional connectivity analysis, representing 81 healthy controls and (2) meta-analytic connectivity modeling (MACM), representing 8260 healthy subjects. We also determined the overlapping regions between these three subjects' rs-fMRI and MACM networks through a conjunction analysis. Results We identified that left PFC was associated with a large-scale functional network including frontal, temporal, and parietal regions, a network that has been associated with multiple cognitive functions including semantics, speech, attention, working memory, and explicit memory. Conclusions We illustrate the neural networks involved in conceptual thought through a unique patient population and argue that PFC supports this function through activation of a widespread network.
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In another patient, complex auditory phenomena were reported following stimulation to a posterior VLPFC site; similar effects in neighboring superior temporal gyrus suggest the isolated effect may be due to close anatomic proximity of auditory regions in the temporal lobe.
“Lastly, in another patient, the authors reported “complex auditory phenomena” following stimulation to a posterior VLPFC site.However, similar effects were reported in the neighboring electrode pairs in the superior temporal gurus, suggesting that this isolated effect may be because of the close anatomic proximity of auditory regions in the temporal lobe.”
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 A. Liu et al., 2020
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Experimental — accuracy not yet measuredIn one patient, stimulation to the left VLPFC elicited conceptual thoughts about a game that kids play in the summer.
“For instance, 1 patient reported conceptual thoughts following stimulation to the left VLPFC: “I had a thought about a game that kids play in the summer, I can't think of the exact game.””
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 A. Liu et al., 2020
In another patient, stimulation of the left DLPFC and middle frontal gyrus elicited thoughts about a person; the patient could not describe the person's physical characteristics and confirmed the experience was not visual.
“In another patient, stimulation of the left DLPFC and middle frontal gyrus elicited thoughts about “a person.”In contrast to the reports by Blanke et al. (2000), the patient was not able to describe the person's physical characteristics and confirmed that the experience was not visual in nature.”
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 A. Liu et al., 2020
A. Liu et al. (2020) described 3 patients who reported conceptual thoughts following lateral PFC stimulation.
“A. Liu et al. (2020) described 3 patients who reported conceptual thoughts following lateral PFC stimulation (Fig. 4).”
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 A. Liu et al., 2020
Stimulation at comparable anatomic sites in the left DLPFC and VLPFC yielded marked changes in thought content without any reported changes in perceptual experience.
“Importantly, this interpretation is challenged by recent evidence showing that stimulation at comparable anatomic sites in the left DLPFC and VLPFC yielded marked changes in thought content without any reported changes in perceptual experience (A. Liu 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 A. Liu et al., 2020
There are isolated case reports of thoughts and visual hallucinations elicited by iES of the more ventral and posterior portions of the lateral PFC.
“There are exceptions to this general trend, however, with some isolated case reports of thoughts (Popa et al., 2016;A. Liu et al., 2020) and visual hallucinations (Blanke et al., 2000;Vignal et al., 2000) elicited by iES of the more ventral and posterior portions of the lateral PFC (Fig. 4).”
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 A. Liu et al., 2020
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- Authors
- Liu, A., Friedman, D., Barron, D. S., Wang, X., Thesen, T., & Dugan, P.
- Affiliations
- NYU Langone Health (US)
- Yale University (US)
- Corresponding author
- Liu, Anli
- Friedman, Daniel
- Barron, Daniel S.
- Wang, Xiuyuan
- Thesen, Thomas
- Dugan, Patricia
- Venue
- Epilepsy & Behavior
- Publisher
- Elsevier BV
- Published
- 2020-03
- Volume
- 104
- Issue
- Pt A
- Pages
- 106644
- ISSN
- 1525-5050 (ISSN-L)
- PMC
- PMC7172015
- OpenAlex
- W3000225586
- Cited by
- 8
- References
- 54
- Citations by year
- 2026: 2 · 2024: 3 · 2022: 1 · 2021: 2
- FWCI
- 0.40
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Epilepsy & Behavior (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Health Sciences › Medicine › Psychiatry and Mental health › Epilepsy research and treatment
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neurobiology of Language and Bilingualism
- Keywords
- left prefrontal cortex, electrical stimulation, epilepsy, conceptual thinking, semantic processing, functional connectivity, large-scale brain networks, meta-analytic connectivity modeling, resting-state functional connectivity, language dominance
- MeSH terms
- Adult, Brain Mapping, Electric Stimulation, Epilepsy, Female, Humans, Magnetic Resonance Imaging, Male, Memory, Short-Term, Nerve Net, Retrospective Studies, Thinking, Prefrontal Cortex
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