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Complex negative emotions induced by electrical stimulation of the human hypothalamus
Journal article   Open access   Peer reviewed

Complex negative emotions induced by electrical stimulation of the human hypothalamus

Josef Parvizi, Michael J. Veit, Daniel A.N. Barbosa, Aaron Kucyi, Claire Perry, Jonathon J. Parker, Rajat S. Shivacharan, Fengyixuan Chen, Jennifer Yih, James J. Gross, …
Brain stimulation, v 15(3), pp 615-623
01 May 2022
PMID: 35413481
url
https://doi.org/10.1016/j.brs.2022.04.008View
Published, Version of Record (VoR) Open

Abstract

Affect Depression EEG Emotion Feelings Hypothalamic nuclei Subjectivity VMH nucleus of hypothalamus
Stimulation of the ventromedial hypothalamic region in animals has been reported to cause attack behavior labeled as sham-rage without offering information about the internal affective state of the animal being stimulated. To examine the causal effect of electrical stimulation near the ventromedial region of the human hypothalamus on the human subjective experience and map the electrophysiological connectivity of the hypothalamus with other brain regions. We examined a patient (Subject S20_150) with intracranial electrodes implanted across 170 brain regions, including the hypothalamus. We combined direct electrical stimulation with tractography, cortico-cortical evoked potentials (CCEP), and functional connectivity using resting state intracranial electroencephalography (EEG). Recordings in the hypothalamus did not reveal any epileptic abnormalities. Electrical stimulations near the ventromedial hypothalamus induced profound shame, sadness, and fear but not rage or anger. When repeated single-pulse stimulations were delivered to the hypothalamus, significant responses were evoked in the amygdala, hippocampus, ventromedial-prefrontal and orbitofrontal cortices, anterior cingulate, as well as ventral-anterior and dorsal-posterior insula. The time to first peak of these evoked responses varied and earliest propagations correlated best with the measures of resting-state EEG connectivity and structural connectivity. This patient's case offers details about the affective state induced by the stimulation of the human hypothalamus and provides causal evidence relevant to current theories of emotion. The complexity of affective state induced by the stimulation of the hypothalamus and the profile of hypothalamic electrophysiological connectivity suggest that the hypothalamus and its connected structures ought to be seen as causally important for human affective experience. •We studied a patient with 170 electrodes in the brain including the hypothalamus.•Hypothalamic stimulation caused profound change in subject's affective state.•Confirmed findings with dose effect and sham stimulations.•Mapped propagation of signals from the hypothalamic site to other brain sites.•Propagation of electrical current correlated with measures of resting connectivity.

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Web of Science research areas
Clinical Neurology
Neurosciences
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