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; Robert Fisher; Jennifer A. McNab; Jessica Falco-Walter; Casey H. Halpern

Brain Stimulation (May 2022)

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,
Robert Fisher,
Jennifer A. McNab,
Jessica Falco-Walter,
Casey H. Halpern

Affiliations

Josef Parvizi: Laboratory of Behavioral and Cognitive Neuroscience, Stanford University School of Medicine, Palo Alto, CA, USA; Department of Neurology and Neurological Sciences, Stanford University School of Medicine, Palo Alto, CA, USA; Department of Neurosurgery, Stanford University School of Medicine, Palo Alto, CA, USA; Corresponding author.Department of Neurology and Neurological Sciences, Stanford University, 500 Pasteur Drive, Stanford, CA, 94305, USA.
Michael J. Veit: Laboratory of Behavioral and Cognitive Neuroscience, Stanford University School of Medicine, Palo Alto, CA, USA; Department of Neurology and Neurological Sciences, Stanford University School of Medicine, Palo Alto, CA, USA
Daniel A.N. Barbosa: Department of Neurosurgery, Stanford University School of Medicine, Palo Alto, CA, USA
Aaron Kucyi: Laboratory of Behavioral and Cognitive Neuroscience, Stanford University School of Medicine, Palo Alto, CA, USA; Department of Neurology and Neurological Sciences, Stanford University School of Medicine, Palo Alto, CA, USA
Claire Perry: Laboratory of Behavioral and Cognitive Neuroscience, Stanford University School of Medicine, Palo Alto, CA, USA; Department of Neurology and Neurological Sciences, Stanford University School of Medicine, Palo Alto, CA, USA
Jonathon J. Parker: Department of Neurosurgery, Stanford University School of Medicine, Palo Alto, CA, USA
Rajat S. Shivacharan: Department of Neurosurgery, Stanford University School of Medicine, Palo Alto, CA, USA
Fengyixuan Chen: Laboratory of Behavioral and Cognitive Neuroscience, Stanford University School of Medicine, Palo Alto, CA, USA
Jennifer Yih: Laboratory of Behavioral and Cognitive Neuroscience, Stanford University School of Medicine, Palo Alto, CA, USA
James J. Gross: Department of Psychology, Stanford University, Palo Alto, CA, USA
Robert Fisher: Department of Neurology and Neurological Sciences, Stanford University School of Medicine, Palo Alto, CA, USA
Jennifer A. McNab: Department of Radiology, Stanford University School of Medicine, Palo Alto, CA, USA
Jessica Falco-Walter: Department of Neurology and Neurological Sciences, Stanford University School of Medicine, Palo Alto, CA, USA
Casey H. Halpern: Department of Neurosurgery, Stanford University School of Medicine, Palo Alto, CA, USA

Journal volume & issue: Vol. 15, no. 3
pp. 615 – 623

Abstract

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Background: 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. Objective: 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. Methods: 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). Results: 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. Conclusion: 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.

Published in Brain Stimulation

ISSN: 1935-861X (Print); 1876-4754 (Online)
Publisher: Elsevier
Country of publisher: United States
LCC subjects: Medicine: Internal medicine: Neurosciences. Biological psychiatry. Neuropsychiatry
Website: https://www.journals.elsevier.com/brain-stimulation

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