Complex negative emotions induced by electrical stimulation of the human hypothalamus
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...
| Main Authors: | , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2022-05-01
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| Series: | Brain Stimulation |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S1935861X22000687 |
| _version_ | 1818235117028507648 |
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| author | 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 |
| author_facet | 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 |
| author_sort | Josef Parvizi |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-12-12T11:48:52Z |
| format | Article |
| id | doaj.art-5674e1d10ae143c1895d079a2cf5efd2 |
| institution | Directory Open Access Journal |
| issn | 1935-861X |
| language | English |
| last_indexed | 2024-12-12T11:48:52Z |
| publishDate | 2022-05-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Brain Stimulation |
| spelling | doaj.art-5674e1d10ae143c1895d079a2cf5efd22022-12-22T00:25:23ZengElsevierBrain Stimulation1935-861X2022-05-01153615623Complex negative emotions induced by electrical stimulation of the human hypothalamusJosef Parvizi0Michael J. Veit1Daniel A.N. Barbosa2Aaron Kucyi3Claire Perry4Jonathon J. Parker5Rajat S. Shivacharan6Fengyixuan Chen7Jennifer Yih8James J. Gross9Robert Fisher10Jennifer A. McNab11Jessica Falco-Walter12Casey H. Halpern13Laboratory 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.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, USADepartment of Neurosurgery, Stanford University School of Medicine, Palo Alto, CA, USALaboratory 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, USALaboratory 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, USADepartment of Neurosurgery, Stanford University School of Medicine, Palo Alto, CA, USADepartment of Neurosurgery, Stanford University School of Medicine, Palo Alto, CA, USALaboratory of Behavioral and Cognitive Neuroscience, Stanford University School of Medicine, Palo Alto, CA, USALaboratory of Behavioral and Cognitive Neuroscience, Stanford University School of Medicine, Palo Alto, CA, USADepartment of Psychology, Stanford University, Palo Alto, CA, USADepartment of Neurology and Neurological Sciences, Stanford University School of Medicine, Palo Alto, CA, USADepartment of Radiology, Stanford University School of Medicine, Palo Alto, CA, USADepartment of Neurology and Neurological Sciences, Stanford University School of Medicine, Palo Alto, CA, USADepartment of Neurosurgery, Stanford University School of Medicine, Palo Alto, CA, USABackground: 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.http://www.sciencedirect.com/science/article/pii/S1935861X22000687SubjectivityDepressionEEGEmotionHypothalamic nucleiFeelings |
| spellingShingle | 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 Complex negative emotions induced by electrical stimulation of the human hypothalamus Brain Stimulation Subjectivity Depression EEG Emotion Hypothalamic nuclei Feelings |
| title | Complex negative emotions induced by electrical stimulation of the human hypothalamus |
| title_full | Complex negative emotions induced by electrical stimulation of the human hypothalamus |
| title_fullStr | Complex negative emotions induced by electrical stimulation of the human hypothalamus |
| title_full_unstemmed | Complex negative emotions induced by electrical stimulation of the human hypothalamus |
| title_short | Complex negative emotions induced by electrical stimulation of the human hypothalamus |
| title_sort | complex negative emotions induced by electrical stimulation of the human hypothalamus |
| topic | Subjectivity Depression EEG Emotion Hypothalamic nuclei Feelings |
| url | http://www.sciencedirect.com/science/article/pii/S1935861X22000687 |
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