Acute Effects and the Dreamy State Evoked by Deep Brain Electrical Stimulation of the Amygdala: Associations of the Amygdala in Human Dreaming, Consciousness, Emotions, and Creativity

Accurate localization of complex human experiences such as emotions, dreaming, creativity, and consciousness to specific cerebral structures or neural networks has remained elusive despite technological advances. We report the use of acute deep brain stimulation (DBS) to evoke behavioral and emotion...

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Main Authors: George Lai, Jean-Philippe Langevin, Ralph J. Koek, Scott E. Krahl, Ausaf A. Bari, James W. Y. Chen
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-02-01
Series:Frontiers in Human Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fnhum.2020.00061/full
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author George Lai
George Lai
Jean-Philippe Langevin
Jean-Philippe Langevin
Ralph J. Koek
Ralph J. Koek
Scott E. Krahl
Scott E. Krahl
Ausaf A. Bari
Ausaf A. Bari
James W. Y. Chen
James W. Y. Chen
author_facet George Lai
George Lai
Jean-Philippe Langevin
Jean-Philippe Langevin
Ralph J. Koek
Ralph J. Koek
Scott E. Krahl
Scott E. Krahl
Ausaf A. Bari
Ausaf A. Bari
James W. Y. Chen
James W. Y. Chen
author_sort George Lai
collection DOAJ
description Accurate localization of complex human experiences such as emotions, dreaming, creativity, and consciousness to specific cerebral structures or neural networks has remained elusive despite technological advances. We report the use of acute deep brain stimulation (DBS) to evoke behavioral and emotional effects by applying electrical stimulation (ES) at various voltage strengths to the basolateral and central subnuclei of the amygdala in addition to the head of hippocampus (HC) for two subjects with medically refractory post-traumatic stress disorder (PTSD). Our results suggest that the amygdala could be a node in a neural network responsible for the generation of complex vivid mental imagery and integrated sensory experiences similar to John Hughlings Jackson’s “dreamy state” and “double consciousness,” which have been classically associated with temporal lobe epilepsy during uncinate seizures. That we were able to elicit similar vivid, dynamic, complex, bizarre, and original mental imagery with ES in non-epileptic subjects suggests that Jackson’s seizure related “dreamy state” and “double consciousness” may arise from heightened innate brain mechanisms with the amygdala acting as a node in the neural network responsible for physiologic dreaming and creative functions. Furthermore, our subjects experienced different emotions with different stimulation strengths at various electrode contacts. Our results suggest that higher voltage stimulation of the amygdala and HC at 4–5 V leads to predominantly negative responses and 2–4 V stimulation showed inversely coupled positive and negative responses of the amygdala in either hemisphere which may imply hemispheric dominance of emotional valences without relation to handedness. Due to the unique and complex responses dependent on location and strength of stimulation, we advise that all patients receiving DBS of the amygdala undergo acute stimulation mapping in a monitored setting before selecting therapeutic parameters for chronic stimulation.
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spelling doaj.art-71258088245a4c0fbcf1dfd1280b760d2022-12-21T18:30:31ZengFrontiers Media S.A.Frontiers in Human Neuroscience1662-51612020-02-011410.3389/fnhum.2020.00061464286Acute Effects and the Dreamy State Evoked by Deep Brain Electrical Stimulation of the Amygdala: Associations of the Amygdala in Human Dreaming, Consciousness, Emotions, and CreativityGeorge Lai0George Lai1Jean-Philippe Langevin2Jean-Philippe Langevin3Ralph J. Koek4Ralph J. Koek5Scott E. Krahl6Scott E. Krahl7Ausaf A. Bari8Ausaf A. Bari9James W. Y. Chen10James W. Y. Chen11Neurology Service, VA Greater Los Angeles Healthcare System, Los Angeles, CA, United StatesDepartment of Neurology, University of California, Los Angeles, Los Angeles, CA, United StatesNeurosurgery Service, VA Greater Los Angeles Healthcare System, Los Angeles, CA, United StatesDepartment of Neurosurgery, University of California, Los Angeles, Los Angeles, CA, United StatesPsychiatry and Mental Health Service, VA Greater Los Angeles Healthcare System, Los Angeles, CA, United StatesDepartment of Psychiatry and Behavior Sciences, University of California, Los Angeles, Los Angeles, CA, United StatesDepartment of Neurosurgery, University of California, Los Angeles, Los Angeles, CA, United StatesResearch and Development, VA Greater Los Angeles Healthcare System, Los Angeles, CA, United StatesNeurosurgery Service, VA Greater Los Angeles Healthcare System, Los Angeles, CA, United StatesDepartment of Neurosurgery, University of California, Los Angeles, Los Angeles, CA, United StatesNeurology Service, VA Greater Los Angeles Healthcare System, Los Angeles, CA, United StatesDepartment of Neurology, University of California, Los Angeles, Los Angeles, CA, United StatesAccurate localization of complex human experiences such as emotions, dreaming, creativity, and consciousness to specific cerebral structures or neural networks has remained elusive despite technological advances. We report the use of acute deep brain stimulation (DBS) to evoke behavioral and emotional effects by applying electrical stimulation (ES) at various voltage strengths to the basolateral and central subnuclei of the amygdala in addition to the head of hippocampus (HC) for two subjects with medically refractory post-traumatic stress disorder (PTSD). Our results suggest that the amygdala could be a node in a neural network responsible for the generation of complex vivid mental imagery and integrated sensory experiences similar to John Hughlings Jackson’s “dreamy state” and “double consciousness,” which have been classically associated with temporal lobe epilepsy during uncinate seizures. That we were able to elicit similar vivid, dynamic, complex, bizarre, and original mental imagery with ES in non-epileptic subjects suggests that Jackson’s seizure related “dreamy state” and “double consciousness” may arise from heightened innate brain mechanisms with the amygdala acting as a node in the neural network responsible for physiologic dreaming and creative functions. Furthermore, our subjects experienced different emotions with different stimulation strengths at various electrode contacts. Our results suggest that higher voltage stimulation of the amygdala and HC at 4–5 V leads to predominantly negative responses and 2–4 V stimulation showed inversely coupled positive and negative responses of the amygdala in either hemisphere which may imply hemispheric dominance of emotional valences without relation to handedness. Due to the unique and complex responses dependent on location and strength of stimulation, we advise that all patients receiving DBS of the amygdala undergo acute stimulation mapping in a monitored setting before selecting therapeutic parameters for chronic stimulation.https://www.frontiersin.org/article/10.3389/fnhum.2020.00061/fullDBSdreamy statedouble consciousnessdreamingemotioncreativity
spellingShingle George Lai
George Lai
Jean-Philippe Langevin
Jean-Philippe Langevin
Ralph J. Koek
Ralph J. Koek
Scott E. Krahl
Scott E. Krahl
Ausaf A. Bari
Ausaf A. Bari
James W. Y. Chen
James W. Y. Chen
Acute Effects and the Dreamy State Evoked by Deep Brain Electrical Stimulation of the Amygdala: Associations of the Amygdala in Human Dreaming, Consciousness, Emotions, and Creativity
Frontiers in Human Neuroscience
DBS
dreamy state
double consciousness
dreaming
emotion
creativity
title Acute Effects and the Dreamy State Evoked by Deep Brain Electrical Stimulation of the Amygdala: Associations of the Amygdala in Human Dreaming, Consciousness, Emotions, and Creativity
title_full Acute Effects and the Dreamy State Evoked by Deep Brain Electrical Stimulation of the Amygdala: Associations of the Amygdala in Human Dreaming, Consciousness, Emotions, and Creativity
title_fullStr Acute Effects and the Dreamy State Evoked by Deep Brain Electrical Stimulation of the Amygdala: Associations of the Amygdala in Human Dreaming, Consciousness, Emotions, and Creativity
title_full_unstemmed Acute Effects and the Dreamy State Evoked by Deep Brain Electrical Stimulation of the Amygdala: Associations of the Amygdala in Human Dreaming, Consciousness, Emotions, and Creativity
title_short Acute Effects and the Dreamy State Evoked by Deep Brain Electrical Stimulation of the Amygdala: Associations of the Amygdala in Human Dreaming, Consciousness, Emotions, and Creativity
title_sort acute effects and the dreamy state evoked by deep brain electrical stimulation of the amygdala associations of the amygdala in human dreaming consciousness emotions and creativity
topic DBS
dreamy state
double consciousness
dreaming
emotion
creativity
url https://www.frontiersin.org/article/10.3389/fnhum.2020.00061/full
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