Abstract

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.

Highlights

  • MATERIALS AND METHODSHuman brain mapping began as early as the 1800 s and was expanded by Wilder Penfield’s and Herbert Jasper’s use of cortical electrical stimulation (ES) in awake patients (Ritaccio et al, 2018)

  • Several intriguing findings were noted with the acute deep brain stimulation (DBS) of the amygdala in subjects with refractory posttraumatic stress disorder (PTSD): (1) Acute ES effects correlate well with the onset and offset of the stimulation

  • (4) Adverse responses are predominantly noted at high-voltage stimulation (4–5 V). (5) Dreamy state and double consciousness were elicited during the ES in these two subjects without epilepsy

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Summary

MATERIALS AND METHODS

Human brain mapping began as early as the 1800 s and was expanded by Wilder Penfield’s and Herbert Jasper’s use of cortical electrical stimulation (ES) in awake patients (Ritaccio et al, 2018). During acute amygdala ES, both of our awake subjects maintained full awareness of reality while simultaneously experiencing vivid mental imagery associated with auditory, visual, tactile, and olfactory sensations involving autobiographical or original contents with emotional valence. These phenomena were analogous to those associated with uncinate seizures described by John Hughlings Jackson as “dreamy state” and “double consciousness,” which are classically associated with temporal lobe epilepsy (TLE) (Hogan and Kaiboriboon, 2003). Experiences suggesting creativity were identified by the production of not-previously experienced original content

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