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

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.

Keywords: DBS; PTSD; amygdala; creativity; double consciousness; dreaming; dreamy state; emotion.

FIGURE 1

In this three-dimensional image, Subject 2’s MRI brain imaging studies were registered to the MNI space (MNI152 NLIN2009a) and then overlaid on the structural atlas of Mai (Horn and Kühn, 2015; Mai and Majtanik, 2017). Here we demonstrate the trajectory for each DBS electrode implanted into the head of the HC and amygdala as represented in “MNI space.” The blue regions represent the putamen while the green regions represent the globus pallidus. The white lines represent the DBS leads with four gray regions representing individual electrode contacts. See Figure 2 for precise localization of each contact.

FIGURE 2

To demonstrate locations of each electrode, Subject 2’s MRI brain imaging studies were registered to the MNI space (MNI152 NLIN2009a) and then overlaid on the structural atlas of Mai (Horn and Kühn, 2015; Mai and Majtanik, 2017) to allow delineation of cerebral cortices and subcortical structures with color coded representations of cortical and subcortical parcelation according to the Mai atlas. The red rectangular markers represent right sided DBS electrode contacts 8–11 while the green rectangular markers represent left sided contacts 0–3. Contact 0 was placed in the left HC and contact 8 was placed in the right HC (A). Contact 1 was placed in the left ventral BLA and contact 9 was placed in the right ventral BLA (B). Contact 2 was placed in the left dorsal BLA and contact 10 was placed in the right dorsal BLA (C). Contact 3 was placed in the left CeA and contact 11 was placed in the right CeA (D).