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Author Notes:

Jon T. Willie, Department of Neurological Surgery, Emory University School of Medicine, 1365 Clifton Road, Suite B6200, Atlanta, GA 30322, jon.t.willie@emory.edu

C.S.I., K.R.B., D.I.B, S.H., and J.T.W. contributed to the study design; C.S.I., K.R.B., D.I.B., R.F., and J.T.W. contributed to the data collection; J.T.W. and R.E.G. conducted the surgeries; C.S.I., K.R.B., and J.T.W. contributed to the electrode localization; C.S.I. and K.R.B. performed the behavioral, psychophysiological, and statistical analyses; K.R.B. designed the mixed linear models; C.S.I, K.R.B., S.H., and J.T.W. contributed to the interpretation; C.S.I., K.R.B., S.H., and J.T.W. wrote the manuscript; C.S.I., J.T.W., K.R.B., D.I.B., R.E.G., and S.H. edited the manuscript.

All authors discussed and commented on the manuscript.

We would like to thank the patients, physicians, and staff of the Emory University Hospital Epilepsy Monitoring Unit for their contributions to this project.

We also thank Nigel Pedersen for helpful conversation and providing useful historical brain stimulation context.

Subjects:

Research Funding:

KRB was supported in part by career development awards from the American Foundation for Suicide Prevention and the NIH (KL2TR000455).

JTW was supported in part by career development awards from the Sleep Research Society Foundation and the Neurosurgery Research Education Fund.

Keywords:

  • Amygdala
  • Autonomic reactivity
  • Brain stimulation
  • Electrodermal activity
  • Emotional experience
  • Heart rate
  • Psychophysiology

Human amygdala stimulation effects on emotion physiology and emotional experience

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Journal Title:

Neuropsychologia

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Type of Work:

Article | Post-print: After Peer Review

Abstract:

The amygdala is a key structure mediating emotional processing. Few studies have used direct electrical stimulation of the amygdala in humans to examine stimulation-elicited physiological and emotional responses, and the nature of such effects remains unclear. Determining the effects of electrical stimulation of the amygdala has important theoretical implications for current discrete and dimensional neurobiological theories of emotion, which differ substantially in their predictions about the emotional effects of such stimulation. To examine the effects of amygdala stimulation on physiological and subjective emotional responses we examined epilepsy patients undergoing intracranial EEG monitoring in which depth electrodes were implanted unilaterally or bilaterally in the amygdala. Nine subjects underwent both sham and acute monopolar electrical stimulation at various parameters in electrode contacts located in amygdala and within lateral temporal cortex control locations. Stimulation was applied at either 50 Hz or 130 Hz, while amplitudes were increased stepwise from 1 to 12 V, with subjects blinded to stimulation condition. Electrodermal activity (EDA), heart rate (HR), and respiratory rate (RR) were simultaneously recorded and subjective emotional response was probed after each stimulation period. Amygdala stimulation (but not lateral control or sham stimulation) elicited immediate and substantial dose-dependent increases in EDA and decelerations of HR, generally without affecting RR. Stimulation elicited subjective emotional responses only rarely, and did not elicit clinical seizures in any subject. These physiological results parallel stimulation findings with animals and are consistent with orienting/defensive responses observed with aversive visual stimuli in humans. In summary, these findings suggest that acute amygdala stimulation in humans can be safe and can reliably elicit changes in emotion physiology without significantly affecting subjective emotional experience, providing a useful approach for investigation of amygdala-mediated modulatory effects on cognition.

Copyright information:

© 2018 Elsevier Ltd

This is an Open Access work distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (http://creativecommons.org/licenses/by-nc-nd/4.0/).

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