Electric field causes volumetric changes in the human brain

Miklos Argyelan; Leif Oltedal; Zhi-De Deng; Benjamin Wade; Marom Bikson; Andrea Joanlanne; Sohag Sanghani; Hauke Bartsch; Marta Cano; Anders M Dale; Udo Dannlowski; Annemiek Dols; Verena Enneking; Randall Espinoza; Ute Kessler; Katherine L Narr; Ketil J Oedegaard; Mardien L Oudega; Ronny Redlich; Max L Stek; Akihiro Takamiya; Louise Emsell; Filip Bouckaert; Pascal Sienaert; Jesus Pujol; Indira Tendolkar; Philip van Eijndhoven; Georgios Petrides; Anil K Malhotra; Christopher Abbott

doi:10.7554/eLife.49115

Electric field causes volumetric changes in the human brain

Elife. 2019 Oct 23:8:e49115. doi: 10.7554/eLife.49115.

Authors

Miklos Argyelan^{1

2

3}, Leif Oltedal^{4

5}, Zhi-De Deng⁶, Benjamin Wade⁷, Marom Bikson⁸, Andrea Joanlanne¹, Sohag Sanghani¹, Hauke Bartsch^{5

9}, Marta Cano^{10

11}, Anders M Dale^{9

12

13}, Udo Dannlowski¹⁴, Annemiek Dols¹⁵, Verena Enneking¹⁴, Randall Espinoza^{16

17}, Ute Kessler^{4

18}, Katherine L Narr^{16

17}, Ketil J Oedegaard^{4

18}, Mardien L Oudega¹⁵, Ronny Redlich¹⁴, Max L Stek¹⁵, Akihiro Takamiya^{19

20}, Louise Emsell²¹, Filip Bouckaert^{21

22}, Pascal Sienaert²², Jesus Pujol^{11

23}, Indira Tendolkar^{24

25

26}, Philip van Eijndhoven^{24

25}, Georgios Petrides^{1

2

3}, Anil K Malhotra^{1

2

3}, Christopher Abbott²⁷

Affiliations

¹ Department of Psychiatry, The Zucker Hillside Hospital, Glen Oaks, United States.
² Center for Neuroscience, Feinstein Institute for Medical Research, Manhasset, United States.
³ Department of Psychiatry, Zucker School of Medicine, Hempstead, United States.
⁴ Department of Clinical Medicine, University of Bergen, Bergen, Norway.
⁵ Department of Radiology, Haukeland University Hospital, Mohn Medical Imaging and Visualization Centre, Bergen, Norway.
⁶ Experimental Therapeutics and Pathophysiology Branch, National Institute of Mental Health, Bethesda, United States.
⁷ Department of Neurology, Ahmanson-Lovelace Brain Mapping Center, University of California, Los Angeles, Los Angeles, United States.
⁸ Department of Biomedical Engineering, The City College of the City University of New York, New York, United States.
⁹ Center for Multimodal Imaging and Genetics, University of California, San Diego, San Diego, United States.
¹⁰ Department of Psychiatry, Bellvitge University Hospital-IDIBELL, Barcelona, Spain.
¹¹ CIBERSAM, Carlos III Health Institute, Barcelona, Spain.
¹² Department of Radiology, University of California, San Diego, San Diego, United States.
¹³ Department of Neurosciences, University of California, San Diego, San Diego, United States.
¹⁴ Department of Psychiatry and Psychotherapy, University of Muenster, Muenster, Germany.
¹⁵ Department of Psychiatry, Amsterdam UMC, location VUmc, GGZinGeest, Old Age Psychiatry, Amsterdam Neuroscience, Amsterdam, Netherlands.
¹⁶ Department of Neurology, University of California, Los Angeles, Los Angeles, United States.
¹⁷ Department of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles, Los Angeles, United States.
¹⁸ Division of Psychiatry, Haukeland University Hospital, University of Bergen, Bergen, Norway.
¹⁹ Department of Neuropsychiatry, Keio University School of Medicine, Tokyo, Japan.
²⁰ Center for Psychiatry and Behavioral Science, Komagino Hospital, Tokyo, Japan.
²¹ Department of Geriatric Psychiatry, University Psychiatric Center, KU Leuven, Leuven, Belgium.
²² Academic center for ECT and Neurostimulation (AcCENT), University Psychiatric Center, KU Leuven, Kortenberg, Belgium.
²³ MRI Research Unit, Department of Radiology, Hospital del Mar, Barcelona, Spain.
²⁴ Department of Psychiatry, Radboud University Medical Center, Nijmegen, Netherlands.
²⁵ Donders Institute for Brain Cognition and Behavior, Centre for Cognitive Neuroimaging, Nijmegen, Netherlands.
²⁶ Faculty of Medicine and LVR Clinic for Psychiatry and Psychotherapy, University of Duisburg-Essen, Essen, Germany.
²⁷ Department of Psychiatry, University of New Mexico School of Medicine, Albuquerque, United States.

Abstract

Recent longitudinal neuroimaging studies in patients with electroconvulsive therapy (ECT) suggest local effects of electric stimulation (lateralized) occur in tandem with global seizure activity (generalized). We used electric field (EF) modeling in 151 ECT treated patients with depression to determine the regional relationships between EF, unbiased longitudinal volume change, and antidepressant response across 85 brain regions. The majority of regional volumes increased significantly, and volumetric changes correlated with regional electric field (t = 3.77, df = 83, r = 0.38, p=0.0003). After controlling for nuisance variables (age, treatment number, and study site), we identified two regions (left amygdala and left hippocampus) with a strong relationship between EF and volume change (FDR corrected p<0.01). However, neither structural volume changes nor electric field was associated with antidepressant response. In summary, we showed that high electrical fields are strongly associated with robust volume changes in a dose-dependent fashion.

Keywords: ECT; depression; electric field modeling; human; human biology; medicine; neuroimaging; volume change.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Adult
Aged
Amygdala / diagnostic imaging
Amygdala / drug effects
Amygdala / pathology
Amygdala / radiation effects
Antidepressive Agents / therapeutic use
Brain Mapping
Depression / diagnostic imaging
Depression / pathology
Depression / therapy*
Electroconvulsive Therapy / adverse effects*
Electromagnetic Radiation
Female
Hippocampus / diagnostic imaging
Hippocampus / drug effects
Hippocampus / pathology
Hippocampus / radiation effects
Humans
Magnetic Resonance Imaging
Male
Middle Aged
Organ Size / drug effects
Organ Size / radiation effects
Temporal Lobe / diagnostic imaging
Temporal Lobe / drug effects
Temporal Lobe / pathology
Temporal Lobe / radiation effects

Substances

Antidepressive Agents

Abstract

Publication types

MeSH terms

Substances

Grants and funding