Electric field causes volumetric changes in the human brain
- The Zucker Hillside Hospital, United States
- University of Bergen, Norway
- National Institute of Mental Health, United States
- University of California, Los Angeles, United States
- The City College of the City University of New York, United States
- University of California, San Diego, United States
- Bellvitge University Hospital-IDIBELL, Spain
- University of Muenster, Germany
- GGZinGeest, Old Age Psychiatry, Amsterdam Neuroscience, Netherlands
- Keio University School of Medicine, Japan
- University Psychiatric Center - KU Leuven, Belgium
- Carlos III Health Institute, Spain
- Radboud University Medical Center, Netherlands
- University of New Mexico School of Medicine, 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.
Data availability
Source data files (.csv) including processed data have been provided for Figures 1-4, Figure 3-figure supplement 1 and Figure 4-figure supplement 1. Raw data cannot be made available publicly because we do not have consent or ethical approval for this and the data cannot be anonymised. The data is stored on a secure centralized server at the Univerity of Bergen, Norway. Participating GEMRIC sites have access to the raw data according to specific data policy and safety rules of the consortium, and in accord with the approval from the ethical committee. The GEMRIC consortium welcomes new members who are interested in the neuroimaging research of ECT. We hold board meetings twice a year when new members can apply to join and gain access to the database available on the GEMRIC servers. For more about the application process please visit https://mmiv.no/how-to-join-gemric/ or write to Leif Oltedal (leif.oltedal@uib.no). General information about the consortium can be found on the following website: https://mmiv.no/gemric/. For transparency and reproducibility, the entire analytical approach is uploaded to the https://github.com/argyelan/Publications/tree/master/ECTEFvsVOLUME (R scripts in org mode), and also was uploaded to eLife.
Article and author information
Author details
Funding
National Institute of Mental Health (MH092301)
- Randall Espinoza
- Katherine L Narr
National Institute of Mental Health (ZIAMH00295)
- Zhi-De Deng
National Institute of Mental Health (MH119616)
- Miklos Argyelan
National Institute of Mental Health (MH111826)
- Christopher Abbott
National Institute of Mental Health (MH110008)
- Randall Espinoza
- Katherine L Narr
National Institute of Mental Health (MH102743)
- Randall Espinoza
- Katherine L Narr
Western Norway Regional Health Authority (911986)
- Ketil J Oedegaard
Western Norway Regional Health Authority (912238)
- Leif Oltedal
Deutsche Forschungsgemeinschaft (DFG FOR2107 DA1151/5-1 and DA1151/5-2)
- Udo Dannlowski
Deutsche Forschungsgemeinschaft (SFB-TRR58)
- Udo Dannlowski
Deutsche Forschungsgemeinschaft (Projects C09 and Z02)
- Udo Dannlowski
Innovative Medical Research (RE111604 and RE111722)
- Ronny Redlich
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Human subjects: All sites' contributing data received approval by their local ethical committees or institutional review board, and the centralized mega-analysis was approved by the Regional Ethics Committee South-East in Norway (2013/1032 ECT and Neuroradiology, June 1, 2015).
Copyright
This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.
Metrics
-
- 2,853
- views
-
- 355
- downloads
-
- 64
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Electric field causes volumetric changes in the human brain
eLife 8:e49115.
https://doi.org/10.7554/eLife.49115
Further reading
-
- Neuroscience
Spiny projection neurons (SPNs) in dorsal striatum are often proposed as a locus of reinforcement learning in the basal ganglia. Here, we identify and resolve a fundamental inconsistency between striatal reinforcement learning models and known SPN synaptic plasticity rules. Direct-pathway (dSPN) and indirect-pathway (iSPN) neurons, which promote and suppress actions, respectively, exhibit synaptic plasticity that reinforces activity associated with elevated or suppressed dopamine release. We show that iSPN plasticity prevents successful learning, as it reinforces activity patterns associated with negative outcomes. However, this pathological behavior is reversed if functionally opponent dSPNs and iSPNs, which promote and suppress the current behavior, are simultaneously activated by efferent input following action selection. This prediction is supported by striatal recordings and contrasts with prior models of SPN representations. In our model, learning and action selection signals can be multiplexed without interference, enabling learning algorithms beyond those of standard temporal difference models.
-
- Neuroscience
Binge drinking is common among adolescents despite mounting evidence linking it to various adverse health outcomes that include heightened pain perception. The prelimbic (PrL) cortex is vulnerable to insult from adolescent alcohol exposure and receives input from the basolateral amygdala (BLA) while sending projections to the ventrolateral periaqueductal gray (vlPAG) – two brain regions implicated in nociception. In this study, adolescent intermittent ethanol (AIE) exposure was carried out in male and female rats using a vapor inhalation procedure. Assessments of mechanical and thermal sensitivity revealed that AIE exposure-induced protracted mechanical allodynia. To investigate synaptic function at BLA inputs onto defined populations of PrL neurons, retrobeads and viral labeling were combined with optogenetics and slice electrophysiology. Recordings from retrobead labeled cells in the PrL revealed AIE reduced BLA-driven feedforward inhibition of neurons projecting from the PrL to the vlPAG, resulting in augmented excitation/inhibition (E/I) balance and increased intrinsic excitability. Consistent with this finding, recordings from virally tagged PrL parvalbumin interneurons (PVINs) demonstrated that AIE exposure reduced both E/I balance at BLA inputs onto PVINs and PVIN intrinsic excitability. These findings provide compelling evidence that AIE alters synaptic function and intrinsic excitability within a prefrontal nociceptive circuit.
