Power signatures of habenular neuronal signals in patients with bipolar or unipolar depressive disorders correlate with their disease severity

Abstract The habenula is an epithalamic structure implicated in negative reward mechanisms and plays a downstream modulatory role in regulation of dopaminergic and serotonergic functions. Human and animal studies show its hyperactivity in depression which is curtailed by the antidepressant response...

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Main Authors: Saurabh Sonkusare, Qiong Ding, Yingying Zhang, Linbin Wang, Hengfen Gong, Alekhya Mandali, Luis Manssuer, Yi-Jie Zhao, Yixin Pan, Chencheng Zhang, Dianyou Li, Bomin Sun, Valerie Voon
Format: Article
Language:English
Published: Nature Publishing Group 2022-02-01
Series:Translational Psychiatry
Online Access:https://doi.org/10.1038/s41398-022-01830-3
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author Saurabh Sonkusare
Qiong Ding
Yingying Zhang
Linbin Wang
Hengfen Gong
Alekhya Mandali
Luis Manssuer
Yi-Jie Zhao
Yixin Pan
Chencheng Zhang
Dianyou Li
Bomin Sun
Valerie Voon
author_facet Saurabh Sonkusare
Qiong Ding
Yingying Zhang
Linbin Wang
Hengfen Gong
Alekhya Mandali
Luis Manssuer
Yi-Jie Zhao
Yixin Pan
Chencheng Zhang
Dianyou Li
Bomin Sun
Valerie Voon
author_sort Saurabh Sonkusare
collection DOAJ
description Abstract The habenula is an epithalamic structure implicated in negative reward mechanisms and plays a downstream modulatory role in regulation of dopaminergic and serotonergic functions. Human and animal studies show its hyperactivity in depression which is curtailed by the antidepressant response of ketamine. Deep brain stimulation of habenula (DBS) for major depression have also shown promising results. However, direct neuronal activity of habenula in human studies have rarely been reported. Here, in a cross-sectional design, we acquired both spontaneous resting state and emotional task-induced neuronal recordings from habenula from treatment resistant depressed patients undergoing DBS surgery. We first characterise the aperiodic component (1/f slope) of the power spectrum, interpreted to signify excitation-inhibition balance, in resting and task state. This aperiodicity for left habenula correlated between rest and task and which was significantly positively correlated with depression severity. Time-frequency responses to the emotional picture viewing task show condition differences in beta and gamma frequencies for left habenula and alpha for right habenula. Notably, alpha activity for right habenula was negatively correlated with depression severity. Overall, from direct habenular recordings, we thus show findings convergent with depression models of aberrant excitatory glutamatergic output of the habenula driving inhibition of monoaminergic systems.
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spelling doaj.art-85e44fd63e4844e1ba26827bc4912aa52022-12-22T01:34:04ZengNature Publishing GroupTranslational Psychiatry2158-31882022-02-011211910.1038/s41398-022-01830-3Power signatures of habenular neuronal signals in patients with bipolar or unipolar depressive disorders correlate with their disease severitySaurabh Sonkusare0Qiong Ding1Yingying Zhang2Linbin Wang3Hengfen Gong4Alekhya Mandali5Luis Manssuer6Yi-Jie Zhao7Yixin Pan8Chencheng Zhang9Dianyou Li10Bomin Sun11Valerie Voon12Department of Psychiatry, University of CambridgeDepartment of Neurosurgery, Center for Functional Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of MedicineDepartment of Neurosurgery, Center for Functional Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of MedicineDepartment of Neurosurgery, Center for Functional Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of MedicineShanghai Pudong New Area Mental Health Center, Tongji University School of MedicineDepartment of Psychiatry, University of CambridgeDepartment of Psychiatry, University of CambridgeInstitute of Science and Technology for Brain-Inspired Intelligence, Fudan UniversityDepartment of Neurosurgery, Center for Functional Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of MedicineDepartment of Neurosurgery, Center for Functional Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of MedicineDepartment of Neurosurgery, Center for Functional Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of MedicineDepartment of Neurosurgery, Center for Functional Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of MedicineDepartment of Psychiatry, University of CambridgeAbstract The habenula is an epithalamic structure implicated in negative reward mechanisms and plays a downstream modulatory role in regulation of dopaminergic and serotonergic functions. Human and animal studies show its hyperactivity in depression which is curtailed by the antidepressant response of ketamine. Deep brain stimulation of habenula (DBS) for major depression have also shown promising results. However, direct neuronal activity of habenula in human studies have rarely been reported. Here, in a cross-sectional design, we acquired both spontaneous resting state and emotional task-induced neuronal recordings from habenula from treatment resistant depressed patients undergoing DBS surgery. We first characterise the aperiodic component (1/f slope) of the power spectrum, interpreted to signify excitation-inhibition balance, in resting and task state. This aperiodicity for left habenula correlated between rest and task and which was significantly positively correlated with depression severity. Time-frequency responses to the emotional picture viewing task show condition differences in beta and gamma frequencies for left habenula and alpha for right habenula. Notably, alpha activity for right habenula was negatively correlated with depression severity. Overall, from direct habenular recordings, we thus show findings convergent with depression models of aberrant excitatory glutamatergic output of the habenula driving inhibition of monoaminergic systems.https://doi.org/10.1038/s41398-022-01830-3
spellingShingle Saurabh Sonkusare
Qiong Ding
Yingying Zhang
Linbin Wang
Hengfen Gong
Alekhya Mandali
Luis Manssuer
Yi-Jie Zhao
Yixin Pan
Chencheng Zhang
Dianyou Li
Bomin Sun
Valerie Voon
Power signatures of habenular neuronal signals in patients with bipolar or unipolar depressive disorders correlate with their disease severity
Translational Psychiatry
title Power signatures of habenular neuronal signals in patients with bipolar or unipolar depressive disorders correlate with their disease severity
title_full Power signatures of habenular neuronal signals in patients with bipolar or unipolar depressive disorders correlate with their disease severity
title_fullStr Power signatures of habenular neuronal signals in patients with bipolar or unipolar depressive disorders correlate with their disease severity
title_full_unstemmed Power signatures of habenular neuronal signals in patients with bipolar or unipolar depressive disorders correlate with their disease severity
title_short Power signatures of habenular neuronal signals in patients with bipolar or unipolar depressive disorders correlate with their disease severity
title_sort power signatures of habenular neuronal signals in patients with bipolar or unipolar depressive disorders correlate with their disease severity
url https://doi.org/10.1038/s41398-022-01830-3
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