Nim Tottenham1, Myrna M Weissman2, Zhishun Wang3, Virginia Warner4, Marc J Gameroff3, David P Semanek4, Xuejun Hao3, Jay A Gingrich5, Bradley S Peterson6, Jonathan Posner5, Ardesheer Talati7. 1. Department of Psychology, Columbia University, New York, New York; Sackler Institute for Developmental Psychobiology, Columbia University, New York, New York. 2. Sackler Institute for Developmental Psychobiology, Columbia University, New York, New York; Mailman School of Public Health, Columbia University, New York, New York; Department of Psychiatry, Vagelos College of Physicians and Surgeons, Columbia University, New York, New York; New York State Psychiatric Institute, NewYork-Presbyterian/Columbia University Irving Medical Center, New York, New York. 3. Department of Psychiatry, Vagelos College of Physicians and Surgeons, Columbia University, New York, New York; New York State Psychiatric Institute, NewYork-Presbyterian/Columbia University Irving Medical Center, New York, New York. 4. New York State Psychiatric Institute, NewYork-Presbyterian/Columbia University Irving Medical Center, New York, New York. 5. Sackler Institute for Developmental Psychobiology, Columbia University, New York, New York; Department of Psychiatry, Vagelos College of Physicians and Surgeons, Columbia University, New York, New York; New York State Psychiatric Institute, NewYork-Presbyterian/Columbia University Irving Medical Center, New York, New York. 6. Center for the Developing Mind, Saban Research Institute, Children's Hospital Los Angeles, Los Angeles, California; Department of Pediatrics, Keck School of Medicine, University of Southern California, Los Angeles, California; Department of Psychiatry, Keck School of Medicine, University of Southern California, Los Angeles, California. 7. Sackler Institute for Developmental Psychobiology, Columbia University, New York, New York; Department of Psychiatry, Vagelos College of Physicians and Surgeons, Columbia University, New York, New York; New York State Psychiatric Institute, NewYork-Presbyterian/Columbia University Irving Medical Center, New York, New York. Electronic address: Adi.Talati@nyspi.columbia.edu.
Abstract
BACKGROUND: Major depressive disorder (MDD) is associated with aberrant limbic neural responses to emotional stimuli. We assessed how self-generated emotions modulate trial-by-trial limbic activity and whether this brain-emotion synchrony varies by familial MDD risk (regardless of personal MDD history) and neuroticism. METHODS: Participants (n = 74, mean age = 34 years) were later-generation family members of depressed or nondepressed probands as part of a longitudinal cohort study. Using an emotion induction task, we examined participant-specific modulation of anatomically defined limbic neurobiology. Neuroticism, mental health, and familial parenting style were assessed, and MDD assessments were routinely collected throughout the previous longitudinal assessments of the study. RESULTS: Participant-specific emotional arousal modulated amygdala and hippocampal activity. Lasso regression identified attenuated right amygdala arousal modulation as being relatively more associated with neuroticism (even though neuroticism was not associated with arousal ratings). Attenuated amygdala modulation and neuroticism were significantly more likely in offspring of parents with MDD. Parental MDD, but not personal history of MDD, predicted attenuated amygdala modulation. CONCLUSIONS: Attenuated right amygdala modulation by emotional arousal was associated with neuroticism, indicating that the amygdala was less synchronous with emotional experiences in individuals higher in neuroticism. This neurophenotype was predicted by participants' parental MDD history but not by their own MDD history; that is, it was observed in unaffected and affected offspring of parents with MDD. These data suggest that weak amygdala-emotion synchrony may be a predisposing risk factor for MDD, rather than a result of the illness, and they suggest pathways by which this risk factor for depression is passed intergenerationally.
BACKGROUND: Major depressive disorder (MDD) is associated with aberrant limbic neural responses to emotional stimuli. We assessed how self-generated emotions modulate trial-by-trial limbic activity and whether this brain-emotion synchrony varies by familial MDD risk (regardless of personal MDD history) and neuroticism. METHODS: Participants (n = 74, mean age = 34 years) were later-generation family members of depressed or nondepressed probands as part of a longitudinal cohort study. Using an emotion induction task, we examined participant-specific modulation of anatomically defined limbic neurobiology. Neuroticism, mental health, and familial parenting style were assessed, and MDD assessments were routinely collected throughout the previous longitudinal assessments of the study. RESULTS: Participant-specific emotional arousal modulated amygdala and hippocampal activity. Lasso regression identified attenuated right amygdala arousal modulation as being relatively more associated with neuroticism (even though neuroticism was not associated with arousal ratings). Attenuated amygdala modulation and neuroticism were significantly more likely in offspring of parents with MDD. Parental MDD, but not personal history of MDD, predicted attenuated amygdala modulation. CONCLUSIONS: Attenuated right amygdala modulation by emotional arousal was associated with neuroticism, indicating that the amygdala was less synchronous with emotional experiences in individuals higher in neuroticism. This neurophenotype was predicted by participants' parental MDD history but not by their own MDD history; that is, it was observed in unaffected and affected offspring of parents with MDD. These data suggest that weak amygdala-emotion synchrony may be a predisposing risk factor for MDD, rather than a result of the illness, and they suggest pathways by which this risk factor for depression is passed intergenerationally.
Authors: Johan Ormel; A Bastiaansen; Harriëtte Riese; Elisabeth H Bos; Michelle Servaas; Mark Ellenbogen; Judith G M Rosmalen; André Aleman Journal: Neurosci Biobehav Rev Date: 2012-10-12 Impact factor: 8.989
Authors: David Pagliaccio; Joan Luby; Mike Gaffrey; Andrew Belden; Kelly Botteron; Ian H Gotlib; Deanna M Barch Journal: Dev Cogn Neurosci Date: 2011-12-24 Impact factor: 6.464
Authors: Lisanne M Jenkins; Kristy A Skerrett; Sophie R DelDonno; Víctor G Patrón; Kortni K Meyers; Scott Peltier; Jon-Kar Zubieta; Scott A Langenecker; Monica N Starkman Journal: Psychiatry Res Neuroimaging Date: 2018-03-05 Impact factor: 2.376
Authors: Victoria B Risbrough; Dewleen G Baker; Daniel M Stout; Alan N Simmons; Caroline M Nievergelt; Arpi Minassian; Nilima Biswas; Adam X Maihofer Journal: Neuropsychopharmacology Date: 2022-03-28 Impact factor: 8.294