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Orbitofrontal cortex activity and connectivity predict future depression symptoms in adolescence.

Published on Oct 1, 2017in Biological Psychiatry: Cognitive Neuroscience and Neuroimaging
· DOI :10.1016/J.BPSC.2017.02.002
Jingwen Jin6
Estimated H-index: 6
(SBU: Stony Brook University),
Ananth Narayanan1
Estimated H-index: 1
(SBU: Stony Brook University)
+ 6 AuthorsAprajita Mohanty21
Estimated H-index: 21
(SBU: Stony Brook University)
Abstract
Abstract Background Major depressive disorder is a leading cause of disability worldwide; however, little is known about pathological mechanisms involved in its development. Research in adolescent depression has focused on reward sensitivity and striatal mechanisms implementing it. The contribution of loss sensitivity to future depression, as well as the orbitofrontal cortex (OFC) mechanisms critical for processing losses and rewards, remains unexplored. Furthermore, it is unclear whether OFC functioning interacts with familial history in predicting future depression. Methods In this longitudinal study, we recorded functional magnetic resonance imaging data while 229 female adolescents with or without parental history of depression completed a monetary gambling task. We examined whether OFC blood oxygen level–dependent response and functional connectivity during loss and win feedback was associated with depression symptoms concurrently and prospectively (9 months later) and whether this relationship was moderated by parental history of depression. Results Reduced OFC response during loss was associated with higher depression symptoms concurrently and prospectively, even after controlling for concurrent depression, specifically in adolescents with parental history of depression. Similarly, increased OFC-posterior insula connectivity during loss was associated with future depression symptoms, but this relationship was not moderated by parental history of depression. Conclusions This study provides the first evidence for loss-related alterations in OFC functioning and its interaction with familial history of depression as possible mechanisms in the development of depression. While the current functional magnetic resonance imaging literature has mainly focused on reward, the current findings underscore the need to include prefrontal loss processing in existing developmental models of depression.
  • References (74)
  • Citations (13)
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References74
Newest
#1Xiaoqian J. Chai (McGovern Institute for Brain Research)H-Index: 17
#2Dina R. Hirshfeld-Becker (Harvard University)H-Index: 32
Last. Susan Whitfield-Gabrieli (McGovern Institute for Brain Research)H-Index: 48
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Abstract Background Neuroimaging studies of patients with major depression have revealed abnormal intrinsic functional connectivity measured during the resting state in multiple distributed networks. However, it is unclear whether these findings reflect the state of major depression or reflect trait neurobiological underpinnings of risk for major depression. Methods We compared resting-state functional connectivity, measured with functional magnetic resonance imaging, between unaffected children...
27 CitationsSource
#1Brady D. Nelson (SBU: Stony Brook University)H-Index: 20
#2Greg Perlman (SBU: Stony Brook University)H-Index: 15
Last. Greg Hajcak (SBU: Stony Brook University)H-Index: 71
view all 5 authors...
Objective:A blunted neural response to rewards has recently emerged as a potential mechanistic biomarker of adolescent depression. The reward positivity, an event-related potential elicited by feedback indicating monetary gain relative to loss, has been associated with risk for depression. The authors examined whether the reward positivity prospectively predicted the development of depression 18 months later in a large community sample of adolescent girls.Method:The sample included 444 girls 13....
77 CitationsSource
#1Katherine R. Luking (SBU: Stony Brook University)H-Index: 13
#2David Pagliaccio (NIH: National Institutes of Health)H-Index: 17
Last. M DeannaH-Index: 81
view all 4 authors...
Striatal response to reward has been of great interest in the typical development and psychopathology literatures. These parallel lines of inquiry demonstrate that although typically developing adolescents show robust striatal response to reward, adolescents with major depressive disorder (MDD) and those at high risk for MDD show a blunted response to reward. Understanding how these findings intersect is crucial for the development and application of early preventative interventions in at-risk c...
51 CitationsSource
#1Jue Xie (WashU: Washington University in St. Louis)H-Index: 2
#2Camillo Padoa-Schioppa (WashU: Washington University in St. Louis)H-Index: 22
Different neurons in orbitofrontal cortex encode the input and the output of economic decisions. The authors demonstrate that this neural circuit is both stable and flexible. When different goods are available for choice, individual neurons adapt to the new behavioral context while preserving their function in the decision circuit.
44 CitationsSource
#1Katherine R. Luking (SBU: Stony Brook University)H-Index: 13
#2David PagliaccioH-Index: 17
Last. M Deanna (WashU: Washington University in St. Louis)H-Index: 81
view all 4 authors...
The large impact of loss of reward on behavior has been well documented in adult populations. However, whether responsiveness to loss relative to gain is similarly elevated in child versus adult populations remains unclear. It is also unclear whether relations between incentive behaviors and self-reported reward/punishment sensitivity are similar within different developmental stages. To investigate these questions, 7–10-year-old children (N=70) and young adults (N=70) completed the Behavioral I...
8 CitationsSource
#1Katherine R. Luking (SBU: Stony Brook University)H-Index: 13
#2David Pagliaccio (WashU: Washington University in St. Louis)H-Index: 17
Last. M Deanna (WashU: Washington University in St. Louis)H-Index: 81
view all 4 authors...
Objective Maternal major depressive disorder (MDD) increases risk for MDD and predicts reduced reward responding in adolescent offspring. However, it is unclear whether alterations in neural response to reward can be detected in school-aged children at high risk before the typical increase in reward response observed in adolescence. Method To assess relationships between neural response to gain/loss feedback, MDD risk, and child depressive symptoms, 47 psychiatrically healthy 7- to 10-year-old c...
28 CitationsSource
#1Qing Gao (University of Electronic Science and Technology of China)H-Index: 13
#2Ke Zou (Sichuan University)H-Index: 7
Last. Huafu Chen (University of Electronic Science and Technology of China)H-Index: 30
view all 5 authors...
Some efforts were done to investigate the disruption of brain causal connectivity networks involved in major depressive disorder (MDD) using Granger causality (GC) analysis. However, the homogenous hemodynamic response function (HRF) assumption over the brain may disturb the inference of temporal precedence. Here we applied a blind deconvolution approach to examine the altered HRF shape in first-episode, drug-naive MDD patients. The regions with abnormal HRF shape in patients were chosen as seed...
15 CitationsSource
#1Tiffany C. Ho (UCSF: University of California, San Francisco)H-Index: 17
#2Shunan Zhang (UCSD: University of California, San Diego)H-Index: 10
Last. Tony T. Yang (UCSF: University of California, San Francisco)H-Index: 33
view all 9 authors...
While the extant literature has focused on major depressive disorder (MDD) as being characterized by abnormalities in processing affective stimuli (e.g., facial expressions), little is known regarding which specific aspects of cognition influence the evaluation of affective stimuli, and what are the underlying neural correlates. To investigate these issues, we assessed 26 adolescents diagnosed with MDD and 37 well-matched healthy controls (HCL) who completed an emotion identification task of dyn...
15 CitationsSource
#1Jingwen Jin (SBU: Stony Brook University)H-Index: 6
#2Christina Zelano (NU: Northwestern University)H-Index: 14
Last. Aprajita Mohanty (SBU: Stony Brook University)H-Index: 21
view all 4 authors...
Although the amygdala is a major locus for hedonic processing, how it encodes valence information is poorly understood. Given the hedonic potency of odor stimuli and the amygdala9s anatomical proximity to the peripheral olfactory system, we combined high-resolution fMRI with pattern-based multivariate techniques to examine how valence information is encoded in the amygdala. Ten human subjects underwent fMRI scanning while smelling 9 odorants that systematically varied in perceived valence. Repre...
35 CitationsSource
#1Tiffany C. Ho (UCSF: University of California, San Francisco)H-Index: 17
#2Colm G. Connolly (UCSF: University of California, San Francisco)H-Index: 19
Last. Tony T. Yang (UCSF: University of California, San Francisco)H-Index: 33
view all 13 authors...
Abstract Background Functional magnetic resonance imaging research suggests that major depressive disorder (MDD) in both adults and adolescents is marked by aberrant connectivity of the default mode network (DMN) during resting state. However, emotional dysregulation is also a key feature of MDD. No studies to date have examined emotion-related DMN pathology in adolescent depression. Comprehensively understanding the dynamics of DMN connectivity across brain states in individuals with depression...
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Cited By13
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#1Dylan M. Nielson (NIH: National Institutes of Health)H-Index: 9
#2Hanna Keren (NIH: National Institutes of Health)H-Index: 3
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Abstract Both human and animal studies support the relationship between depression and reward processing abnormalities, giving rise to the expectation that neural signals of these processes may serve as biomarkers or mechanistic treatment targets. Given the great promise of this research line, we scrutinize those findings and the theoretical claims that underlie them. To achieve this, we apply the framework provided by classical work on causality as well as contemporary approaches to prediction....
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#1Dorothée Lulé (University of Ulm)H-Index: 27
#2Sabine Müller (University of Ulm)H-Index: 2
Last. Ulrike M. E. Schulze (University of Ulm)H-Index: 11
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PURPOSE: The aim of the study was to define specific substrates of pathological behaviour patterns by analysing cortical activity using functional magnetic resonance imaging (fMRI) during an emotional processing task. METHODS: In a sample of N = 11 adolescent patients with AN (16.36 years, SD +/- 1.36) and N = 11 age-matched controls, we performed a functional MRI study to detect BOLD signal changes in a 3 T MRI scanner while presenting emotional facial stimuli. RESULTS: Young people with AN pre...
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#1Jingwen Jin (SBU: Stony Brook University)H-Index: 6
#2Jared Van Snellenberg (SBU: Stony Brook University)H-Index: 1
Last. Aprajita Mohanty (SBU: Stony Brook University)H-Index: 21
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BACKGROUND: Adolescence is characterized by affective and cognitive changes that increase vulnerability to depression, especially in females. Neurodevelopmental models attribute adolescent depression to abnormal responses in amygdala, striatum, and prefrontal cortex (PFC). We examined whether the strength of functional brain networks involving these regions predicts depression symptoms in adolescent females. METHODS: In this longitudinal study, we recorded resting-state functional connectivity (...
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#1Dylan M. Nielson (NIH: National Institutes of Health)H-Index: 9
#2Hanna Keren (NIH: National Institutes of Health)H-Index: 3
Last. Lisa S. Gorham (NIH: National Institutes of Health)
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Both human and animal studies support the relationship between depression and reward processing abnormalities, giving rise to the expectation that neural signals of these processes may serve as biomarkers or mechanistic treatment targets. Given the great promise of this research line, we scrutinize those findings and the theoretical claims that underlie them. To achieve this, we apply the framework provided by classical work on causality as well as contemporary approaches to prediction. We ident...
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Abstract Adolescence represents a key developmental period in terms of both mood and overweight and is linked to disturbed eating behavior. Therefore, it is essential to investigate the basis of food intake in healthy adolescents by considering mood impacts which remain largely unexplored. Hence this study aims to investigate the impact of hunger and mood on cerebral blood flow (CBF) changes in healthy adolescents. Fifteen participants underwent two MRI sessions including a 3D pseudo-continuous ...
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#1Abigail Oliver ('KCL': King's College London)
#2Victoria Pile ('KCL': King's College London)H-Index: 5
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#2Elena Peterson (CU: University of Colorado Boulder)H-Index: 1
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Abstract Background Adolescence is a developmental period in which depression and related mood syndromes often emerge, but few objective markers exist to guide diagnosis or predict symptoms. One potential mood marker is the functioning of frontoinsular networks, which undergo substantial development in adolescence and have been implicated in adult depression. To test this hypothesis, we used task-based neuroimaging to evaluate whether frontoinsular network dysfunction was linked to current and p...
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: The five-factor model consists of cognitive-affective-behavioral trait dimensions (neuroticism, extraversion, openness to experience, agreeableness, conscientiousness) that are central to models of psychopathology. In adults, individual differences in three of the Big Five traits, neuroticism, extraversion, and conscientiousness, have been linked to structural morphology and connectivity of the orbitofrontal cortex (OFC) and the amygdala, two brain regions critically involved in affective and ...
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