Pia Pechtel1, Diego A Pizzagalli. 1. Center for Depression, Anxiety and Stress Research, McLean Hospital, Harvard Medical School, Belmont, MA 02478, USA. ppechtel@mclean.harvard.edu
Abstract
IMPORTANCE: Childhood sexual abuse (CSA) has been associated with psychopathology, particularly major depressive disorder (MDD), and high-risk behaviors. Despite the epidemiological data available, the mechanisms underlying these maladaptive outcomes remain poorly understood. OBJECTIVE: We examined whether a history of CSA, particularly in conjunction with a past episode of MDD, is associated with behavioral and neural dysfunction in reinforcement learning, and whether such dysfunction is linked to maladaptive behavior. DESIGN: Participants completed a clinical evaluation and a probabilistic reinforcement task while 128-channel event-related potentials were recorded. SETTING: Academic setting; participants recruited from the community. PARTICIPANTS: Fifteen women with a history of CSA and remitted MDD (CSA + rMDD), 16 women with remitted MDD with no history of CSA (rMDD), and 18 healthy women (controls). EXPOSURE: Three or more episodes of coerced sexual contact (mean [SD] duration, 3.00 [2.20] years) between the ages of 7 and 12 years by at least 1 male perpetrator. MAIN OUTCOMES AND MEASURES: Participants' preference for choosing the most rewarded stimulus and avoiding the most punished stimulus was evaluated. The feedback-related negativity and error-related negativity-hypothesized to reflect activation in the anterior cingulate cortex-were used as electrophysiological indices of reinforcement learning. RESULTS: No group differences emerged in the acquisition of reinforcement contingencies. In trials requiring participants to rely partially or exclusively on previously rewarded information, the CSA + rMDD group showed (1) lower accuracy (relative to both controls and the rMDD group), (2) blunted electrophysiological differentiation between correct and incorrect responses (relative to controls), and (3) increased activation in the subgenual anterior cingulate cortex (relative to the rMDD group). A history of CSA was not associated with impairments in avoiding the most punished stimulus. Self-harm and suicidal behaviors correlated with poorer performance of previously rewarded, but not previously punished, trials. CONCLUSIONS AND RELEVANCE: Irrespective of past MDD episodes, women with a history of CSA showed neural and behavioral deficits in utilizing previous reinforcement to optimize decision making in the absence of feedback (blunted "Go learning"). Although our study provides initial evidence for reward-specific deficits associated with CSA, future research is warranted to determine if disrupted positive reinforcement learning predicts high-risk behavior following CSA.
IMPORTANCE: Childhood sexual abuse (CSA) has been associated with psychopathology, particularly major depressive disorder (MDD), and high-risk behaviors. Despite the epidemiological data available, the mechanisms underlying these maladaptive outcomes remain poorly understood. OBJECTIVE: We examined whether a history of CSA, particularly in conjunction with a past episode of MDD, is associated with behavioral and neural dysfunction in reinforcement learning, and whether such dysfunction is linked to maladaptive behavior. DESIGN:Participants completed a clinical evaluation and a probabilistic reinforcement task while 128-channel event-related potentials were recorded. SETTING: Academic setting; participants recruited from the community. PARTICIPANTS: Fifteen women with a history of CSA and remitted MDD (CSA + rMDD), 16 women with remitted MDD with no history of CSA (rMDD), and 18 healthy women (controls). EXPOSURE: Three or more episodes of coerced sexual contact (mean [SD] duration, 3.00 [2.20] years) between the ages of 7 and 12 years by at least 1 male perpetrator. MAIN OUTCOMES AND MEASURES: Participants' preference for choosing the most rewarded stimulus and avoiding the most punished stimulus was evaluated. The feedback-related negativity and error-related negativity-hypothesized to reflect activation in the anterior cingulate cortex-were used as electrophysiological indices of reinforcement learning. RESULTS: No group differences emerged in the acquisition of reinforcement contingencies. In trials requiring participants to rely partially or exclusively on previously rewarded information, the CSA + rMDD group showed (1) lower accuracy (relative to both controls and the rMDD group), (2) blunted electrophysiological differentiation between correct and incorrect responses (relative to controls), and (3) increased activation in the subgenual anterior cingulate cortex (relative to the rMDD group). A history of CSA was not associated with impairments in avoiding the most punished stimulus. Self-harm and suicidal behaviors correlated with poorer performance of previously rewarded, but not previously punished, trials. CONCLUSIONS AND RELEVANCE: Irrespective of past MDD episodes, women with a history of CSA showed neural and behavioral deficits in utilizing previous reinforcement to optimize decision making in the absence of feedback (blunted "Go learning"). Although our study provides initial evidence for reward-specific deficits associated with CSA, future research is warranted to determine if disrupted positive reinforcement learning predicts high-risk behavior following CSA.
Authors: Nancy E Adleman; Vinod Menon; Christine M Blasey; Christopher D White; Ilana S Warsofsky; Gary H Glover; Allan L Reiss Journal: Neuroimage Date: 2002-05 Impact factor: 6.556
Authors: Philip Shaw; Noor J Kabani; Jason P Lerch; Kristen Eckstrand; Rhoshel Lenroot; Nitin Gogtay; Deanna Greenstein; Liv Clasen; Alan Evans; Judith L Rapoport; Jay N Giedd; Steve P Wise Journal: J Neurosci Date: 2008-04-02 Impact factor: 6.167
Authors: Daniel G Dillon; Avram J Holmes; Jeffrey L Birk; Nancy Brooks; Karlen Lyons-Ruth; Diego A Pizzagalli Journal: Biol Psychiatry Date: 2009-04-09 Impact factor: 13.382
Authors: Michael T Treadway; Merida M Grant; Zhaohua Ding; Steven D Hollon; John C Gore; Richard C Shelton Journal: PLoS One Date: 2009-03-26 Impact factor: 3.240
Authors: Jamie L Hanson; Wouter van den Bos; Barbara J Roeber; Karen D Rudolph; Richard J Davidson; Seth D Pollak Journal: J Child Psychol Psychiatry Date: 2017-02-03 Impact factor: 8.982
Authors: Erik M Mueller; Pia Pechtel; Andrew L Cohen; Samuel R Douglas; Diego A Pizzagalli Journal: Depress Anxiety Date: 2015-01-23 Impact factor: 6.505
Authors: Daniel G Dillon; Isabelle M Rosso; Pia Pechtel; William D S Killgore; Scott L Rauch; Diego A Pizzagalli Journal: Depress Anxiety Date: 2013-10-21 Impact factor: 6.505
Authors: Andrew M Novick; Mateus L Levandowski; Laura E Laumann; Noah S Philip; Lawrence H Price; Audrey R Tyrka Journal: J Psychiatr Res Date: 2018-02-13 Impact factor: 4.791
Authors: Meg J Dennison; Maya L Rosen; Kelly A Sambrook; Jessica L Jenness; Margaret A Sheridan; Katie A McLaughlin Journal: Child Dev Date: 2017-12-21