Brain and behavioral evidence for altered social learning mechanisms among women with assault-related posttraumatic stress disorder

https://doi.org/10.1016/j.jpsychires.2015.02.014Get rights and content

Highlights

  • Women with assault-related PTSD demonstrated altered learning mechanisms during the trust game.

  • Women with assault-related PTSD demonstrated altered neural encoding during a social learning task.

  • These results suggest a need to include social learning mechanisms in models of PTSD.

Abstract

Current neurocircuitry models of PTSD focus on the neural mechanisms that mediate hypervigilance for threat and fear inhibition/extinction learning. Less focus has been directed towards explaining social deficits and heightened risk of revictimization observed among individuals with PTSD related to physical or sexual assault. The purpose of the present study was to foster more comprehensive theoretical models of PTSD by testing the hypothesis that assault-related PTSD is associated with behavioral impairments in a social trust and reciprocity task and corresponding alterations in the neural encoding of social learning mechanisms. Adult women with assault-related PTSD (n = 25) and control women (n = 15) completed a multi-trial trust game outside of the MRI scanner. A subset of these participants (15 with PTSD and 14 controls) also completed a social and non-social reinforcement learning task during 3T fMRI. Brain regions that encoded the computationally modeled parameters of value expectation, prediction error, and volatility (i.e., uncertainty) were defined and compared between groups. The PTSD group demonstrated slower learning rates during the trust game and social prediction errors had a lesser impact on subsequent investment decisions. PTSD was also associated with greater encoding of negative expected social outcomes in perigenual anterior cingulate cortex and bilateral middle frontal gyri, and greater encoding of social prediction errors in the left temporoparietal junction. These data suggest mechanisms of PTSD-related deficits in social functioning and heightened risk for re-victimization in assault victims; however, comorbidity in the PTSD group and the lack of a trauma-exposed control group temper conclusions about PTSD specifically.

Introduction

There have been considerable efforts to understand the cognitive and neural mechanisms mediating posttraumatic stress disorder (PTSD) symptoms in order to boost treatment efficacy and ameliorate the poor quality of life associated with PTSD. Neurocircuitry models of PTSD (Rauch et al., Aug 15 20 06, Shin et al., Jul 2006, Admon et al., Jul 2013, Pitman et al., Nov 2012) have focused on identifying the neural mechanisms that mediate the clinical and behavioral observations of hypervigilance for threat and impaired fear extinction/fear inhibition. These models have ample empirical support and powerfully explain critical phenomena among PTSD populations. For example, hyperactive amygdala (Patel et al., Oct 2012, Rauch et al., May 1 2000) and insular cortex responses (Aupperle et al., 2012) during threat processing and anticipation explain attentional bias towards threat (Cisler et al., Jul 2011) and heightened interoceptive monitoring (Aupperle et al., 2012); altered structure and function of the hippocampus (Pitman et al., Nov 2012, Dannlowski et al., Feb 15 2012, Gilbertson et al., Nov 2002, Milad et al., Dec 15 2009, Admon et al., Aug 18 2009) explain the impaired ability to extinguish learned fear responses (Milad et al., Dec 15 2009, Wessa and Flor, Nov 2007, Jovanovic et al., Jul-Aug 2013, Norrholm et al., Mar 15 2011, Fani et al., Mar 2012, Milad et al., Jun 2008); weaker recruitment of perigenual anterior cingulate cortex (ACC) (Shin et al., Dec 15 2001, Shin et al., Mar 2005) explains observed deficits in emotion regulation (Moore et al., Sep 2008, Tull et al., Sep 2007). While these neurocircuitry models represent mechanisms of hypervigilance for threat, fear extinction, and emotion regulation, they do not account for observed PTSD-related deficits in social domains.

A less widely-known literature (Messman-Moore and Brown, Jun 2006, Messman-Moore et al., Mar 2013, Walsh et al., Oct 2012, Yeater et al., Feb 2011, Yeater and Viken, Aug 2010) demonstrates significant deficits in risk perceptions for social situations among violence victims and individuals with PTSD. For example, one study found that the latency with which victimized women decided to escape hypothetical risky social situations escalating towards rape significantly predicted subsequent revictimization (Messman-Moore and Brown, Jun 2006). A related line of research has demonstrated both among adolescents (Cisler et al., Oct 2011) and adults (Cougle et al., May 2009) that greater baseline histories of assault exposure and PTSD symptoms prospectively predict increased rates of revictimization. These data suggest that 1) violence victims have lower danger perceptions of risky social situations, and 2) assaultive violence exposure and PTSD severity predict heightened risk for future victimization. Critically, both of these observations cannot be explained by existing neurocircuitry models of PTSD or trauma exposure. For example, given the known findings of amygdala hyper-reactivity and attentional bias towards threat, one would predict greater risk perceptions in social situations when in fact the opposite is observed.

We previously demonstrated among adolescent girls that assaultive violence exposure is associated with less behavioral slowing as well as decreased ACC and bilateral anterior insula responses to unexpected negative social behavior during a social contingency learning task (Lenow et al., Jul 30 2014). These preliminary data supported a hypothesis of altered social learning mechanisms among adolescent assault victims and ostensibly suggest mediating mechanisms to explain their decreased social risk perceptions and increased risk for revictimization. Here, we sought to elaborate this model by investigating the neural and cognitive mechanisms of altered social learning among adult women with assault-related PTSD. We assessed social learning behavior outside of an fMRI context using the trust game, a widely used neuroeconomic game that quantifies social trust based on monetary exchanges with another player. Multi-trial versions of the trust game (Belli et al., Oct 2012, King-Casas et al., Aug 8 2008, Krueger et al., Dec 11 2007, Unoka et al., Aug 2009) enable the study of dynamic interactions in social dyads (e.g., characterizing how one player responds when their investments are not reciprocated). We also characterized and compared social and non-social learning mechanisms during fMRI using two-arm variants of commonly used bandit tasks (Daw et al., Jun 15 2006, Behrens et al., Nov 13 2008, Behrens et al., Sep 2007). In these tasks, we manipulated the reward structure of task responses and used computational modeling to probe the neural correlates of the task components of value expectation, prediction errors, and volatility (i.e. uncertainty) (Behrens et al., Sep 2007, Rushworth and Behrens, Apr 2008). To isolate a hypothesized unique relationship between assault-related PTSD and neural encoding of these component mechanisms during social learning, we modeled these same components in a non-social learning task. This methodology and analytic approach enabled testing the hypothesis that assault-related PTSD is associated with altered behavioral and neural correlates of social learning. However, it is important to note that our control group included only women with no history of trauma or PTSD; accordingly, inferences cannot be derived regarding specificity of the findings for PTSD specifically (vs just assault exposure) or for assault specifically (versus general trauma exposure).

Section snippets

Participants and assessment

Forty adult women, aged 20–53, were enrolled in the study. Five additional women were screened, but were ineligible due to the presence of a psychotic disorder (among a woman with PTSD), a current mental health disorder (among control women), or assault exposure without a current diagnosis of PTSD. The PTSD sample was comprised of 25 adult women and the control sample was comprised of 15 women. Table 1 provides demographic and clinical characteristics of the sample. Inclusion criteria for the

Trust Game

Trial-by-trial comparisons of investment behavior (Fig. 2) demonstrated greater reductions in investments among the PTSD group during the second phase and slower increases in investments during the third phase. These results were followed up with analyses of the RW learning model.

Preliminary analyses demonstrated validity of the RW modeling approach to participant behavior during the trust game (Supplemental Fig. 2 and Supplement Material) and no differences in model fit between groups (t

Discussion

Prior to discussing results, it is again important to note that our control group was limited to women without trauma exposure or PTSD. Accordingly, inferences regarding the unique effect of PTSD or assault exposure specifically cannot be made.

Observations of participant overt investment behavior on the trust game (Fig. 2) suggested that the PTSD group appeared to respond to the decrease in reinforcement with greater decreases in trust and appeared to demonstrate resistance to returning to

Funding sources

Portions of this work were supported through grants 1R21MH097784-01 and 1R01DA036360-01. The content is solely the responsibility of the authors and does not necessarily represent the official views of National Institute for Mental Health or the National Institutes of Health.

Contributions

Jennifer Lenow was involved in study design, interpretation, and manuscript writing. Scott Steele was involved in study design, interpretation, and manuscript writing. Sonet Smitherman was involved in study design. Clint Kilts was involved in study design and interpretation. Josh Cisler was involved in study design, analysis, interpretation, and manuscript writing. Keith Bush was involved in study design, interpretation, analysis, and manuscript writing.

Financial disclosures

All authors report no financial conflicts of interest.

Acknowledgments

We thank Cindy Mosley, Andi Ham, Jonathan Young, Shanti Tripathi, and George Andrew James for help with recruitment, analysis, and administration.

References (51)

  • S.A. Moore et al.

    Are expressive suppression and cognitive reappraisal associated with stress-related symptoms?

    Behav Res Ther

    (Sep 2008)
  • S.D. Norrholm et al.

    Fear extinction in traumatized civilians with posttraumatic stress disorder: relation to symptom severity

    Biol Psychiatry

    (Mar 15 2011)
  • R. Patel et al.

    Neurocircuitry models of posttraumatic stress disorder and beyond: a meta-analysis of functional neuroimaging studies

    Neurosci Biobehav Rev

    (Oct 2012)
  • S.L. Rauch et al.

    Neurocircuitry models of posttraumatic stress disorder and extinction: human neuroimaging research–past, present, and future

    Biol Psychiatry

    (Aug 15 2006)
  • S.L. Rauch et al.

    Exaggerated amygdala response to masked facial stimuli in posttraumatic stress disorder: a functional MRI study

    Biol Psychiatry

    (May 1 2000)
  • L.M. Shin et al.

    An fMRI study of anterior cingulate function in posttraumatic stress disorder

    Biol Psychiatry

    (Dec 15 2001)
  • M.T. Tull et al.

    A preliminary investigation of the relationship between emotion regulation difficulties and posttraumatic stress symptoms

    Behav Ther

    (Sep 2007)
  • K. Vogeley et al.

    Mind reading: neural mechanisms of theory of mind and self-perspective

    Neuroimage

    (Jul 2001)
  • R. Admon et al.

    Human vulnerability to stress depends on amygdala's predisposition and hippocampal plasticity

    Proc Natl Acad Sci USA

    (Aug 18 2009)
  • R.L. Aupperle et al.

    Dorsolateral prefrontal cortex activation during emotional anticipation and neuropsychological performance in posttraumatic stress disorder

    Arch Gen Psychiatry

    (2012)
  • A.T. Beck et al.

    Manual for the BDI-II

    (1996)
  • T.E. Behrens et al.

    The computation of social behavior

    Science

    (May 29 2009)
  • T.E. Behrens et al.

    Associative learning of social value

    Nature

    (Nov 13 2008)
  • T.E. Behrens et al.

    Learning the value of information in an uncertain world

    Nat Neurosci

    (Sep 2007)
  • J.R. Cougle et al.

    A prospective examination of PTSD symptoms as risk factors for subsequent exposure to potentially traumatic events among women

    J Abnorm. Psychol

    (May 2009)
  • Cited by (0)

    View full text