Posttraumatic stress disorder (PTSD) is a debilitating psychiatric disorder, which develops following exposure to extreme stress or trauma. Trauma-related symptoms, including hyperarousal, avoidance and intrusive memories, are often experienced in the period immediately following trauma exposure (McFarlane 2000
). In the majority of cases these symptoms resolve in the first month following exposure, however a subset of individuals will go on to develop the persistent symptoms that characterize PTSD (Kessler 1995
). One reason for the failure of symptoms to resolve over time may be the use of emotion regulation strategies that aim to suppress rather than modify an emotional response, when confronted with negative emotions (Cisler and Olatunji 2012
; Gross 1998
; Moore et al. 2008
; Tull et al. 2007
Gross’s highly influential process model of emotion regulation distinguishes regulation strategies by the point at which they occur during an unfolding emotional response. At the broadest level, strategies can be divided into early (antecedent-focused) and late (response-focused) (Gross 1998
). Early strategies aim to modify an emotional response before it occurs, such as through reinterpreting the meaning or context of a stimulus—situation-focused cognitive reappraisal—or by modifying one’s perspective—self-focused cognitive reappraisal (Ochsner et al. 2004
; Willroth and Hilimire 2016
). For example, when faced with a challenging situation, a medical professional may adopt a professional distance to perceive it in a detached and objective manner rather than a personal or emotional one (Doulougeri et al. 2016
; Ochsner et al. 2004
; Shapiro 2013
). In contrast, late strategies attempt to inhibit an emotional response once it has already occurred, for example, by suppressing any outward expression of emotion. Late strategies have been shown to be less effective than early strategies in regulating experienced emotion (Gross 1998
In PTSD populations, difficulties with emotion regulation were found to be significantly associated with PTSD symptom severity and to partially mediate the relationship between PTSD and related comorbidities (Klemanski et al. 2012
). PTSD symptoms have been associated with greater spontaneous use of suppression and less use of reappraisal (Shepherd and Wild 2014
), and shifting from suppression- (late) to reappraisal-based (early) emotion regulation strategies has been associated with improvements in treatment outcomes (Price et al. 2006
). In addition, therapeutic interventions such as cognitive behavior therapy (CBT) aim to promote emotional regulation self-efficacy, training clients to change their emotions by changing their thoughts through cognitive restructuring (Beck 2011
At the neural level, cognitive reappraisal and expressive suppression have been shown to be both functionally and temporally distinct. Previous work in healthy individuals (Goldin et al. 2008
) has demonstrated that during emotion regulation, patterns of neural activity differ between reappraisal and suppression and change over time, with reappraisal showing a pattern of high initial medial prefrontal neural activity which then decreases over time and suppression showing low initial medial prefrontal neural activity which then increases. At a functional level, the medial prefrontal cortex is involved in multiple processes relevant to emotion regulation, including emotional processing and modulation of the fear response (Diekhof et al. 2011
; Etkin et al. 2011
; Milad et al. 2007a
; Northoff et al. 2006
). At a structural level, regions within the medial prefrontal cortex show strong connections to the limbic system, including the amygdala (Bush et al. 2000
; Devinsky et al. 1995
). Goldin et al. conclude that the early activation of prefrontal control regions during reappraisal leads to the effective down-regulation of amygdala and insular reactivity, accompanied by successful regulation of the emotional response and a reduced need for continued cognitive control. Conversely, during suppression, later activation of prefrontal control regions seemingly fails to inhibit the emotional response, leading to a need for sustained activity in these regions and no decrease in amygdala and insular activity.
PTSD patients have previously demonstrated less prefrontal neural activity than controls in response to threat-related stimuli, and this is thought to play a key role in the development and maintenance of PTSD symptoms (Rauch et al. 2006
; Shin et al. 2006
). Lower prefrontal neural activity has also been observed during the down-regulation of negative emotion in PTSD, in populations as diverse as female victims of sexual violence (New et al. 2009
), male combat veterans (Rabinak et al. 2014
) and male and female motor vehicle accident victims (Xiong et al. 2013
). The above studies did not contrast different types of down-regulation, such as expressive suppression and cognitive reappraisal. However, in a study by Shepherd and Wild (Shepherd and Wild 2014
), PTSD patients and trauma-exposed controls were instructed to feel, maintain or decrease their emotional response to negative and neutral images. PTSD symptoms were associated with greater spontaneous use of suppression and less use of reappraisal (Shepherd and Wild 2014
). In addition, previous neuroimaging work in PTSD has not distinguished between task preparation and image presentation. It is therefore unclear whether and how neural activity alters during an unfolding emotional response in individuals with PTSD, and whether patterns of change differ between groups in during suppression, as both groups can employ suppression when instructed.
In the current study, we investigate neural and behavioral differences between combat-related PTSD patients and combat-exposed controls during an emotion regulation task. In line with Gross’s process model of emotion regulation, we distinguish between cognitive reappraisal and expressive suppression. In addition, previous work has demonstrated that patterns of neural activity not only differ between reappraisal and suppression, but also change over time (Goldin et al. 2008
), and that physiological and behavioral changes are observable during preparation for emotion regulation (Gross 1998
). Gross and colleagues propose that when individuals are aware that they will soon be required to manage their emotions, they “appear to steel themselves”, and that physiological and behavioural changes are indicative of an individual’s efforts to prepare themselves (1998
). As such, we also distinguish between preparatory neural activity, during the instruction phase, and active emotion regulation, during the image presentation phase, a distinction that has not previously been made in neuroimaging research on PTSD.
We recruited patients with combat-related PTSD and combat-exposed individuals without psychopathology, and employed a mixed design to compare the effects of cognitive reappraisal and expressive suppression on subjective arousal and neural activity in individuals with and without PTSD. Combat-related images were used to generate a powerful trauma-related negative affective state. We hypothesize that during emotional regulation, patients and controls will differ at both a behavioral and neural level. On the basis of previous literature, one may postulate on a number of potential neural patterns that PTSD patients may demonstrate. Based on neuroimaging work in PTSD, one may expect that prefrontal neural activity will be lower in PTSD patients than controls during all stages and for all forms of emotion regulation (New et al. 2009
; Rabinak et al. 2014
; Rauch et al. 2006
; Xiong et al. 2013
). Alternatively, if PTSD is particularly associated with the use of suppression (Shepherd and Wild 2014
), then one may expect that when instructed to use reappraisal, PTSD patients will rather demonstrate a pattern similar to suppression in healthy controls, of lower initial prefrontal neural activity which then increases (Goldin et al. 2008
). In this case, one would not expect to observe a difference between patients and controls. We aim to clarify whether during cognitive reappraisal, PTSD patients show reduced neural activity across both task preparation and stimulus presentation, or if they present a pattern similar to that of expressive suppression in healthy controls, with lower preparatory neural activity followed by sustained activity during stimulus presentation. At the behavioral level, we hypothesize that PTSD patients will be less effective in down-regulating emotion and will report higher subjective arousal ratings than controls during cognitive reappraisal and expressive suppression.
The goal of this study was to assess differences between combat-PTSD patients and combat-exposed healthy controls during an emotion regulation task, both at a behavioral and neural level. Two emotion regulation strategies, cognitive reappraisal and expressive suppression, were assessed during preparation and image presentation. In the reappraisal condition, controls showed higher prefrontal neural activity than patients during the preparatory phase, while patients showed higher prefrontal neural activity than controls during image presentation. No difference between patients and controls was observed in the suppression condition, either during the preparatory phase or during image presentation.
In the preparatory phase, controls showed higher activation than patients in the vmPFC and rACC, regions that have been previously implicated in affective and cognitive processing, including the regulation of fear expression, memory and emotional processing (Carter et al. 1999
; Diekhof et al. 2011
; Etkin et al. 2011
; Milad et al. 2007a
), as well as in the neurocircuitry of PTSD (Rauch et al. 2006
). The rACC is known to regulate emotional responses and assess the salience of emotional stimuli, and has strong connections to limbic and paralimbic regions including the amygdala (Bush et al. 2000
; Devinsky et al. 1995
). The vmPFC is known to play a key role in self-referential processing and the extinction of conditioned fear (Milad et al. 2007a
; Northoff et al. 2006
). Previous work on cognitive reappraisal in healthy controls has demonstrated that early enhanced bold
responses in the medial prefrontal cortex correlates with reduced late activation of the amygdala (Goldin et al. 2008
), and a decrease in self-reported negative experiences. As such, higher activation of these regions during the preparatory phase should lead to more effective down regulation of negative emotion during the image presentation phase. This is reflected in the current results, as controls also reported significantly less arousal than patients.
During image presentation, patients showed higher activity than controls in the dorsal ACC (dACC) and in the visual cortex. The dACC shows strong connections with regions including the dorsolateral prefrontal cortex and supplementary motor areas, and has been implicated in conflict monitoring and response selection (Devinsky et al. 1995
). The region observed in this study also corresponds to the anterior mid-cingulate cortex (aMCC) (Rotge et al. 2015
), a region shown to be involved in negative affect, (social) pain, and cognitive control (Rotge et al. 2015
; Shackman et al. 2011
). In addition, the aMCC includes the rostral cingulate zone (RCZ), a region involved in conflict monitoring and facial movement (Picard and Strick 1996
), with links to motor centers responsible for expressing affect and executing goal-directed behavior (Shackman et al. 2011
). Greater activation in the visual cortex during image presentation in patients may suggest that controls disengage from the stimuli more than patients. Although not instructed, controls may have spontaneously engaged in attentional deployment, another form of early emotion regulation (Gross 2008
). Previous eye-tracking studies have shown that PTSD is related to attentional bias for trauma-related stimuli, accompanied by greater autonomic arousal, compared with trauma-exposed controls (Felmingham et al. 2011
; Kimble et al. 2010
Therefore, patients and controls differ not only on a temporal dimension, but also on a regional, and therewith functional level, suggesting that during the reappraisal condition, patients and controls actually engaged in different strategies at different times. During the reappraisal condition, higher activation in controls in the rACC during the preparation phase may suggest that they implement preparatory affective regulation strategies. Higher activation in patients in the dACC during image presentation may suggest that patients implement more suppression-based strategies, such as control or suppression of motoric responses, later and less effectively, as indexed by higher subjective arousal ratings. In a similar neuroimaging study with healthy controls, higher early activation of prefrontal regions including the mPFC was observed during cognitive reappraisal, while higher late activation in regions including the vmPFC and dACC was observed during expressive suppression (Goldin et al. 2008
). We did not observe a difference in neural activity between patients and controls in the suppression condition, either during the preparatory phase or during image presentation. This may indicate that PTSD patients and controls use similar brain regions at similar times when suppressing negative emotion.
We did not observe a difference in amygdala activity between patients and controls in any condition. This may be due to the highly relevant nature of the stimuli, as both groups had been exposed to combat. This is in line with previous neuroimaging studies that have also failed to demonstrate increased amygdala activity in PTSD patients during emotion regulation (New et al. 2009
; Rabinak et al. 2014
; Xiong et al. 2013
), as well as image presentation (Phan et al. 2006
) and traumatic reminders (Britton et al. 2005
). In future studies, the addition of a non-trauma exposed control group may prove useful in teasing apart differences between trauma exposure per se and PTSD in amygdala reactivity.
One potential limitation of this study is that we did not include a measure of how effectively participants felt they had implemented each strategy. Previous work in healthy controls that has included a post-task measure to verify that the correct emotion regulation strategy was implemented has shown a compliance rate of 96% (Ochsner et al. 2002
). Nevertheless, future work could usefully incorporate a measure of perceived success of strategy implementation to assess how PTSD patients perceive their abilities to down-regulate negative emotion regulation. In addition, the short preparation phase may have resulted in low power and future studies could provide longer preparation times to further disentangle preparation from target presentation.
Another potential limitation is that the patient group was significantly younger than the control group. Previous neuroimaging studies comparing age groups have found age-related differences, however these appear to be more pronounced at the structural level rather than the functional level (Rajah and D’Esposito 2005
). In addition, although precise cutoffs vary, studies of age-related differences usually compare younger adults, for example between 18 and 35 years of age, to older adults, 60 years of age and above (Persson and Reuter-Lorenz 2008
). However, in the current study, all individuals were in young to middle adulthood, with no individuals in old age. Nevertheless, age was included as a covariate in the neuroimaging analysis, although repeating the analyses without including age did not change the results.
One should also note that the generalizability of the current findings may be limited by both the specific nature and size of the participant groups. Given the relatively small sample size and the unequal subgroup sizes, we may lack sufficient power to detect smaller effects. Future work is needed to replicate the current findings and to explore how these results may extend to non-military and female samples.
In the current study, we analyzed the image presentation phase as a single block, as due to the duration of image presentation modelling the data using a time series approach was unlikely to produce interpretable results. Future studies may consider using a longer image presentation duration, similar to one used by Goldin et al. (2008
), to also allow a time-series analysis approach.
The patients in the current study were assessed prior to treatment. Psychotherapies, such as CBT, train individuals to effectively employ emotion regulation techniques (Beck 2011
), and one may expect that behavioral and neural correlates of emotion regulation will change following successful therapeutic intervention. Going forward, studies employing a longitudinal design would be useful to assess whether neural correlates of emotion regulation are useful in predicting responsiveness to therapy, and if these patterns change following training and the resolution of symptoms.