REVIEW ARTICLE published: 09 October 2012 INTEGRATIVE NEUROSCIENCE doi: 10.3389/fnint.2012.00089 Emotion and cognition interactions in PTSD: a review of neurocognitive and neuroimaging studies

Jasmeet P. Hayes 1,2 *, Michael B. VanElzakker 3,4 and Lisa M. Shin 3,4

1 National Center for PTSD, VA Boston Healthcare System, Boston, MA, USA 2 Department of Psychiatry, Boston University School of Medicine, Boston, MA, USA 3 Department of Psychology, Tufts University, Medford, MA, USA 4 Department of Psychiatry, The Massachusetts General Hospital, Boston, MA, USA

Edited by: Posttraumatic stress disorder (PTSD) is a psychiatric syndrome that develops after Lihong Wang, Duke University, USA exposure to terrifying and life-threatening events including warfare, motor-vehicle Reviewed by: accidents, and physical and sexual assault. The emotional experience of psychological Robin L. Aupperle, University trauma can have long-term cognitive effects. The hallmark symptoms of PTSD involve of Missouri, USA Apostolos Georgopoulos, University alterations to cognitive processes such as memory, attention, planning, and problem of Minnesota, USA solving, underscoring the detrimental impact that negative emotionality has on cognitive *Correspondence: functioning. As such, an important challenge for PTSD researchers and treatment Jasmeet P. Hayes, National Center providers is to understand the dynamic interplay between emotion and cognition. for PTSD (116B-2), VA Boston Contemporary cognitive models of PTSD theorize that a preponderance of information Healthcare System, 150 S. Huntington Ave., Boston, processing resources are allocated toward threat detection and interpretation of MA 02130, USA. innocuous stimuli as threatening, narrowing one’s attentional focus at the expense of e-mail: [email protected] other cognitive operations. Decades of research have shown support for these cognitive models of PTSD using a variety of tasks and methodological approaches. The primary goal of this review is to summarize the latest neurocognitive and neuroimaging research of emotion-cognition interactions in PTSD. To directly assess the influence of emotion on cognition and vice versa, the studies reviewed employed challenge tasks that included both cognitive and emotional components. The findings provide evidence for memory and attention deficits in PTSD that are often associated with changes in functional brain activity. The results are reviewed to provide future directions for research that may direct better and more effective treatments for PTSD.

Keywords: neuropsychology, fMRI, amygdala, threat bias, cognitive control, memory, anxiety, neuroimaging

INTRODUCTION process information about perception, meaning, and action Stress and anxiety serve the important functions of preparing responses toward executing goals (Lang, 1977; Foa and Kozak, an individual to meet the demands of everyday life and increas- 1986; Chemtob et al., 1988). In PTSD, networks representing ing the chance for survival. It is therefore not surprising that information about fear become highly elaborated and accessible, arousing and emotionally salient stimuli readily capture attention which has implications for encoding and retrieval of information. and have a powerful influence on how information is processed, For instance, an elaborated fear structure may lower one’s capac- encoded, stored, and retrieved. However, extreme levels of stress ity to process non-threat related information, leading to atten- can have a devastating effect on healthy functioning. Nowhere tional bias toward potential threats in the environment (Chemtob is this demonstrated more clearly than in psychiatric disorders et al., 1988). Furthermore, nodes of the fear network represent- such as posttraumatic stress disorder (PTSD). PTSD develops ing threat arousal may predispose an individual to interpret even after exposure to terrifying and life threatening events and is innocuous stimuli as threatening. Intrusive memories result from characterized by intense reliving of the traumatic event through spreading activation of the threat arousal node to related threat disruptive memories and nightmares, avoidance of reminders nodes, while nodes representing opposing alternatives become of the event, and hypervigilance toward potential threats in the inhibited. environment. These hallmark symptoms involve alterations to In this review, we summarize the latest research examining cognitive processes such as memory, attention, planning, and the dynamic interplay between emotions and cognitive processes problem solving, underscoring the impact that emotion has on in PTSD. We begin with an overview of the criteria that must cognitive functioning. be met for a PTSD diagnosis. Next, we separately review stud- Influential cognitive theories of PTSD emphasize the inter- ies that examine the effect of emotion on cognitive functions action between emotion and cognition in contributing to the and those that examine the effect of top-down cognitive con- symptoms of PTSD. These theories contend that psychopathol- trol processes on emotion, following this useful distinction put ogy arises when emotional stress alters cognitive networks that forth by Dolcos et al. (2011). Finally, we provide a summary

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of the reviewed literature and discuss open questions in the EMOTIONAL EFFECTS ON COGNITIVE FUNCTION field. To directly assess emotion-cognition interactions in PTSD, MEMORY AND LEARNING we focus our review on studies employing a challenge task in Explicit memory which both emotional and neutral stimuli were presented. Such Decades of emotional memory research in healthy individuals studies may lend themselves to better reproduce conditions in suggests that emotional information tends to be remembered everyday life in which emotions influence task performance. better than neutral information (Christianson, 1992; Kensinger, Other recent papers have comprehensively reviewed studies that 2007). However, the extent to which emotion provides a facil- employed only neutral stimuli (i.e., Aupperle et al., 2012b)or itating effect on memory encoding and retrieval in PTSD is have examined the brain under task-free conditions in PTSD (i.e., unclear. Cognitive models of PTSD predict that patients remem- Engdahl et al., 2010; Georgopoulos et al., 2010; Daniels et al., ber emotional information better due to a bias toward (Chemtob 2012). et al., 1988)ordifficultydisengagingfrom(Chemtob et al., 1999) threat-related information, which may lead to greater resources CLINICAL DEFINITION OF PTSD applied to processing and encoding emotional information. A As outlined in the current Diagnostic and Statistical Manual variety of behavioral and neuroimaging memory paradigms (DSM-IV-TR), PTSD develops after exposure to a Criterion A1 have been employed to examine the extent to which patients event, defined as involving actual or threatened death, serious with PTSD remember emotional information better than neutral injury, or threat to one’s physical integrity (American Psychiatric information in comparison to healthy or trauma-exposed con- Association, 2000). To meet Criterion A1, the individual must trols. Consistent with the notion that emotion enhances memory, have been directly involved in the traumatic event, witnessed the there is evidence for a memory advantage in patients vs. con- event, or learned about the death or serious injury of a fam- trols for negative threat information (Vrana et al., 1995; McNally ily member or close friend. The individual must have responded et al., 1998; Golier et al., 2002; Paunovic et al., 2002). In these to the traumatic event with intense fear, helplessness, or horror studies, word lists were presented with either incidental or inten- (referred to as Criterion A2) although future conceptualizations tional encoding instructions and participants were subsequently of PTSD may omit this criterion (Friedman et al., 2011). The instructed to recall as many words as they could from the lists. symptoms of PTSD can be broadly divided into three symp- Results showed that patients either remembered more emotional tom clusters, B, C, and D. Symptom cluster B involves persistent words than controls or that memory performance for emotional and unwanted recollections of the traumatic event, intrusive vs. neutral words improved to a greater extent than controls. memories of the event, and dissociative flashbacks. The indi- However, memories are often subject to a wide range of dis- vidual re-experiences the event despite being removed from the tortions and biases that impact accurate recollection (Schacter, traumatic situation and context. These symptoms can be fright- 1999). One of the most controversial topics in the field of ening and highly disruptive of activities of daily living. Cluster C traumatic stress is that of the accuracy of recovered mem- involves persistent avoidance of people, places, and activities that ories, prompting PTSD researchers to examine how memory serve as reminders of the traumatic event, emotional numbing, for negative and traumatic information fares in false mem- difficulty experiencing a full range of emotions, and dimin- ory paradigms such as the Deese–Roediger–McDermott (DRM) ished expectations of one’s ability to lead a long, fulfilling life. paradigm (Roediger and McDermott, 1995). In the DRM Finally, symptom cluster D involves symptoms of hyperarousal paradigm, participants are presented with a list of words that including difficulty with sleep, irritability and anger, poor con- are semantically related to a critical non-presented word (lure). centration, hypervigilance, and exaggerated startle response. The The critical lure is often falsely remembered as being previously symptoms of PTSD must be present for more than one month presented on subsequent recall and recognition tests and may and cause significant distress or impairment in social and occu- reflect gist-based encoding rather than encoding of specific details pational functioning in order to differentiate the disorder from (Brainerd and Reyna, 2002). In PTSD, two of the three DRM transient and acute stress reactions. The typical course of PTSD studies employing verbal lists indeed reported greater false alarms begins with the development of symptoms within 6 months of to critical lures in patients with PTSD than control participants the onset of the traumatic event, although delays in symptom (Bremner et al., 2000; Brennen et al., 2007). However, a third occurrence can occur. Individuals whose symptoms persist for study employing the DRM paradigm did not report greater false more than 3 months are diagnosed with chronic PTSD, which is alarms in patients (Zoellner et al., 2000). It is unclear why these associated with a host of poor health outcomes, including heart studies found differential effects, although it is possible that the disease, obesity, alcohol abuse, and lowered perceptions of gen- false memory effect is more likely to be elicited when trauma- eral health (Dobie et al., 2004; Hoge et al., 2007; Boscarino, specific material, as opposed to generally negative material, is 2008). presented. Studies employing paradigms other than the DRM The prevalence rate of PTSD is estimated to be 7–8% in the but including trauma-specific material have reported greater false general population (Kessler et al., 1995) although prevalence esti- alarms in PTSD (Hayes et al., 2011) or a bias in making memory mates have varied depending on the type of trauma exposure decisions about trauma-specific information (Litz et al., 1996). and demographic characteristics. For instance, prevalence rates Negative arousal can alter the type of information that are higher among individuals exposed to military combat, rang- is encoded and retrieved. Neurohormones including nore- ing between 12–20% (Hoge et al., 2004; Dohrenwend et al., 2006; pinephrine and cortisol play a critical role in the fear and stress Tanielian and Jaycox, 2008). response by mobilizing the body’s response to the stressor via

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the hypothalamus-pituitary-adrenal axis (HPA) and amygdala, identify brain regions subserving successful memory operations among several other key regions. Norepinephrine has been shown (Paller and Wagner, 2002). Hayes et al. (2011) reported reduced to facilitate emotional memory (for a review see Ferry et al., amygdala and hippocampal activity during successful memory 1999). However, emotional memory may not be uniformly encoding of trauma-related material in patients with PTSD. In enhanced during high levels of arousal. For example, individuals this study, patients with PTSD produced greater false alarms for exposed to highly arousing negative material show a narrowing trauma-specific negative information, suggesting that the reduced of attention (Easterbrook, 1959), referred to as “tunnel mem- medial temporal lobe activity may underlie memory distortions. ory,” in which the central objects and features of a scene are However, Brohawn et al. (2010) reported enhanced hippocam- better remembered than peripheral background (Christianson pal activity in patients with PTSD during encoding of emotional and Loftus, 1991). A recent study examined the extent to which items relative to controls and Dickie et al. (2008) reported greater patients with PTSD showed this memory trade-off effect (i.e., activity in both the amygdala and hippocampus for remembered greater memory for negative items vs. backgrounds) in compari- vs. forgotten stimuli (a control group was not included in this son to a trauma-exposed control group and a healthy unexposed study and therefore comparisons were made within the PTSD group (Mickley Steinmetz et al., 2012). The findings showed that group). Two major differences may explain the discrepant results the PTSD and the healthy non-trauma exposed group exhibited among studies. In the latter two studies, there were no behav- a greater memory trade-off effect for emotional items than the ioral differences in memory performance between patients and trauma-exposed-no-PTSD group. Although further research is controls or between emotional and neutral information, and gen- required, these results suggest that patients with PTSD do not eral negative stimuli were used whereas Hayes and colleagues used exhibit greater tunnel memory than healthy control participants. trauma-specific combat stimuli in recent war veterans. Therefore, Distortions in memory have been observed during autobio- although these studies report mixed results, the findings may graphical retrieval in PTSD. Autobiographical memories repre- provide more support for the notion that false memory, and sent personally experienced recollections and knowledge about associated decreases in neural signal in the amygdala and hip- oneself (Conway and Pleydell-Pearce, 2000)andmaybekeyin pocampus, is elicited primarily for trauma-specific information understanding the accessibility and completeness of traumatic in PTSD. memories (McNally et al., 1994). Two experimental studies have In summary, the research findings of explicit memory perfor- shown that during the recollection of personal past events, indi- mance in PTSD are decidedly complex. The evidence suggests viduals with PTSD tend to recall personal memories with very few that recall of gist-based negative information may be enhanced details and very little specificity (McNally et al., 1994, 1995). This in PTSD, whereas information about specific details and con- “overgeneral memory” effect is thought to result from inadequate textual information appears to be diminished. This is consistent search of memory during retrieval, perhaps due to rumination, with the notion that cognitive resources may be preferentially avoidance, and impairment in executive capacity (Williams et al., allocated to process threat information at the expense of neutral 2007). However, the difficulty with retrieving detailed personal or non-threat related information. An important consideration information does not appear to be specific to traumatic memories is whether memory alterations occur for all types of emotional but extends to neutral and positive events. information or only for trauma-specific information. Although Research on the neural underpinnings emotion and memory there are mixed findings in this regard, overall there is stronger suggests that the benefit of emotion on memory occurs in part via evidence that false memories are elicited mainly for trauma- interactions between the amygdala and hippocampus. According specific information. Research regarding the neural correlates of to the modulation hypothesis, emotional events are remem- memory in PTSD is still in its infancy, but the abnormalities bered better than neutral events due to the amygdala’s influence observed in the amygdala and hippocampus suggests that the on other medial temporal lobe structures including the hip- symptoms of PTSD are associated with disturbances in memory pocampus (McGaugh et al., 1996). Support for the modulation encoding and retrieval. hypothesis has been reported in humans using fMRI, showing greater activity in the amygdala and hippocampus for successfully Fear conditioning remembered vs. forgotten emotional memories (Dolcos et al., Pavlovian fear conditioning and extinction has been a fruitful 2004). However, a key question is whether medial temporal lobe model of fear memory in PTSD. Fear conditioning paradigms structures interact in PTSD as the modulation hypothesis would involve the repeated presentation of a neutral conditioned stim- predict. Whereas the majority of imaging studies have shown ulus (CS) such as an auditory tone or a colored light, followed increased amygdala activity in PTSD (Pissiota et al., 2002; Shin immediately by an aversive unconditioned stimulus (US) such as et al., 2004a, 2005), studies of hippocampal activity have been a finger shock. Extinction of the fear memory occurs when the CS mixed, showing either an increase (Shin et al., 2004b; Thomaes is subsequently and repeatedly presented in the absence of the US. et al., 2009)ordecreaseinPTSD(Bremner et al., 2003; Astur This experimental paradigm models a crucial aspect of emotion- et al., 2006). To examine the role of the amygdala and hippocam- cognition interactions in PTSD: individuals with PTSD repeatedly pus in emotional memory formation in PTSD, researchers have show elevated fear responses to trauma reminders, even when employed the subsequent memory paradigm, in which neural those reminders occur in a safe context (i.e., a film portraying activity is measured at encoding for items that are probed for combat). Some researchers see a parallel between this clinical phe- memory success after a delay. Differences in encoding activity for nomenon and a failure of fear extinction or fear extinction recall successfully remembered and forgotten material is evaluated to (e.g., Pitman, 1988).

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Early in the PTSD fear conditioning and extinction litera- of PTSD in that the functional neurocircuitry abnormalities in ture, fear responsivity was quantified as physiological responses this disorder point to enhanced conditioning responses during such as skin conductance responsivity and heart rate. In line with trauma, as well as deficits in fear extinction and extinction recall the enhanced effect of emotion on explicit declarative memory after the trauma has passed. discussed above, physiological studies have demonstrated that, relative to controls, individuals with PTSD show evidence of Implicit memory enhanced fear conditioning (Orr et al., 2000). This may represent Implicit memory refers to memory for encoded items that are a pre-existing vulnerability. Severity of PTSD symptoms and the not associated with conscious recollection. Perceptual priming is PTSD-linked personality trait of behavioral inhibition have been a type of implicit memory in which prior exposure to a stim- correlated with facilitated eyeblink conditioning (Myers et al., ulus leads to subsequent facilitated perception of this stimulus. 2012). Furthermore, fear extinction studies have demonstrated Intrusive memories in PTSD are often triggered by sensory cues impaired safety signal learning (Orr et al., 2000; Peri et al., 2000), that individuals experienced right before or during their trau- a possible mechanism for the intractability of fear responses to matic event. Thus, several studies have examined the hypothesis reminders of a trauma decades past. A more recent study measur- that there is enhanced perceptual priming for trauma-related ing skin conductance responses in identical twins discordant for cues. Early PTSD priming studies used word-stem completion Vietnam combat exposure provided evidence that deficits in fear tasks and either failed to find evidence that individuals with PTSD extinction recall are an acquired characteristic of PTSD and not a have enhanced priming for trauma-related words (McNally and familial risk factor (Milad et al., 2008). Amir, 1996) or found only weak evidence (Amir et al., 1996). In general, neuroimaging studies of healthy individuals have Using a more sensitive word-stem completion protocol, Michael found activation of amygdala and dorsal anterior cingulate cor- et al. (2005) found that participants with assault-related PTSD tex (dACC) during fear conditioning, and activation of ventral showed preferential priming for assault-related words more than medial prefrontal cortex (vmPFC) structures during fear extinc- general threat or neutral words, relative to the control group tion and extinction recall (reviewed in VanElzakker et al., 2012). who had experienced assault but did not have PTSD. However, The first imaging study of fear conditioning in PTSD compared there may be an important reason for the inconsistent findings in a fear acquisition condition, in which a picture of a blue square word-stem priming studies: words prime conceptual or seman- was paired with shock, to a control condition, in which par- tic trauma reminders while the cues that trigger re-experiencing ticipants were shocked randomly without a CS, and found that in PTSD tend to be perceptual or sensory. Therefore, perceptual women with childhood sexual abuse-related PTSD had greater stimuli such as pictures may be more appropriate priming stimuli dACC and left amygdala activation than healthy women with no than conceptual stimuli such as words. history of abuse (Bremner et al., 2005). During extinction of the A two-part study utilizing a blurred picture paradigm reported blue square-shock association, the PTSD group had less activation that individuals with PTSD and acute stress disorder (ASD) in vmPFC structures than the comparison group. identified more blurred trauma-related pictures than blurred More recently, a series of studies compared fMRI responses neutral pictures (see Figure 2), and that this processing advan- between individuals with PTSD and trauma-exposed healthy con- tage for trauma-related pictures correlated positively with severity trol participants at each stage of a two-day fear conditioning and of PTSD symptoms, dissociative symptoms, and re-experiencing extinction paradigm. The authors reported that the PTSD group symptoms, as well as with self-reports of fear levels and perceptual had increased amygdala responsivity to the UC (shock) relative processing during the actual traumatic experience (Kleim et al., to trauma-exposed control group (Linnman et al., 2011). During 2012). A follow-up study of the individuals with ASD demon- late conditioning and early extinction, after the CS had been asso- strated that the initial processing advantage for trauma-related ciated with the US and still signaled threat, the PTSD group pictures predicted a diagnosis of PTSD 6 months post-trauma. showed increased dACC activation, relative to the control group. Blurred picture paradigms have also been used to demonstrate Presentation of the CS during late extinction learning, when the enhanced perceptual priming in healthy, trauma-unexposed indi- CS should no longer have signaled danger, also led to relatively viduals for neutral pictures that were associated with violent increased amygdala and dACC responses and relatively decreased stories, and an association between enhanced perceptual prim- vmPFC activation in the PTSD group. Furthermore, on the sec- ing and trait dissociation (Ehlers et al., 2006; Michael and Ehlers, ond day of the paradigm, during early extinction recall, the PTSD 2007). In addition, “re-experiencing” (operationalized as sensory group showed vmPFC hypoactivation and dACC hyperactivation memories imbued with a sense of immediacy) was associated with (Milad et al., 2009; Rougemont-Bücking et al., 2011)(Figure 1). greater priming, and that re-experiencing was reduced by asking These results provide a neurobiological basis to the character- participants to write about the stories and relate them to their istic unrelenting strength of trauma memories in PTSD patients personal lives, which the authors argued was a model of elab- (re-experiencing) and the mechanisms of associative learning oration of traumatic memories during clinical therapy. Future between trauma and the environmental cues that later serve as studies may replicate these findings in participants with PTSD. triggers for intrusive memories. The simple fear conditioning In a recent fMRI study of trauma-unrelated emotional prim- model of PTSD does not explain aspects of the disorder such ing, Mazza et al. (2012) administered a subliminal affective prim- as emotional responses other than fear, neuroendocrine dysfunc- ing task to 10 individuals with earthquake-related PTSD and to tion, or many of the more complex cognitive deficits discussed 10 healthy controls. In this task, the subliminal (150 ms) pre- elsewhere in this review. However, it has been a valuable model sentation of emotional faces was immediately followed by the

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FIGURE 1 | Neural correlates of extinction recall in PTSD. During early extinction recall, participants with PTSD showed hypoactivation in bilateral ventromedial prefrontal cortex (vmPFC) and hippocampus and hyperactivation in dorsal anterior cingulate cortex (ACC) relative to the trauma-exposed normal control (TENC) group. CS + E = stimulus that was extinguished; CS + U = stimulus that was not extinguished. Adapted with permission from Figure 3; Milad et al. (2009).

In summary, some priming studies demonstrate enhanced perceptual priming for threat-associated cues in both individu- als with PTSD and in healthy populations. The enhanced priming for threat cues may be associated with hyperactivity of amyg- dala and insular cortex in PTSD. Future studies should more systematically investigate differences in conceptual vs. percep- tual priming. The propensity for enhanced perceptual priming of these cues, combined with the facilitated conditioning and attenuated fear extinction recall discussed previously, may be a powerful combination in both the etiology and maintenance of PTSD.

ATTENTION AND WORKING MEMORY Attention bias FIGURE 2 | Performance on an implicit memory task (blurred picture paradigm). Patients with PTSD identified more trauma-related blurred In individuals with PTSD, trauma-related memories intrude into images than neutral images. No difference between trauma-related and consciousness and are difficult to ignore. In addition, reminders neutral pictures was observed for the No PTSD group. This figure was of traumatic events can capture attention and evoke distress and created from the data supplied in Table 3; Kleim et al. (2012). anxiety. Some researchers have hypothesized that in PTSD, atten- tion is involuntarily biased toward stimuli that are threatening, supraliminal (1850 ms) presentation of neutral pictures (Chinese leading to a disruption of ongoing cognitive activities. Researchers ideographs), which were later rated as pleasant or unpleasant. have attempted to study attention biases in the laboratory using Individuals with PTSD were more likely than controls to rate the several different paradigms: the emotional Stroop (also known ideographs that followed negative facial expressions as negative, as the “modified Stroop”), the dot probe paradigm, and the and less likely than controls to rate the ideographs that followed emotional oddball paradigm. positive facial expressions as pleasant, suggesting a propensity in In the emotional Stroop, researchers ask participants to view PTSD for priming of threat-related cues. Furthermore, during the (on a computer screen or on printed cards) words of varying emo- contrast between negative facial expression primes and the base- tional salience and to name the color of the words while ignoring line fixation dot, individuals with PTSD had significantly greater their meaning. The researchers record the time it takes for par- BOLD responses in left amygdala and right insular cortex, relative ticipants to name the colors of different types of words (e.g., to controls. trauma-related words, neutral words, positive words). Delays in

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color naming (i.e., Stroop interference) occur when the meaning (e.g., one trauma-related and one neutral) are briefly shown on of a particular category of words is closely related to the partici- either side of a screen. The participant responds when a target pants’ psychopathology and thus attracts attention despite efforts probe then appears in the location previously occupied by one of to the contrary. the stimuli. Attentional bias toward trauma-related stimuli would Several studies in the literature have reported increased result in faster reaction time during those trials in which the probe response times for trauma-related words relative to neutral words replaces the trauma-related stimulus. (and/or other types of words) in individuals with PTSD com- Dot probe studies in PTSD have reported mixed findings. pared to trauma-exposed comparison participants without PTSD Some studies have found bias toward trauma or threat-related (e.g., McNally et al., 1990; Foa et al., 1991; Cassiday et al., 1992; stimuli in PTSD (Bryant and Harvey, 1997; Dalgleish et al., 2001, Thrasher et al., 1994; Bryant and Harvey, 1995; Kaspi et al., 2003; Fani et al., 2012), while others reported an association 1995; Vrana et al., 1995; Beck et al., 2001; El Khoury-Malhame between PTSD and a bias away from trauma or threat (Pine et al., et al., 2011a). Furthermore, measures of trauma-related Stroop 2005; Fani et al., 2011). Still others have failed to find signifi- interference have been shown to positively correlate with PTSD cant attentional bias differences between PTSD and two control symptom severity (McNally et al., 1990; Cassiday et al., 1992; groups, consisting of healthy individuals and a group of recent Paunovic et al., 2002; Fleurkens et al., 2011). Stroop interfer- trauma survivors that included both individuals with and without ence in PTSD appears to be specific to trauma-related material, ASD (Elsesser et al., 2004, 2005). although some studies have reported interference to other types A recent fMRI study of the dot probe task presented angry of emotional stimuli (Litz et al., 1996; Paunovic et al., 2002). (threat-related) and happy and neutral (threat-unrelated) faces Increased interference for trauma-related words in PTSD may to female survivors of multiple traumas who either did or did not occur outside of conscious awareness, as this effect has not not have PTSD (Fani et al., 2012). Within the PTSD group but been consistently demonstrated with masked stimulus presenta- not within the control group, bias toward threatening faces corre- tions (McNally et al., 1996; Paunovic et al., 2002)butseealso lated positively with activation in the dACC and insula, as well (Harvey et al., 1996). Importantly, however, some studies have as the parietal lobe, caudate and the medial frontal, precentral failed to replicate the finding of greater interference for trauma- and parahippocampal gyri. However, there were no response time related words in PTSD (e.g., Freeman and Beck, 2000; Devineni differences between the two groups, indicating no consistent bias et al., 2004; Wittekind et al., 2010)seealso(Kimble et al., 2009). toward or away from threat. Two functional neuroimaging studies have attempted to exam- Time since trauma may be an important factor in these incon- ine the brain circuits that may mediate emotional Stroop inter- sistencies. There is evidence that, under immediate acute stress ference in PTSD (Shin et al., 2001; Bremner et al., 2004). Both conditions, individuals under threat have a bias away from threat- studies reported that the rostral anterior cingulate cortex (rACC) related stimuli, which predicts later PTSD symptoms (Wald et al., was less activated during trauma-related vs. control Stroop con- 2011). One series of studies tested this explicitly, under unique ditions in individuals with PTSD compared to trauma-exposed circumstances. During the Israeli military operation against Gaza individuals without PTSD. One of the studies also found greater (Operation Cast Lead) Israeli civilians near the border experi- activation in the dACC in PTSD during trauma-related vs. gen- enced a predictable increase in danger from retaliatory rocket erally negative Stroop conditions (Shin et al., 2001). Rostral attacks. The immediacy of danger increased as a function of prox- ACC activation may be required to effectively ignore the trauma- imity to border areas, allowing for quantification of threat. Using related information in the service of completing the color-naming a dot probe task adapted for Hebrew, researchers found that indi- (or word-counting) task at hand. When the rACC is not function- viduals under greatest imminent threat had an attentional bias ing normally, increased activation of the dACC may be required away from threat-related words (e.g., DEAD) compared to neu- in order to facilitate task performance. Interpretation of these tral words (e.g., DATA) (Bar-Haim et al., 2010). Individuals who imaging findings within the framework of earlier behavioral were more than 40 km from the border and not within rocket findings in the literature is somewhat limited by the fact that range showed attention bias toward threat-related words. PTSD response times in the neuroimaging studies were either not mea- and depression symptoms also increased as a function of threat, sured (Bremner et al., 2004) or did not show significant group and state anxiety was highest among individuals who lived within differences (Shin et al., 2001) probably due to small sample sizes. 10 km of the border and thus had 15 s or less to seek shelter when Although a useful tool for investigating the nature of intru- they heard warning sirens. One year after the conflict, attentional sive cognitions in PTSD, the emotional Stroop is limited in that bias away from threat during the acute stressor predicted PTSD it cannot be used to determine whether individuals with PTSD symptoms (Wald et al., 2011). The process by which attentional have increased attentional engagement to trauma-related stimuli bias away from threat during an acute stressor putatively trans- or delayed disengagement from them. The dot probe task (some- forms to attentional bias toward threat in PTSD may be related times called the attentional deployment task, the visual probe to the “rebound effect” discussed below in the section concerning task, or the probe detection task) represents an improvement over thought suppression. the Stroop task in that it can measure the direction of atten- Attentional bias toward threat in PTSD could reflect either tional bias (e.g., toward or away from trauma-related stimuli) as difficulty disengaging from threat-related stimuli or facilitated opposed to merely assessing the existence of interference, and can engagement of such stimuli. A study of healthy individuals that also use pictorial stimuli, reducing the need for semantic process- related attentional mechanisms to subclinical PTSD symptoms ing (MacLeod et al., 1986). In the dot probe task, two stimuli provided indirect evidence that attentional bias toward threat

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in PTSD reflects difficulty disengaging as opposed to facilitated Delis–Kaplan Executive Function System) and a digit symbol test. engagement (Bardeen and Orcutt, 2011). Interestingly, difficulty These intriguing results may suggest that engaging the lateral pre- disengaging from threatening stimuli has been associated with the frontal cortex in the face of anticipatory threat supports cognitive 5-HTTLPR serotonin transporter gene polymorphism (Beevers performance, possibly through an inhibitory mechanism. et al., 2009). Children’s 5-HTTLPR short allele significantly mod- In summary, a majority of studies have found evidence for erated the relationship between maternal criticism and the chil- attentional bias effects in PTSD. Although the findings are mixed, dren’s attentional bias for angry faces, but not happy or sad there appears to be growing evidence that the attentional bias faces, in a dot probe task (Gibb et al., 2011). This same poly- reflects difficulty disengaging from, rather than facilitated detec- morphism may predict poor response to cognitive-behavioral tion of, negative stimuli. Collectively, the brain regions consis- therapy in PTSD (Bryant et al., 2010). Furthermore, an fMRI tently active during tasks of negative attention in PTSD include study of a related attentional task called the detection of tar- the dACC, amygdala, insula, with mixed findings of the vmPFC. get (DOT) paradigm demonstrated that amygdala activation The aforementioned regions have previously been associated with in PTSD patients, but not in healthy controls, correlated with emotional reactivity, perhaps underlying privileged processing of attentional bias toward threatening faces and words (El Khoury- negative images in PTSD. Malhame et al., 2011b). Future studies can better elucidate the relationships among time since trauma, serotonin function in the Working memory amygdala, and attentional processes in PTSD. Working memory is often defined as the maintenance and manip- The emotional oddball paradigm has proved to be useful in ulation of information in a temporary memory store (Baddeley, demonstrating attention bias in PTSD. In this task, infrequent 1992). Importantly, working memory has a limited capacity, target stimuli are interspersed with frequent standard stimuli and suggesting that individuals can track and work with a small infrequent distractor emotional stimuli. The task requires partici- amount of information at a given time. An implication of pants to inhibit their prepotent response to frequent standard and this limited capacity store is that interference from distract- distractor stimuli in order to identify the target stimuli accurately. ing stimuli can reduce an individual’s ability to maintain goal- Patients with PTSD are impaired in identifying neutral targets, relevant information. The interference of distracting stimuli, which may be a consequence of attention bias to distracting, such as intrusive thoughts and trauma memories seems to be potentially threat-related information (Pannu Hayes et al., 2009). a particular difficulty in PTSD and may underlie the hallmark Furthermore, event-related potential (ERP) studies have shown symptom of difficulty with concentration. Working memory that during processing of threat stimuli, an enhanced P3 ampli- deficits in patients with PTSD have been demonstrated using tude response is observed in patients with PTSD, which is thought both verbal and visual stimuli. Schweizer and Dalgleish (2011) to reflect heightened attention toward those stimuli (Attias et al., reported poorer working memory performance in patients vs. 1996; Stanford et al., 2001). More recently, fMRI studies using trauma-exposed controls on a verbal sentence task, in which the emotional oddball paradigm demonstrated that PTSD symp- participants were instructed to remember words presented fol- tomatology was associated with greater activity in the dorsolateral lowing trauma-related or neutral sentences. Consistent with the prefrontal cortex and vmPFC for threat stimuli (Pannu Hayes idea that trauma-related material is particularly disruptive to et al., 2009), accompanied by a reduction in dorsolateral pre- working memory performance, memory was worse for words frontal cortex activity for target, non-threat stimuli (Morey et al., presented after trauma vs. neutral sentences. Working mem- 2008; Pannu Hayes et al., 2009). These studies provide a neural ory difficulty was observed in both participants with a current marker for threat bias in PTSD that is characterized by heightened diagnosis of PTSD and individuals with a lifetime history of activity in putative attention and emotion circuitry for potentially PTSD. threatening information and dysfunction in attention circuitry Neuroimaging studies investigating the impact of emotional during goal-relevant target identification. distraction on working memory have suggested that hyperac- Anticipation of an impending negative stimulus may influ- tivity in an emotional processing network (including regions ence attention allocation and subsequent cognitive performance. such as the amygdala, ventrolateral prefrontal cortex, and medial Researchers have examined whether women exposed to inti- prefrontal cortex) and hypoactivity in a dorsal executive func- mate partner violence show alterations in attention performance tion processing network (including regions such as the dorso- and neural circuitry while anticipating a negative visual stimulus lateral prefrontal cortex and parietal cortex) underlies impaired (Simmons et al., 2008; Aupperle et al., 2012a). One particu- maintenance of information in working memory as a result of lar study with a large sample size (41 women with PTSD and emotional distraction (Dolcos and McCarthy, 2006). This model 34 healthy controls) examined the neural correlates of negative was supported in an fMRI studying examining working mem- and positive anticipation embedded within a continuous per- ory in PTSD. Morey et al. (2009) showed that patients with formance task (Aupperle et al., 2012a). Results indicated that PTSD had poorer memory performance when both neutral and patients with PTSD showed greater activity in the insula and less trauma-specific distracters were presented during the working activity in the dorsolateral prefrontal cortex than controls dur- memory delay in comparison to a trauma-exposed control group. ing anticipation of negative events. Furthermore, greater activity Furthermore, this fMRI study showed disrupted activity in the in the dorsolateral and ventrolateral prefrontal cortex was associ- dorsal executive function network during the working memory ated with better performance on an attention switching task (i.e., delay in PTSD that could explain the diminished performance. the Color–Word Interference Inhibition/Switching subtest of the An interesting outcome of this study is that performance was

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disrupted for both trauma-specific and neutral distracters, per- (Resick and Schnicke, 1993). Preliminary evidence suggests that haps providing evidence for generalized hypervigilance. these types of interventions not only reduce symptoms, but also improve cognitive performance (Sutherland and Bryant, 2007). DECISION-MAKING AND REWARD PROCESSING In PTSD, experimental work investigating the cognitive con- Individuals make decisions in part based on motivational influ- trol of emotion has examined whether patients can purposely ences, weighing the rewards and costs that may result from each forget negative information. Some researchers have suggested that option. On one end of the spectrum, seeking immediate posi- patients with PTSD have an enhanced ability to forget informa- tive rewards is associated with the psychopathology of addiction tion, which may explain amnesia for important details of their disorders (Bechara et al., 2002) while on the other end of the traumatic event. This idea, mainly evolving out of the child sex- spectrum, lack of reward seeking is associated with depressive ual abuse literature, suggests that repeat trauma survivors with disorders (Pizzagalli et al., 2008). In PTSD, numbing symptoms PTSD cope during their trauma by dissociating from their sur- including loss of pleasure in activities and loss of the ability to roundings and disengaging attention from the event, sometimes experience positive emotions may suggest altered processing of leading to amnesia for large stretches of time (Terr, 1991). This positive rewards. Consistent with this notion, patients with PTSD avoidant coping style may manifest in adulthood by increased are less satisfied with rewards than controls (Hopper et al., 2008) ability to forget new information presented in an experimental and expend less effort to obtain positive rewards (Elman et al., setting (McNally et al., 1998). Alternatively, others have suggested 2005). Thus, it follows that patients with PTSD may have altered that intrusive memories arise from the failure of inhibitory pro- decision-making capacity if the drive to achieve positive rewards cesses to curb distracting and aversive memories (Zwissler et al., is reduced. 2011). Neuroimaging studies in healthy individuals have supported One frequently used paradigm to examine this issue is the the notion of a putative reward circuit that includes the ventral directed forgetting task, which examines deliberate attempts striatum, ventral pallidum, orbital frontal cortex, and anterior to control memory performance. In this task, participants are cingulate. Two studies have examined the neural correlates of instructed to either remember or forget words presented in a decision-making and reward in PTSD, both providing evidence list. Subsequently, participants attempt to recall and/or recog- for reduced capacity for positive reward in PTSD. Sailer et al. nize all the words that were presented in the list regardless of (2008) showed that the nucleus accumbens (part of the ventral whether they were to-be-remembered or to-be-forgotten. The striatum) was less active in patients with PTSD than controls “standard directed forgetting effect” refers to the behavioral out- during processing of positive gains. Behaviorally, patients with come showing greater remembering for items presented during PTSD were slower in learning how to maximize their gains in a the remember condition than the forget condition. The task is monetary gain/loss paradigm. Although speculative, it is possi- often adapted for study of PTSD by including general emotional ble that reduced reward processing in PTSD may have negatively or trauma-specific words. Two studies that examined directed for- influenced patients’ motivation in learning the task. Similarly, getting of trauma-relevant information in PTSD failed to show PTSD patients showed reduced activity in the striatum during between group differences among PTSD and control participants gains vs. losses of a monetary task in another study (Elman et al., (McNally et al., 1998; Zoellner et al., 2003). However, these stud- 2009). Interestingly, striatal activity for gains vs. losses was neg- ies and others have demonstrated differences between groups atively correlated with CAPS items “loss of interest in significant for non-trauma emotional and/or neutral stimuli. Specifically, activities” and “feelings of detachment/estrangement.” patients fail to show the standard directed forgetting effect either due to difficulty forgetting to-be-forgotten items (Zoellner et al., COGNITIVE CONTROL OF EMOTION AND TREATMENT 2003; Cottencin et al., 2006) or decreased performance in the EFFECTS remember condition (McNally et al., 1998; Zwissler et al., 2011). When distressing events occur during the course of the lifes- Taken together, the directed forgetting literature provides lit- pan, individuals often engage in various strategies to manage tle evidence that patients with PTSD adopt an avoidant coping and cope with negative emotions. In doing so, they can change style that results in enhanced forgetting of negative information. their emotional experience of the stimulus, and also change Rather, a general inhibitory control mechanism may be impaired how the emotional stimulus affects their cognitive performance. evidenced by poorer performance for non-threat related items. Individuals can exercise control of emotion for the desired effect; A separate literature has emerged examining the effects of they can engage in cognitive reappraisal to improve affect, or con- actively suppressing one particular thought. Unlike directed for- versely, amplify negative affect (Dillon et al., 2007). Furthermore, getting paradigms, thought suppression is less concerned with cognitive control strategies can be used to improve memory recall and recognition memory performance but rather the fre- performance (Hayes et al., 2010) or suppress unwanted memo- quency with which thoughts arise following instructions to sup- ries (Depue et al., 2007). Such deliberate modulation of emo- press them. Wegner and colleagues demonstrated that when tion serves to manage distractions in the face of otherwise participants were instructed to initially suppress a thought, they debilitating affect and helps individuals to remain focused on went on to think about it to a greater extent than if they were ini- goal-directed behaviors. In treating psychopathology, cognitive- tially allowed to let the thought enter consciousness, referred to as behavioral interventions often instruct patients to exercise greater a “rebound effect” (Wegner et al., 1987). Two studies have shown control of emotion through thought challenging exercises and that patients with PTSD have more trauma-related thoughts promoting alternative ways of thinking about a negative situation after a thought suppression period than trauma-exposed controls

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which may suggest that controls engage in cognitive control to a greater extent than patients with PTSD. Psychosocial treatment interventions may benefit patients by teaching them the cognitive control skills necessary to manage their symptoms, thereby reducing the detrimental effect of strong negative emotion on cognitive performance. Alternatively, drug therapies may directly affect neural circuitry and consequently blunt the effect of emotion on cognitive function. A few studies have examined the extent to which therapy improves cognitive function in PTSD. Although the evidence is limited, there is a small body of data that supports the effectiveness of therapy on normalizing cognitive function in certain domains in patients. Sutherland and Bryant (2007) reported improved autobiographi- cal memory specificity in PTSD after treatment. Two studies have reported improved emotional Stroop performance in patients relative to controls after psychosocial intervention (El Khoury- Malhame et al., 2011a; Thomaes et al., 2012). Finally, Putman et al. (2007) reported a reduction in color naming response times to masked fearful vs. neutral facial expressions after a 40 mg dose of hydrocortisone (vs. placebo) in highly anxious men. Although this study did not include individuals with PTSD, its findings FIGURE 3 | Performance on a thought suppression task. (A) Patients seem to call for examining the effect of glucocorticoids on emo- with PTSD reported more trauma-related (i.e., motor vehicle accident, tional Stroop interference in PTSD, especially given that the MVA) thoughts after engaging in thought suppression, showing a administration of glucocorticoids has been associated with symp- “rebound” effect. (B) Participants did not show a rebound effect for neutral tomatic improvement (e.g., Surís et al., 2010) and a reduction of thoughts. Reproduced with permission from Shipherd and Beck (2005). fear responses in this disorder (e.g., Jovanovic et al., 2011; Miller et al., 2011), but see also (Grossman et al., 2006). Other stud- (Shipherd and Beck, 1999, 2005)(seeFigure 3). In another study ies, however, have not found effects of treatment on emotional that instructed participants to suppress neutral information, Stroop measures in PTSD (Devineni et al., 2004; Taylor et al., combat veterans with PTSD had greater combat-trauma related 2006). Clearly, additional research is necessary to examine what intrusions during attempts to suppress thoughts about a “white types of treatments may confer benefits in cognitive function to bear” than combat veterans without PTSD (Aikins et al., 2009). individuals with PTSD. These studies suggest that attempts at thought suppression might in fact be associated with greater frequency of trauma-related SUMMARY AND FUTURE DIRECTIONS cognitions in PTSD. Theliteraturesummarizedhereprovidesstrongsupportfor Other forms of cognitive control include emotion regulation the privileged processing of emotionally charged information in strategies, in which participants are instructed to change their PTSD. A key question is whether emotional information facil- natural response to a stimulus. Gross and colleagues have shown itates or interferes with cognitive processing. In other words, that individuals can engage in thought-change strategies, such as does PTSD confer advantages in cognitive performance given cognitive reappraisal, to deliberately reduce negative affect (Gross, that emotional stimuli are often processed with greater efficiency 1998). Most studies examining emotion regulation in PTSD have than neutral stimuli? Over the span of different study paradigms, used self-report measures to examine the frequency with which there appears to be a trade-off in cognitive performance as cogni- these different strategies are used and whether they are associated tive models of PTSD predict; although fear learning, perceptual with greater or reduced frequency of trauma symptoms. However, priming, and recall memory for negative items are sometimes there appears to be only one paper to date that has directly enhanced in PTSD, this advantage comes at the expense of pro- manipulated emotion regulation strategies in PTSD (New et al., cessing other types of information. For example, task-irrelevant 2009). This fMRI study compared sexual assault victims with and emotional information slows processing of goal-directed activity without PTSD on an emotion regulation task. Participants were and interferes with memory and learning of neutral informa- shown negative photos and instructed to down-regulate their tion. Furthermore, extinction learning and learning of safety cues emotional response to the picture (diminish condition), enhance is often impaired, memory for specific, detailed information is their negative response, or maintain their current response to the often poor, and patients with PTSD may be more prone to falsely picture. Behavioral results showed that the healthy control group remembering novel information. Deficits in cognitive control and was able to diminish negative affect to a greater extent than the emotion regulation may be exacerbated by the impact of emotion PTSD group whereas no group difference was observed in the on cognitive function. enhance condition. Imaging results showed that the control group Neuroimaging studies have uncovered several key brain recruited greater prefrontal cortex activity across superior and regions that may underlie the emotional bias effects observed middle frontal gyri for both the diminish and enhance conditions, in PTSD. Across studies, activity appears to be altered in

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the anterior cingulate cortex, vmPFC, amygdala, hippocampus, However, a number of key questions need to be further examined insula, and lateral prefrontal cortex. Findings from quantitative to gain a better understanding of how emotion affects cognitive meta-analyses of the neural correlates of PTSD have confirmed function in PTSD. An important consideration is the extent to the importance of these regions in PTSD (Etkin and Wager, 2007; which individual differences and moderating factors impact the Hayes et al., 2012; Simmons and Matthews, 2012). A recent meta- development of PTSD. There is some evidence that deficits in analysis of imaging studies in PTSD showed that the amygdala configural cue processing and lower IQ precede the development and mid-ACC is hyperactive, whereas lateral and medial pre- of PTSD (Gilbertson et al., 2007; Vasterling et al., 2002). Further frontal cortex is hypoactive in PTSD for negative emotional stim- research is necessary to determine whether impairment in other uli vs. neutral and positive stimuli (Figure 4). A neurocircuitry cognitive processes precede trauma exposure and, conversely, the model of PTSD posits that dysfunction of the vmPFC prefrontal extent to which cognitive control and emotion regulation capacity cortex results in failure to inhibit an overactive amygdala, lead- prior to trauma exposure can offer resilience. ing to an exaggerated fear response and impaired fear extinction Currently, little is known regarding the neurobiology of cogni- learning (Rauch et al., 2006). Hippocampal dysfunction may tive control in PTSD. Surprisingly few studies have examined the be related to impairment in processing contextual information neural correlates of deliberate attempts to control emotions. As (Rauch et al., 2006; Hayes et al., 2011). The dACC, anterior reviewed above, there is presently only one neuroimaging study insula, and amygdala, among other regions, comprise a putative investigating emotion regulation in PTSD (New et al., 2009). “salience network” that processes information of personal rele- This area needs to be developed to further examine whether vance and is hyperresponsive in individuals with anxiety (Seeley impairment in the cognitive control of emotions is a PTSD et al., 2007). Researchers have posited that, in PTSD, hyperre- symptom-maintaining factor and whether neural abnormali- sponsivity of salience network regions and hyporesponsivity in ties during top-down regulation of emotion represents a useful putative regions important for cognitive control and working biomarker for the diagnosis of PTSD. Moreover, further exami- memory underlie greater distribution of processing resources in nation of the interplay between medial temporal lobe structures favor of potentially threatening stimuli even when neutral infor- and the prefrontal cortex is necessary to better understand con- mation is goal-relevant (Morey et al., 2009; Pannu Hayes et al., trol processes during emotional memory encoding and retrieval. 2009; Hayes et al., 2012). In healthy individuals, prefrontal cortex activity is associated with As reviewed in this paper, our understanding of emotion- deep semantic encoding that supports improved recall of emo- cognition interactions in PTSD has progressed tremendously tional memories (Ritchey et al., 2011), as well as suppression over the last two decades and neuroimaging research has iden- of aversive memories that reduces recall (Depue et al., 2007). tified pathways involved in the effect of emotion on cognition. However, less is known regarding the extent to which patients with PTSD can engage critical prefrontal cortex regions to influ- ence the memorability of emotional stimuli. Another emerging area of research is using drug therapies to manipulate emotion-cognition interactions. Norepinephrine has been shown to enhance emotional memory whereas adren- ergic receptor blockers such as propranolol compromise the enhancing effect that emotional arousal has on memory (Cahill et al., 1994). Cerebrospinal norepinephrine levels are elevated in chronic PTSD (Geracioti et al., 2001) and research regard- ing the effectiveness of adrenergic blockers in preventing PTSD is underway. Although preliminary results have not yielded strong evidence to recommend the use of propronolol for the prevention of PTSD (Pitman et al., 2002; Vaiva et al., 2003; Hoge et al., 2012), further research is necessary to determine the precise time window in which such drug therapies may be useful (Cain et al., 2012). Furthermore, additional research is required to examine whether these drugs impact specific types of memory (e.g., explicit vs. implicit memory, autobiographi- cal vs. memory for general negative events, central vs. peripheral details). FIGURE 4 | Meta-analysis of functional neuroimaging studies in PTSD. Finally,averyimportantareathatisunderstudiedisthecom- Across various task designs, the amygdala and mid-ACC are hyperactive in monalities or specificity of cognitive alterations in PTSD vs. PTSD whereas the lateral and medial prefrontal cortex are hypoactive for negative emotional stimuli vs. neutral and positive stimuli. Areas of other comorbidities such as depression, traumatic brain injury, hyperactivation in PTSD (PTSD > Control) are shown in yellow and areas of and attention deficit and hyperactivity disorder. In many cases, hypoactivation in PTSD (Control > PTSD) are shown in blue. AMY = cognitive abnormalities are observed across different mood and amygdala, IFG = inferior frontal gyrus, L = left, mid-ACC = mid anterior anxiety disorders. For example, overgeneral autobiographical = = cingulate cortex, R right, vmPFC ventromedial prefrontal cortex. memory is also a characteristic of individuals diagnosed with Reproduced from Hayes et al. (2012). depression. Although many studies of PTSD focus on the fear and

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anxiety based symptoms such as hypervigilance, it is possible comorbidities to better determine the origin of and potential that many of these cognitive deficits are related to the dyspho- treatments for PTSD. ria and maladaptive appraisals that are often observed in PTSD. In fact, in recognition of these common symptoms, the proposed ACKNOWLEDGMENTS changes to the current diagnosis of PTSD for DSM-V may add a The authors were supported by grants from the National Institute fourth symptom cluster of “negative alterations in cognitions and of Mental Health (K23 MH084013 awarded to Jasmeet P. Hayes mood” (Friedman et al., 2011). Furthermore, a movement toward and 5R01MH054636 awarded to Lisa M. Shin) and a National dimensional classification of symptoms that are shared among Defense Science and Engineering Graduate Fellowship (awarded disorders is gaining momentum (Ofrat and Krueger, 2012). It to Michael B. VanElzakker). These funding sources had no further is therefore important to understand the similarities and differ- role in the interpretation of the findings, writing of the paper, or ences in emotion-cognition interactions between PTSD and other approval of the paper.

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