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Greater avoidance behavior in individuals with posttraumatic stress disorder symptoms

Greater avoidance behavior in individuals with posttraumatic stress disorder symptoms STRESS, 2017 VOL. 20, NO. 3, 285–293 http://dx.doi.org/10.1080/10253890.2017.1309523 ORIGINAL RESEARCH REPORT Greater avoidance behavior in individuals with posttraumatic stress disorder symptoms a,b c c c d c,e Jony Sheynin , Christine Shind , Milen Radell , Yasheca Ebanks-Williams , Mark W. Gilbertson , Kevin D. Beck c,e and Catherine E. Myers a b Veterans Affairs Ann Arbor Healthcare System, Ann Arbor, MI, USA; Department of Psychiatry, University of Michigan, Ann Arbor, MI, USA; c d Department of Veterans Affairs, New Jersey Health Care System, East Orange, NJ, USA; Department of Veterans Affairs, Manchester, NH, USA; Department of Pharmacology, Physiology & Neuroscience, New Jersey Medical School, Rutgers University, Newark, NJ, USA ABSTRACT ARTICLE HISTORY Received 19 October 2016 While avoidance is a core symptom of PTSD, little is known about whether individuals with PTSD show Revised 6 February 2017 a general cognitive bias to acquire and express avoidance, in situations not related to trauma or fear. Accepted 8 March 2017 Here, we used a computer-based task to examine operant acquisition and extinction of avoidance in participants with and without severe self-reported PTSD symptoms. A total of 119 participants (77 male, 42 female; 74 veteran, 45 civilian) with symptoms (PTSS; n¼ 63) or with few/no symptoms (noPTSS; KEYWORDS n¼ 56) performed a task, in which they controlled a spaceship and could shoot a target to gain points Avoidance; posttraumatic or hide in “safe areas” to escape or avoid on-screen aversive events. Results show that participants with stress disorder; gender PTSS exhibited more avoidance across trials than noPTSS participants, particularly due to more avoid- differences; computer-based ance behavior in PTSS females compared to noPTSS females. Avoidance behavior decreased across task; assessment tool extinction trials but interactions with PTSS and gender fell short of significance. Overall, PTSD symptoms were associated with propensity to acquire and express avoidance behavior, in both civilians and veter- ans, and even in a cognitive task that does not explicitly involve trauma or fear. This effect was more pronounced in females, highlighting the role of gender differences in PTSD symptomatology. Importantly, this study also demonstrates the potential of an objective assessment of avoidance behav- ior, which could be used to supplement the common but limited self-report tools. Introduction lead to the development of better therapeutic strategies to manage or reduce PTSD symptoms (PTSS), as well as ways to Posttraumatic stress disorder (PTSD) can develop following identify individuals at highest risk for PTSD following trauma exposure to a traumatic event; symptoms include cognitive exposure. and behavioral avoidance of reminders of the trauma Avoidance learning is a complex phenomenon that (American Psychiatric Association, 2013). These avoidant includes both aversively motivated learning and reward learn- behaviors tend to increase over time subsequent to the incipi- ing; the balance between these two processes influences the ent traumatic event (Foa et al., 2006; Karamustafalioglu et al., degree and expression of avoidance (Stein & Paulus, 2009). 2006), and the degree of increased avoidance can differentiate Computer-based tasks, in which participants learn to avoid between those trauma-exposed individuals who develop PTSD on-screen aversive events (such as point loss or destruction and those who recover (Foa et al., 2006; North et al., 2004; of the participant’s avatar), can provide a useful tool to exam- O'Donnell et al., 2007). Lifetime prevalence of PTSD among ine how individuals acquire and express avoidance behavior. adult Americans is estimated at about 6.8% (Kessler et al., In one recent study, male veterans learned to categorize stim- 2005); however, some populations may have much higher risk. uli in order to obtain reward (point gain) and avoid punish- For example, the prevalence of PTSD may be twice as high in ment (point loss); participants with severe PTSD symptoms females as in males (Kessler et al., 2005), while lifetime preva- outperformed those with few/no symptoms (Myers et al., lence among veterans may reach 15–20% (Hoge et al., 2004; 2013). In another computer task, where participants guided Magruder et al., 2016), presumably reflecting stressors such as an on-screen character (avatar) through several scripted scen- deployment, wartime service and exposure to combat arios, such as attending a party or participating in a volunteer (Dohrenwend et al., 2006; Kessler et al., 1995; Wolfe et al., activity, severity of self-assessed PTSD symptoms correlated 1999). Given the prevalence and costs of PTSD, better under- with participants’ tendency to display avoidant behavioral standing of how avoidance is acquired and expressed could patterns (Myers et al., 2016). However, in the first task, CONTACT Catherine E. Myers [email protected] Research Services, VA New Jersey Health Care System, 385 Tremont Avenue, East Orange, NJ 07018, USA 2017 US Government author 286 J. SHEYNIN ET AL. subjects learned to select between predefined alternative flyers and word-of-mouth referral. One participant withdrew responses (categorization), while in the second, subjects did from the testing session before completing the spaceship not receive explicit feedback for their responses. Thus, neither task, and a second participant failed to complete the task task fully examined the manner in which subjects discover due to experimenter’s error. A third participant’s testing ses- and acquire avoidance responses, nor the rate at which these sion was terminated early due to a medical condition (glau- avoidance responses extinguish when there is no longer any coma), which made it difficult for the participant to tolerate threat. viewing the computer screen. Data from these three partici- Recently, we developed and validated a computer-based pants were excluded from analysis, leaving a final set of 119 task in which the participants control an on-screen spaceship participants. Several additional participants had physical chal- and fire at targets to gain points (Sheynin et al., 2014a; lenges (e.g. prosthetic eye or wheelchair-bound); however, these individuals were able to position themselves comfort- Sheynin et al., 2014b). At intervals, a series of on-screen ably to view the computer screen and register their explosions occurs, which damages the participants’ ship and responses, and so they were not excluded from participation. causes accumulating point loss. A warning signal on the One female participant had a history of military service but screen predicts upcoming threat; participants can learn to did not qualify for veterans benefits; her data were included avoid the point loss by hiding their spaceship in response to in the veteran sample. Participants received $40 reimburse- this warning signal. In prior studies with this task, young ment for a single 2-h testing session. All participants signed adults with inhibited temperament, an increased tendency to statements of informed consent at the start of the session. withdraw from or avoid aversive situations, showed more Procedures were approved by the VANJHCS Institutional avoidance behavior than uninhibited peers; there was also an Review Board and conformed to guidelines for the protection effect of gender, with females showing longer avoidance of human subjects established by the Declaration of Helsinki responses than males (Sheynin et al., 2014a). Note that longer and the US Federal Government. avoidance duration (e.g. initiate hiding as soon as the warn- Participants completed a demographic questionnaire that ing signal appeared) was suboptimal; rather, the optimal included questions about gender, age, education and details response was to continue shooting to gain points for as long of military service. When asked to self-identify race, 84 self- as possible, and then hide at the last possible moment to identified as Black/African-American, 18 as White/Caucasian, avoid the upcoming threat. In a follow-up study, females also and 17 as other, Mixed Race or declined to specify. When showed slower extinction, continuing to emit avoidance asked to self-identify ethnicity as Hispanic or non-Hispanic, 5 responses even when the aversive event no longer followed self-identified as Hispanic, 111 self-identified as non-Hispanic the warning signal (Sheynin et al., 2014b). These results are and 3 declined to specify ethnicity. intriguing, since both inhibited temperament (Biederman Participants reporting prior military service (n¼ 74) were et al., 1993; Hirshfeld et al., 1992; Rosenbaum et al., 1993) also administered the Combat Exposure Scale (CES; Keane and female gender (Tolin & Foa, 2006) have been noted as et al., 1989); following prior studies (Ginsberg et al., 2008; risk factors for the development of PTSD following trauma Myers et al., 2012), those scoring below 8 on the CES were exposure. classified as non-combat-exposed (n¼ 47) and the remainder Here, we adapted the spaceship task to examine acquisi- as having a history of exposure to combat (n¼ 27). Asked tion and extinction of avoidance in adults with vs. without about specific conflicts in which they had served, 27 reported severe PTSS. Our prediction was that, since avoidance is a Vietnam, 11 Gulf War/Operation Desert Storm, 10 Operation core feature of PTSD, participants with severe PTSS would Enduring Freedom/Operation Iraqi Freedom, 13 Other (e.g. show greater acquisition, and reduced extinction, compared Beirut, Somalia, Korea, Iraq/Operation Southern Watch), and to those with few/no PTSS. Given high rates of PTSD in 23 reported no specific conflict or peacetime service; veterans, particularly combat-exposed veterans, we included numbers sum to greater than 74 due to some veterans civilians, combat-exposed veterans, and non-combat exposed whose service spanned multiple conflicts. In summary, three veterans in our sample, to determine whether history of subject groups were included: combat-exposed veterans, military service and/or combat exposure affected avoidance non-combat-exposed veterans and civilians (never served in in the task. We were also interested in whether the the military, n¼ 45). Table 1 shows demographic characteris- pattern would be similar among males and females, given tics for each group. data suggesting that females are at higher risk for PTSD All participants also completed the PTSD Checklist-Civilian (Tolin & Foa, 2006) and that the course and expression of version (PCL-C), a 17-item questionnaire that asks about pres- PTSD may be different in females than in males (Olff et al., ence and frequency of PTSS not necessarily military in nature 2007). (Blanchard et al., 1996). PCL scores of 50þ have been shown to predict PTSD in military samples (Blanchard et al., 1996; Methods Weathers et al., 1993); based on this criterion, participants were classified with current severe PTSD symptoms (PTSS), or Participants few/no PTSS (noPTSS). PTSS rates were higher among males (47 of 77) than females (16 of 42; Yates-corrected chi-square, One hundred and twenty-two participants (including 76 vet- v ¼4.86, df¼ 1, p¼ .028, Cramer’s V¼ .22), but did not differ erans and 46 civilians without military experience) were between combat and non-combat groups or between civil- recruited from the Veterans Affairs New Jersey Health Care System (VANJHCS) and surrounding community, by posted ians and either veteran group (all p> .100). STRESS 287 Table 1. Demographic characteristics and questionnaire scores for the three participant groups. Combat-exposed veterans Non-combat exposed veterans Civilians N27 47 45 Gender Two females (7.4%) 10 females (21.3%) 30 females (66.7%) Age (years) 52.2 (SD 11.0) 55.7 (SD 10.6) 47.5 (SD 16.4) Education (years) 15.1 (SD 3.0) 14.6 (SD 1.9) 14.9 (SD 2.4) CES score 17.8 (SD 7.9) 1.8 (SD 2.7) N/A PCL score 57.3 (SD 14.5) 51.0 (SD 16.6) 39.2 (SD 15.6) PTSS cases 21 (77.8%) 28 (59.6%) 31 (68.9%) throughout the subsequent punishment period). In both Spaceship avoidance task cases, if the participant emerged from hiding before the The spaceship avoidance task was a modification of that end of the punishment period, point loss would resume. previously described (Sheynin et al., 2014a, 2014b, 2016); an Importantly, participants were not given any explicit instruc- executable version of the software is available for replication tions about the safe areas or the hiding response. and additional study on the Open Source Framework (OSF) at The task was divided into acquisition and extinction www.osf.io/p78fr. The software was programed in SuperCard phases. The acquisition phase consisted of 12 trials, each version 3.7.1 (Solutions Etcetera, Pollock Pines, CA) and pre- composed of a warning period, a punishment period and ITI, sented on a Macintosh iMac computer. The keyboard was as described earlier. The transition to the extinction phase masked except for three keys labeled FIRE, LEFT and RIGHT, was not signaled to the participant; it consisted of 12 extinc- which the subject could use to enter responses. At the start tion trials which were similar to the acquisition trials except of the experiment, the following instructions appeared: "You that the mothership never fired lasers and point loss never are about to play a game in which you will be piloting a occurred. Prior to the first acquisition trial, participants spaceship. You may use LEFT and RIGHT keys to move your received 1 min of practice time, during which target ships spaceship [picture below], and press the FIRE key to fire appeared and the participant could shoot to gain points. lasers. Your goal is to maximize your total score. The total A running tally at the bottom of the screen showed the cur- score will be displayed at the bottom of the screen. (We’ll rent points accumulated, which was initialized to 325 at the start you off with a few points now.) Good luck!" start of the experiment. In the task, participants controlled a spaceship, and could move it left and right across the bottom of the screen, using the LEFT and RIGHT keys. Target spaceships periodically Post-task questionnaire appeared at one of six locations on the screen for approxi- mately 2 s, and participants could use the FIRE key to shoot After finishing the task, participants completed a paper- at and attempt to destroy these ships; participants gained and-pencil questionnaire asking about experience with one point for every target ship successfully destroyed (Figure computer games, whether participants noticed the different 1(A,B)). Every 20 s, a large “mothership” appeared on the objects that appeared during the task and understood their screen, and remained for a 5 s warning period, during which meaning, along with an open-ended question asking partic- no target ships appeared (Figure 1(C)). The warning period ipants what they thought was the purpose of the task. was followed by a 5 s punishment period, during which the The purpose of these questions was to determine whether mothership would fire lasers at the participant’s ship (Figure differences in computer familiarity or understanding of 1(D)). The punishment period was divided into five 1-s seg- task demands might underlie any group differences in ments; during each segment, there was an explosion of the performance. participant’s ship and a loss of 5 points, up to a maximum of 25 points. The punishment period was followed by a 10 s intertrial interval (ITI) before the onset of the next warning Data analysis period. Every 100 ms, the program recorded whether the participant’s Throughout the experiment, two shelters representing spaceship was inside one of the designated safe areas. For “safe areas” were present at the left and right corners of the each trial, avoidance hiding was defined as the percent of screen. When the participant moved left or right into one of time spent hiding during the 5 s warning period, and escape these areas, the participant’s ship entered the safe area and a hiding was defined as the percent of time spent hiding dur- door closed behind the ship (“hiding”; Figure 1(E)). While ing the subsequent 5 s punishment period. Avoidance and hiding, the participant’s spaceship could not be hit by the escape hiding were scored for the acquisition and extinction mothership’s lasers, and no point loss occurred, but neither phases, even though there was no possibility of punishment could the participant shoot at targets and acquire points during the extinction phase. ITI hiding was defined as the (Figure 1(F)). Hiding during a punishment period was defined percent of time spent hiding during the 10 s ITI between tri- as “escape hiding,” and terminated point loss (for as long as als, averaged separately across the acquisition and extinction the participant remained in hiding, up to the full length of phases. Several additional task variables were scored for each the punishment period). Hiding during the warning period was defined as “avoidance hiding,” and could cause complete participant, including total score at the end of the task, num- omission of point loss (if the participant remained in hiding ber of shots fired (presses on the FIRE key), locomotion 288 J. SHEYNIN ET AL. Figure 1. Screen events during the spaceship avoidance task. (A) The participant’s ship could move from left to right and fire at target ships that appeared at inter- vals; (B) successful “hits” were rewarded with 1 point. (C) During the warning period of each trial, a mothership appeared, and the participant’s lasers were ineffect- ive against it. (D) In the subsequent punishment period, the mothership fired lasers repeatedly, each time exploding the participant’s spaceship and causing a loss of 5 points, to a maximum of 25 points lost. (E) The participant could escape or avoid point loss by hiding in either of the two designated “safe areas” at the sides of the screen; the door slid shut behind the participant, or opened when the participant emerged. (F) While the participant’s ship was hidden, the mothership’s lasers were ineffective (no destruction or point loss). The participant could thus hide during the punishment period to terminate point loss (escape response), or pre- vent point loss all together by hiding during the warning period and remaining hidden throughout the subsequent punishment period (avoidance response). (presses on the LEFT or RIGHT keys) and total targets shot on a 2 2 table, Yates Continuity Correction was applied (equivalent to points gained) across the task. to adjust expected values. Where data failed assumptions Statistical analyses were conducted using IBM SPSS version of equality of variance/sphericity, appropriate corrections were used (Greenhouse-Geisser for ANOVA, Welch’s t for 22. Primary analyses for hiding performance were mixed t test) to correct degrees of freedom. The threshold for sig- ANOVA with and within-subjects factors of trial, or univariate nificance was set at .05; effects that did not approach ANOVA (for other task variables), with factors of group significance (p> .100) were generally not discussed. Where (civilian, non-combat veteran, combat veteran), gender and multiple tests were conducted, Bonferroni’s correction was PTSS status (PTSS, noPTSS). Significant results were followed used to protect against inflated risk of family-wise type-I up as appropriate by post hoc tests. Chi-square test was error. used for comparison of distributions. For chi-square tests STRESS 289 Figure 2. Escape hiding (hiding during punishment period) across the 12 acquisition trials for (A) all n¼ 119 participants, (B) n¼ 105 excluding 14 non-escapers. Error bars represent standard error of the mean. Avoidance hiding decreased across extinction trials Results (Figure 4; F(7.15,665.00)¼ 3.77, p< .001, partial g ¼ .04) with Escape/avoidance behavior no effect of group, gender, or PTSS, although both the Escape hiding increased over the 12 acquisition trials trial PTSS group interaction and the trial PTSS group (Figure 2), as indicated by a main effect of trial (mixed gender interaction approached significance (both .05< ANOVA, F(4.80, 513.44)¼ 13.54, p< .001, partial g ¼ 0.11) p< .100). with no effects of group or gender and no interactions (all p> .090). A subset of 14 participants (11.8%) showed no escape hiding during the experiment. There were no differen- Other performance measures ces between escapers and non-escapers in age, education or Univariate ANOVA on total score obtained during the task, PCL scores (t tests, all p> .100), and no differences in distribu- revealed a significant main effect of PTSS (F(1,93)¼ 5.36, tion of escape vs. non-escape behavior across groups or gen- p¼ .023, partial g ¼ .05); specifically, PTSS participants aver- ders (chi-square tests, all p> .100). The participants who aged 613.8 points (SD 234.2) while noPTSS participants never showed escape hiding never experienced the contin- averaged only 531.0 points (SD 227.5). To examine whether gency that their actions could affect point loss; as such, their the difference in total score might be attributable to other ability to learn an avoidance response is moot and their data performance measures, multiple t tests were conducted. The were excluded from further analysis. Figure 2(B) re-plots aver- difference in locomotion between PTSS and noPTSS groups age escape hiding for the 105 participants who did show fell short of corrected significance (PTSS: M¼ 1111.3, SD escape hiding. 532.8; noPTSS: M¼ 936.4, SD 249.3; t(103)¼ 2.15, p¼ .034, Avoidance hiding also increased over the 12 acquisition partial g ¼ .04). There were no significant differences in total trials (Figure 3(A)), as indicated by a main effect of trial (mixed ANOVA, F(6.76,628.89)¼ 24.60, p< .001, partial shots fired, number of target ships hit or time spent hiding g ¼ .21) with trial PTSS (F(13.53, 628.89)¼ 2.23, p¼ .032, during ITI (all p> .100). partial g ¼ .01) and trial PTSS gender (F(6.76, 628.89)¼ 2.25, p¼ .031, partial g ¼ .02) interactions. The main effect of PTSS also approached significance Post-task questionnaire (F(1,93)¼ 3.84, p¼ .053, partial g ¼.04). To further investigate One participant was not administered the post-task question- the three-way interaction, separate analyses were run in naire due to an experimenter’s error. Among the remaining males vs. females (Figure 3(B,C)). Males showed an effect of 118 participants, self-assessed computer gaming was modest, trial on avoidance hiding (F(5.95,368.59)¼ 57.34, p< .001, par- with only 16 participants reporting that they played games tial g ¼ .48) but no effect of PTSS and no interaction (all “very often” and 34 reporting “sometimes,” with the remain- p> .400). Females also showed an effect of trial on avoidance der reporting “seldom” or “never.” Distribution of these hiding (F(5.89,229.81)¼ 15.16, p< .001, partial g ¼ .28), as responses did not differ as a function of group, gender or well as a main effect of PTSS (F(1,39)¼ 5.49, p¼ .024, partial PTSS status (all p> .100). g ¼ .12) and a trial PTSS interaction (F(5.89,229.81)¼ 2.85, Asked about the purpose of the current game, 59 partici- p¼ .011, partial g ¼ .07). Post hoc independent-samples t pants mentioned something to do with assessing motor skills, tests, with alpha corrected to .0042 to protect significance levels, revealed significant differences between PTSS and eye-hand coordination, or reflexes; 16 mentioned something noPTSS females early in training, specifically on trials 2 to do with testing patience or stress; 15 mentioned some- (Welch’s t(29.3)¼ 3.14, p¼ .004, Cohen’s d¼ 1.01) and 5 thing to do with memory or coordination; 36 stated that the (Welch’s t(38.0)¼ 2.04, p¼ .004, Cohen’s d¼ 0.65). purpose was to gain points or shoot/destroy enemy ships. 290 J. SHEYNIN ET AL. Figure 3. Avoidance hiding (hiding during the warning period). (A) Avoidance hiding increased across trials, and was greater in the PTSS subgroup particularly toward later trials. (B) Males with vs. without PTSS showed similar levels of avoidance hiding, but (C) avoidance hiding was significantly greater in females with PTSS compared to noPTSS females. Asterisks denote significant group differences between PTSS and noPTSS groups. Error bars represent standard error of the mean. “escapers” and 10 of the 14 “non-escapers” responded “yes;” these endorsement rates did not differ significantly between escapers and non-escapers (p¼ .229). Participants were next asked about the purpose of those objects. Of the 103 partici- pants who specified a purpose, 81 mentioned something to do with safety, hiding, or protection; 3 additional participants mentioned “bunkers” or “hangars” without specifically men- tioning the concept of hiding or safety. The remaining 19 participants said they did not know or mentioned a different concept such as “borders” or places for refueling. The con- cept of safety was expressed significantly more often by escapers (78 of 93) than by non-escapers (3 of 10; Yates-cor- rected chi-square, v ¼12.56, df¼ 1, p< .001, Cramer’s V¼ .39); however, there were no differences as a function of gender, group, or PTSS status (all p> .100). Figure 4. Avoidance hiding during the 12 extinction trials. Error bars represent standard error of the mean. Discussion The central finding of the current study was that, while most participants learned an escape response, there were group Only one participant specifically mentioned the concept of differences in how well participants learned an anticipatory learning to avoid or hide from danger. Asked whether they had noticed objects at the lower cor- avoidance response. There was an interaction of trial with ners of the screen (i.e. the safe areas), 91 of the 104 PTSS, indicating that PTSS participants acquired avoidance STRESS 291 faster and to a greater degree than noPTSS participants. This above appeared primarily due to greater avoidance in PTSS result suggests that, while avoidance of reminders of the females compared to noPTSS females, with little difference trauma is a core feature of PTSD, a propensity for avoidance between male groups. To our knowledge, this represents the can be observed even in the context of a fairly innocuous first time that an interaction with gender has been observed computer game. This in turn suggests that avoidance symp- in a behavioral study assessing avoidance in those with PTSS. toms may reflect a general cognitive bias, not limited to This, together with a recent study that found gender differen- learning about trauma or fear. ces in avoidance in opioid addicts (Sheynin et al., 2016), There are several possible factors that could drive a group emphasize the importance of studying gender in mental difference in avoidance. First, it is possible that individuals disorders, and that the course and expression of avoidance with PTSS simply learn faster in general. This would be con- may differ in men and women, which of course could have sistent with prior work that has shown faster learning by indi- important implications for optimizing treatment by patient viduals with PTSS in a computer task where the goal is to gender. earn points and avoid point loss (Myers et al., 2013), although Finally, there was no evidence of differences in avoidance other studies have found no such effects of PTSD or PTSS between veterans and civilians, or between combat-exposed burden on computer-based tasks where the goal is to earn and non-combat exposed veterans. As noted earlier, PTSD points (but there is no threat of point loss; Levy-Gigi et al., risk may be higher in veterans than in civilians, and higher in 2012; Kostek et al., 2014; Anastasides et al., 2015). This idea is combat-exposed than non-exposed veterans, and indeed the also generally consistent with a number of other studies current study also found lower PCL scores in the civilian showing better associative learning in PTSD patients on tasks group than in the two veteran groups, and higher PTSS rates that involve learning to avoid explicitly aversive stimuli, such among combat than non-combat veterans. Despite this, the as mild electric shocks (Blechert et al., 2007; Orr et al., 2000), current study did not find evidence of differences in how airpuffs to the eye (Burriss et al., 2007), trauma-specific pic- avoidance is acquired and expressed among these subgroups. tures (Wessa & Flor, 2007), or loud noise bursts (Peri et al., This might suggest that different life experiences, leading to 2000). However, in the current task, subjects typically first different rates and types of traumatic exposure, might affect learn to escape from punishment (i.e. hiding once the moth- vulnerability to PTSD, without necessarily affecting the course ership starts shooting, to terminate point loss), and then to or expression of avoidance symptoms in those who do avoid punishment altogether (via anticipatory hiding initiated develop the disorder. Obviously, further work should explore during the warning period). Results showed no difference this question further. between PTSS and noPTSS participants in escape responding, Several limitations of the current study raise open ques- nor any difference between participants who did vs. did not tions that could be addressed in future work. First, although learn to escape (escapers vs. non-escapers) in PCL scores. This our study included males and females, as well civilians and indicates that individuals with severe PTSD symptoms were veterans, cell size was imbalanced. Most obviously, there not faster to learn to escape; however, they were significantly was low inclusion of female combat veterans. This is unsur- faster to learn the avoidance response. This in turn appears prising given the demographics of the population of combat to argue against a general facilitation of (all types of) learning veterans; nevertheless, this imbalance doubtless hindered the in the PTSS group, but rather a selective facilitation in learn- ability to investigate interactions between gender and history ing avoidance responses. of exposure to combat. Future studies might redress this Another factor that could drive group differences is vari- issue, particularly as the pool of female combat veterans con- ability in reward and punishment sensitivity. Successful per- tinues to increase. formance on the spaceship task involves balancing the need Second, while the spaceship task was validated in young to hide to avoid punishment, and the need to stay out in the adults, and later tested in opioid-addicted patients (Sheynin open in order to shoot and gain points. Prior computational et al., 2014a, 2014b, 2016), the current work is the first to modeling of behavior in the spaceship task suggests that the report performance on this task in participants with PTSS. performance is modulated by both the absolute sensitivity to In addition, PTSS status was assigned based on PCL scores, punishment, as well as the relative sensitivity to reward and representing symptom self-assessment, rather than a result punishment (Sheynin et al., 2015). of clinical diagnostic status. Prior studies have suggested Finally, it is possible that greater acquisition of avoidance in that PCL scores are highly predictive of clinician-rated PTSD the PTSS group could simply reflect increased motivation to in veterans (Lunney et al., 2014; Weathers et al., 1993). perform well, or better understand the goals of the game, com- Nevertheless, self-report questionnaires are obviously subject pared to the noPTSS group. Consistent with this, the PTSS to limitations including demand characteristics, which can group did acquire more total points, although they did not dif- lead to both underreporting and overreporting of symptoms. fer from noPTSS participants in other performance measures. Additionally, clinical diagnosis includes additional factors such In addition, although the post-task questionnaire is only an as duration and impact on daily life, not directly assessed by indirect measure of understanding, there was no evidence that PCL. Future studies are necessary to further validate the either group could verbalize that the purpose of the game was spaceship task in PTSD, and extend it to clinically diagnosed to assess avoidance learning, nor any evidence that the PTSS patients. group had more familiarity with computer games in general. Additionally, participants in the current study were not The second key finding of the current study was the inter- assessed for, nor excluded based on, presence of comorbid action with gender. In particular, the effect of PTSS discussed disorders such as depression or anxiety, or for the presence 292 J. SHEYNIN ET AL. of psychoactive drugs including antidepressant medication, Funding all of which might differ across groups and contribute to dif- This work was supported by Merit Review Award I01 CX000771 from the ference in learning and behavior. This is particularly salient U. S. Department of Veterans Affairs Clinical Sciences Research and given our prior findings of group-gender interactions among Development Service. opioid-addicted and control participants (Sheynin et al., 2016). Future studies should further examine the effects of References (prescription and illicit) psychoactive drugs, and possible interactions with PTSD, on avoidance learning. However, it is American Psychiatric Association. (2013). Diagnostic and statistical manual important to note that the prior study found a difference of mental disorders. 5th ed. Washington, DC. Anastasides N, Beck KD, Pang KCH, Servatius RJ, Gilbertson MW, Orr SP, between opiate-addicted and never-addicted males, while the Myers CE. (2015). Increased generalization of learned associations is current study found a difference between PTSS and noPTSS related to re-experiencing symptoms in veterans with symptoms of females. Additionally, although depression is often comorbid posttraumatic stress. 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Stable behavioral inhibition avoidance in participants with severe PTSD symptoms, using and its association with anxiety disorder. J Am Acad Child Adolesc Psychiatry 31:103–11. a computer-based task in which the aversive event to be Hoge C, Castro C, Messer S, McGurk D, Cotting D, Koffman R. (2004). avoided was point loss. In particular, PTSS females showed Combat duty in Iraq and Afghanistan, mental health problems, and greater avoidance than noPTSS females. This is, to our know- barriers to care. N Engl J Med 351:13–22. ledge, the first demonstration of such a gender difference in Karamustafalioglu OK, Zohar J, Guveli M, Gal G, Bakim B, Fostick L, avoidance learning in participants with PTSD symptoms. Karamustafalioglu N, Sasson Y. (2006). Natural course of posttraumatic stress disorder: a 20-month prospective study of Turkish earthquake Results suggest first, that avoidance symptoms in PTSD repre- survivors. J Clin Psychiatry 67:882–9. sent a general cognitive bias not limited to learning about Keane TM, Fairbank JA, Caddell JM. (1989). Clinical evaluation of a meas- trauma-related or fear-evoking stimuli, and second, that there ure to assess combat exposure. Psychol Assessment 1:53–5. may be important interactions with gender. A better under- Kessler RC, Berglund P, Demler O, Jin R, Merikangas KR, Walters EE. standing of how acquisition and expression of avoidance is (2005). Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Arch Gen altered in PTSD may provide important insight into the devel- Psychiatry 62:593–602. opment and persistence of pathological behaviors, which in Kessler RC, Sonnega A, Bromet E, Hughes M, Nelson CB. (1995). turn could guide the development of more effective treat- Posttraumatic stress disorder in the National Comorbidity Survey. Arch ments or preventative interventions, and how these might Gen Psychiatry 52:1048–60. differ between male and female patients. Kostek JA, Beck KD, Gilbertson MW, Orr SP, Pang KCH, Servatius RJ, Myers CE. (2014). Acquired equivalence in U. S. veterans with symp- toms of post-traumatic stress: reexperiencing symptoms are associated with better generalization. J Trauma Stress 27:717–20. Levy-Gigi E, Keri S, Myers CE, Lencovsky Z, Sharvit-Benbaji H, Orr SP, Disclosure statement Gilbertson MW, et al. (2012). Individuals with post-traumatic stress dis- The funder played no role in the study design, collection, analysis or order show a selective deficit in generalization of associative learning. interpretation of the data, in the writing of the report, or decision to sub- Neuropsychology 26:758–67. mit the article for publication. 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The PTSD Orr SP, Metzger LJ, Lasko NB, Macklin ML, Peri T, Pitman RK. (2000). De checklist (PCL): Reliability, validity, and diagnostic utility. Paper pre- novo conditioning in trauma-exposed individuals with and without sented at the Annual Meeting of the International Society for posttraumatic stress disorder. J Abnorm Psychol 109:290–8. Traumatic Stress Studies. Peri T, Ben-Shakhar G, Orr SP, Shalev AY. (2000). Psychophysiologic Wessa M, Flor H. (2007). Failure of extinction of fear responses in post- assessment of aversive conditioning in posttraumatic disorder. Biol traumatic stress disorder: evidence from second-order conditioning. Psychiatry 47:512–9. Am J Psychiatry 164:1684–92. Rosenbaum JF, Biederman J, Bolduc-Murphy EA, Faraone SV, Chaloff J, Wolfe J, Erikson DJ, Sharkansky EJ, King DW, King LA. (1999). Course and Hirshfeld DR, Kagan J. (1993). Behavioral inhibition in childhood: a risk predictors of posttraumatic stress disorder among Gulf War veterans: a factor for anxiety disorders. Harv Rev Psychiatry 1:2–16. prospective analysis. J Consult Clin Psychol 67:520–8. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Stress: The International Journal on the Biology of Stress Taylor & Francis

Greater avoidance behavior in individuals with posttraumatic stress disorder symptoms

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STRESS, 2017 VOL. 20, NO. 3, 285–293 http://dx.doi.org/10.1080/10253890.2017.1309523 ORIGINAL RESEARCH REPORT Greater avoidance behavior in individuals with posttraumatic stress disorder symptoms a,b c c c d c,e Jony Sheynin , Christine Shind , Milen Radell , Yasheca Ebanks-Williams , Mark W. Gilbertson , Kevin D. Beck c,e and Catherine E. Myers a b Veterans Affairs Ann Arbor Healthcare System, Ann Arbor, MI, USA; Department of Psychiatry, University of Michigan, Ann Arbor, MI, USA; c d Department of Veterans Affairs, New Jersey Health Care System, East Orange, NJ, USA; Department of Veterans Affairs, Manchester, NH, USA; Department of Pharmacology, Physiology & Neuroscience, New Jersey Medical School, Rutgers University, Newark, NJ, USA ABSTRACT ARTICLE HISTORY Received 19 October 2016 While avoidance is a core symptom of PTSD, little is known about whether individuals with PTSD show Revised 6 February 2017 a general cognitive bias to acquire and express avoidance, in situations not related to trauma or fear. Accepted 8 March 2017 Here, we used a computer-based task to examine operant acquisition and extinction of avoidance in participants with and without severe self-reported PTSD symptoms. A total of 119 participants (77 male, 42 female; 74 veteran, 45 civilian) with symptoms (PTSS; n¼ 63) or with few/no symptoms (noPTSS; KEYWORDS n¼ 56) performed a task, in which they controlled a spaceship and could shoot a target to gain points Avoidance; posttraumatic or hide in “safe areas” to escape or avoid on-screen aversive events. Results show that participants with stress disorder; gender PTSS exhibited more avoidance across trials than noPTSS participants, particularly due to more avoid- differences; computer-based ance behavior in PTSS females compared to noPTSS females. Avoidance behavior decreased across task; assessment tool extinction trials but interactions with PTSS and gender fell short of significance. Overall, PTSD symptoms were associated with propensity to acquire and express avoidance behavior, in both civilians and veter- ans, and even in a cognitive task that does not explicitly involve trauma or fear. This effect was more pronounced in females, highlighting the role of gender differences in PTSD symptomatology. Importantly, this study also demonstrates the potential of an objective assessment of avoidance behav- ior, which could be used to supplement the common but limited self-report tools. Introduction lead to the development of better therapeutic strategies to manage or reduce PTSD symptoms (PTSS), as well as ways to Posttraumatic stress disorder (PTSD) can develop following identify individuals at highest risk for PTSD following trauma exposure to a traumatic event; symptoms include cognitive exposure. and behavioral avoidance of reminders of the trauma Avoidance learning is a complex phenomenon that (American Psychiatric Association, 2013). These avoidant includes both aversively motivated learning and reward learn- behaviors tend to increase over time subsequent to the incipi- ing; the balance between these two processes influences the ent traumatic event (Foa et al., 2006; Karamustafalioglu et al., degree and expression of avoidance (Stein & Paulus, 2009). 2006), and the degree of increased avoidance can differentiate Computer-based tasks, in which participants learn to avoid between those trauma-exposed individuals who develop PTSD on-screen aversive events (such as point loss or destruction and those who recover (Foa et al., 2006; North et al., 2004; of the participant’s avatar), can provide a useful tool to exam- O'Donnell et al., 2007). Lifetime prevalence of PTSD among ine how individuals acquire and express avoidance behavior. adult Americans is estimated at about 6.8% (Kessler et al., In one recent study, male veterans learned to categorize stim- 2005); however, some populations may have much higher risk. uli in order to obtain reward (point gain) and avoid punish- For example, the prevalence of PTSD may be twice as high in ment (point loss); participants with severe PTSD symptoms females as in males (Kessler et al., 2005), while lifetime preva- outperformed those with few/no symptoms (Myers et al., lence among veterans may reach 15–20% (Hoge et al., 2004; 2013). In another computer task, where participants guided Magruder et al., 2016), presumably reflecting stressors such as an on-screen character (avatar) through several scripted scen- deployment, wartime service and exposure to combat arios, such as attending a party or participating in a volunteer (Dohrenwend et al., 2006; Kessler et al., 1995; Wolfe et al., activity, severity of self-assessed PTSD symptoms correlated 1999). Given the prevalence and costs of PTSD, better under- with participants’ tendency to display avoidant behavioral standing of how avoidance is acquired and expressed could patterns (Myers et al., 2016). However, in the first task, CONTACT Catherine E. Myers [email protected] Research Services, VA New Jersey Health Care System, 385 Tremont Avenue, East Orange, NJ 07018, USA 2017 US Government author 286 J. SHEYNIN ET AL. subjects learned to select between predefined alternative flyers and word-of-mouth referral. One participant withdrew responses (categorization), while in the second, subjects did from the testing session before completing the spaceship not receive explicit feedback for their responses. Thus, neither task, and a second participant failed to complete the task task fully examined the manner in which subjects discover due to experimenter’s error. A third participant’s testing ses- and acquire avoidance responses, nor the rate at which these sion was terminated early due to a medical condition (glau- avoidance responses extinguish when there is no longer any coma), which made it difficult for the participant to tolerate threat. viewing the computer screen. Data from these three partici- Recently, we developed and validated a computer-based pants were excluded from analysis, leaving a final set of 119 task in which the participants control an on-screen spaceship participants. Several additional participants had physical chal- and fire at targets to gain points (Sheynin et al., 2014a; lenges (e.g. prosthetic eye or wheelchair-bound); however, these individuals were able to position themselves comfort- Sheynin et al., 2014b). At intervals, a series of on-screen ably to view the computer screen and register their explosions occurs, which damages the participants’ ship and responses, and so they were not excluded from participation. causes accumulating point loss. A warning signal on the One female participant had a history of military service but screen predicts upcoming threat; participants can learn to did not qualify for veterans benefits; her data were included avoid the point loss by hiding their spaceship in response to in the veteran sample. Participants received $40 reimburse- this warning signal. In prior studies with this task, young ment for a single 2-h testing session. All participants signed adults with inhibited temperament, an increased tendency to statements of informed consent at the start of the session. withdraw from or avoid aversive situations, showed more Procedures were approved by the VANJHCS Institutional avoidance behavior than uninhibited peers; there was also an Review Board and conformed to guidelines for the protection effect of gender, with females showing longer avoidance of human subjects established by the Declaration of Helsinki responses than males (Sheynin et al., 2014a). Note that longer and the US Federal Government. avoidance duration (e.g. initiate hiding as soon as the warn- Participants completed a demographic questionnaire that ing signal appeared) was suboptimal; rather, the optimal included questions about gender, age, education and details response was to continue shooting to gain points for as long of military service. When asked to self-identify race, 84 self- as possible, and then hide at the last possible moment to identified as Black/African-American, 18 as White/Caucasian, avoid the upcoming threat. In a follow-up study, females also and 17 as other, Mixed Race or declined to specify. When showed slower extinction, continuing to emit avoidance asked to self-identify ethnicity as Hispanic or non-Hispanic, 5 responses even when the aversive event no longer followed self-identified as Hispanic, 111 self-identified as non-Hispanic the warning signal (Sheynin et al., 2014b). These results are and 3 declined to specify ethnicity. intriguing, since both inhibited temperament (Biederman Participants reporting prior military service (n¼ 74) were et al., 1993; Hirshfeld et al., 1992; Rosenbaum et al., 1993) also administered the Combat Exposure Scale (CES; Keane and female gender (Tolin & Foa, 2006) have been noted as et al., 1989); following prior studies (Ginsberg et al., 2008; risk factors for the development of PTSD following trauma Myers et al., 2012), those scoring below 8 on the CES were exposure. classified as non-combat-exposed (n¼ 47) and the remainder Here, we adapted the spaceship task to examine acquisi- as having a history of exposure to combat (n¼ 27). Asked tion and extinction of avoidance in adults with vs. without about specific conflicts in which they had served, 27 reported severe PTSS. Our prediction was that, since avoidance is a Vietnam, 11 Gulf War/Operation Desert Storm, 10 Operation core feature of PTSD, participants with severe PTSS would Enduring Freedom/Operation Iraqi Freedom, 13 Other (e.g. show greater acquisition, and reduced extinction, compared Beirut, Somalia, Korea, Iraq/Operation Southern Watch), and to those with few/no PTSS. Given high rates of PTSD in 23 reported no specific conflict or peacetime service; veterans, particularly combat-exposed veterans, we included numbers sum to greater than 74 due to some veterans civilians, combat-exposed veterans, and non-combat exposed whose service spanned multiple conflicts. In summary, three veterans in our sample, to determine whether history of subject groups were included: combat-exposed veterans, military service and/or combat exposure affected avoidance non-combat-exposed veterans and civilians (never served in in the task. We were also interested in whether the the military, n¼ 45). Table 1 shows demographic characteris- pattern would be similar among males and females, given tics for each group. data suggesting that females are at higher risk for PTSD All participants also completed the PTSD Checklist-Civilian (Tolin & Foa, 2006) and that the course and expression of version (PCL-C), a 17-item questionnaire that asks about pres- PTSD may be different in females than in males (Olff et al., ence and frequency of PTSS not necessarily military in nature 2007). (Blanchard et al., 1996). PCL scores of 50þ have been shown to predict PTSD in military samples (Blanchard et al., 1996; Methods Weathers et al., 1993); based on this criterion, participants were classified with current severe PTSD symptoms (PTSS), or Participants few/no PTSS (noPTSS). PTSS rates were higher among males (47 of 77) than females (16 of 42; Yates-corrected chi-square, One hundred and twenty-two participants (including 76 vet- v ¼4.86, df¼ 1, p¼ .028, Cramer’s V¼ .22), but did not differ erans and 46 civilians without military experience) were between combat and non-combat groups or between civil- recruited from the Veterans Affairs New Jersey Health Care System (VANJHCS) and surrounding community, by posted ians and either veteran group (all p> .100). STRESS 287 Table 1. Demographic characteristics and questionnaire scores for the three participant groups. Combat-exposed veterans Non-combat exposed veterans Civilians N27 47 45 Gender Two females (7.4%) 10 females (21.3%) 30 females (66.7%) Age (years) 52.2 (SD 11.0) 55.7 (SD 10.6) 47.5 (SD 16.4) Education (years) 15.1 (SD 3.0) 14.6 (SD 1.9) 14.9 (SD 2.4) CES score 17.8 (SD 7.9) 1.8 (SD 2.7) N/A PCL score 57.3 (SD 14.5) 51.0 (SD 16.6) 39.2 (SD 15.6) PTSS cases 21 (77.8%) 28 (59.6%) 31 (68.9%) throughout the subsequent punishment period). In both Spaceship avoidance task cases, if the participant emerged from hiding before the The spaceship avoidance task was a modification of that end of the punishment period, point loss would resume. previously described (Sheynin et al., 2014a, 2014b, 2016); an Importantly, participants were not given any explicit instruc- executable version of the software is available for replication tions about the safe areas or the hiding response. and additional study on the Open Source Framework (OSF) at The task was divided into acquisition and extinction www.osf.io/p78fr. The software was programed in SuperCard phases. The acquisition phase consisted of 12 trials, each version 3.7.1 (Solutions Etcetera, Pollock Pines, CA) and pre- composed of a warning period, a punishment period and ITI, sented on a Macintosh iMac computer. The keyboard was as described earlier. The transition to the extinction phase masked except for three keys labeled FIRE, LEFT and RIGHT, was not signaled to the participant; it consisted of 12 extinc- which the subject could use to enter responses. At the start tion trials which were similar to the acquisition trials except of the experiment, the following instructions appeared: "You that the mothership never fired lasers and point loss never are about to play a game in which you will be piloting a occurred. Prior to the first acquisition trial, participants spaceship. You may use LEFT and RIGHT keys to move your received 1 min of practice time, during which target ships spaceship [picture below], and press the FIRE key to fire appeared and the participant could shoot to gain points. lasers. Your goal is to maximize your total score. The total A running tally at the bottom of the screen showed the cur- score will be displayed at the bottom of the screen. (We’ll rent points accumulated, which was initialized to 325 at the start you off with a few points now.) Good luck!" start of the experiment. In the task, participants controlled a spaceship, and could move it left and right across the bottom of the screen, using the LEFT and RIGHT keys. Target spaceships periodically Post-task questionnaire appeared at one of six locations on the screen for approxi- mately 2 s, and participants could use the FIRE key to shoot After finishing the task, participants completed a paper- at and attempt to destroy these ships; participants gained and-pencil questionnaire asking about experience with one point for every target ship successfully destroyed (Figure computer games, whether participants noticed the different 1(A,B)). Every 20 s, a large “mothership” appeared on the objects that appeared during the task and understood their screen, and remained for a 5 s warning period, during which meaning, along with an open-ended question asking partic- no target ships appeared (Figure 1(C)). The warning period ipants what they thought was the purpose of the task. was followed by a 5 s punishment period, during which the The purpose of these questions was to determine whether mothership would fire lasers at the participant’s ship (Figure differences in computer familiarity or understanding of 1(D)). The punishment period was divided into five 1-s seg- task demands might underlie any group differences in ments; during each segment, there was an explosion of the performance. participant’s ship and a loss of 5 points, up to a maximum of 25 points. The punishment period was followed by a 10 s intertrial interval (ITI) before the onset of the next warning Data analysis period. Every 100 ms, the program recorded whether the participant’s Throughout the experiment, two shelters representing spaceship was inside one of the designated safe areas. For “safe areas” were present at the left and right corners of the each trial, avoidance hiding was defined as the percent of screen. When the participant moved left or right into one of time spent hiding during the 5 s warning period, and escape these areas, the participant’s ship entered the safe area and a hiding was defined as the percent of time spent hiding dur- door closed behind the ship (“hiding”; Figure 1(E)). While ing the subsequent 5 s punishment period. Avoidance and hiding, the participant’s spaceship could not be hit by the escape hiding were scored for the acquisition and extinction mothership’s lasers, and no point loss occurred, but neither phases, even though there was no possibility of punishment could the participant shoot at targets and acquire points during the extinction phase. ITI hiding was defined as the (Figure 1(F)). Hiding during a punishment period was defined percent of time spent hiding during the 10 s ITI between tri- as “escape hiding,” and terminated point loss (for as long as als, averaged separately across the acquisition and extinction the participant remained in hiding, up to the full length of phases. Several additional task variables were scored for each the punishment period). Hiding during the warning period was defined as “avoidance hiding,” and could cause complete participant, including total score at the end of the task, num- omission of point loss (if the participant remained in hiding ber of shots fired (presses on the FIRE key), locomotion 288 J. SHEYNIN ET AL. Figure 1. Screen events during the spaceship avoidance task. (A) The participant’s ship could move from left to right and fire at target ships that appeared at inter- vals; (B) successful “hits” were rewarded with 1 point. (C) During the warning period of each trial, a mothership appeared, and the participant’s lasers were ineffect- ive against it. (D) In the subsequent punishment period, the mothership fired lasers repeatedly, each time exploding the participant’s spaceship and causing a loss of 5 points, to a maximum of 25 points lost. (E) The participant could escape or avoid point loss by hiding in either of the two designated “safe areas” at the sides of the screen; the door slid shut behind the participant, or opened when the participant emerged. (F) While the participant’s ship was hidden, the mothership’s lasers were ineffective (no destruction or point loss). The participant could thus hide during the punishment period to terminate point loss (escape response), or pre- vent point loss all together by hiding during the warning period and remaining hidden throughout the subsequent punishment period (avoidance response). (presses on the LEFT or RIGHT keys) and total targets shot on a 2 2 table, Yates Continuity Correction was applied (equivalent to points gained) across the task. to adjust expected values. Where data failed assumptions Statistical analyses were conducted using IBM SPSS version of equality of variance/sphericity, appropriate corrections were used (Greenhouse-Geisser for ANOVA, Welch’s t for 22. Primary analyses for hiding performance were mixed t test) to correct degrees of freedom. The threshold for sig- ANOVA with and within-subjects factors of trial, or univariate nificance was set at .05; effects that did not approach ANOVA (for other task variables), with factors of group significance (p> .100) were generally not discussed. Where (civilian, non-combat veteran, combat veteran), gender and multiple tests were conducted, Bonferroni’s correction was PTSS status (PTSS, noPTSS). Significant results were followed used to protect against inflated risk of family-wise type-I up as appropriate by post hoc tests. Chi-square test was error. used for comparison of distributions. For chi-square tests STRESS 289 Figure 2. Escape hiding (hiding during punishment period) across the 12 acquisition trials for (A) all n¼ 119 participants, (B) n¼ 105 excluding 14 non-escapers. Error bars represent standard error of the mean. Avoidance hiding decreased across extinction trials Results (Figure 4; F(7.15,665.00)¼ 3.77, p< .001, partial g ¼ .04) with Escape/avoidance behavior no effect of group, gender, or PTSS, although both the Escape hiding increased over the 12 acquisition trials trial PTSS group interaction and the trial PTSS group (Figure 2), as indicated by a main effect of trial (mixed gender interaction approached significance (both .05< ANOVA, F(4.80, 513.44)¼ 13.54, p< .001, partial g ¼ 0.11) p< .100). with no effects of group or gender and no interactions (all p> .090). A subset of 14 participants (11.8%) showed no escape hiding during the experiment. There were no differen- Other performance measures ces between escapers and non-escapers in age, education or Univariate ANOVA on total score obtained during the task, PCL scores (t tests, all p> .100), and no differences in distribu- revealed a significant main effect of PTSS (F(1,93)¼ 5.36, tion of escape vs. non-escape behavior across groups or gen- p¼ .023, partial g ¼ .05); specifically, PTSS participants aver- ders (chi-square tests, all p> .100). The participants who aged 613.8 points (SD 234.2) while noPTSS participants never showed escape hiding never experienced the contin- averaged only 531.0 points (SD 227.5). To examine whether gency that their actions could affect point loss; as such, their the difference in total score might be attributable to other ability to learn an avoidance response is moot and their data performance measures, multiple t tests were conducted. The were excluded from further analysis. Figure 2(B) re-plots aver- difference in locomotion between PTSS and noPTSS groups age escape hiding for the 105 participants who did show fell short of corrected significance (PTSS: M¼ 1111.3, SD escape hiding. 532.8; noPTSS: M¼ 936.4, SD 249.3; t(103)¼ 2.15, p¼ .034, Avoidance hiding also increased over the 12 acquisition partial g ¼ .04). There were no significant differences in total trials (Figure 3(A)), as indicated by a main effect of trial (mixed ANOVA, F(6.76,628.89)¼ 24.60, p< .001, partial shots fired, number of target ships hit or time spent hiding g ¼ .21) with trial PTSS (F(13.53, 628.89)¼ 2.23, p¼ .032, during ITI (all p> .100). partial g ¼ .01) and trial PTSS gender (F(6.76, 628.89)¼ 2.25, p¼ .031, partial g ¼ .02) interactions. The main effect of PTSS also approached significance Post-task questionnaire (F(1,93)¼ 3.84, p¼ .053, partial g ¼.04). To further investigate One participant was not administered the post-task question- the three-way interaction, separate analyses were run in naire due to an experimenter’s error. Among the remaining males vs. females (Figure 3(B,C)). Males showed an effect of 118 participants, self-assessed computer gaming was modest, trial on avoidance hiding (F(5.95,368.59)¼ 57.34, p< .001, par- with only 16 participants reporting that they played games tial g ¼ .48) but no effect of PTSS and no interaction (all “very often” and 34 reporting “sometimes,” with the remain- p> .400). Females also showed an effect of trial on avoidance der reporting “seldom” or “never.” Distribution of these hiding (F(5.89,229.81)¼ 15.16, p< .001, partial g ¼ .28), as responses did not differ as a function of group, gender or well as a main effect of PTSS (F(1,39)¼ 5.49, p¼ .024, partial PTSS status (all p> .100). g ¼ .12) and a trial PTSS interaction (F(5.89,229.81)¼ 2.85, Asked about the purpose of the current game, 59 partici- p¼ .011, partial g ¼ .07). Post hoc independent-samples t pants mentioned something to do with assessing motor skills, tests, with alpha corrected to .0042 to protect significance levels, revealed significant differences between PTSS and eye-hand coordination, or reflexes; 16 mentioned something noPTSS females early in training, specifically on trials 2 to do with testing patience or stress; 15 mentioned some- (Welch’s t(29.3)¼ 3.14, p¼ .004, Cohen’s d¼ 1.01) and 5 thing to do with memory or coordination; 36 stated that the (Welch’s t(38.0)¼ 2.04, p¼ .004, Cohen’s d¼ 0.65). purpose was to gain points or shoot/destroy enemy ships. 290 J. SHEYNIN ET AL. Figure 3. Avoidance hiding (hiding during the warning period). (A) Avoidance hiding increased across trials, and was greater in the PTSS subgroup particularly toward later trials. (B) Males with vs. without PTSS showed similar levels of avoidance hiding, but (C) avoidance hiding was significantly greater in females with PTSS compared to noPTSS females. Asterisks denote significant group differences between PTSS and noPTSS groups. Error bars represent standard error of the mean. “escapers” and 10 of the 14 “non-escapers” responded “yes;” these endorsement rates did not differ significantly between escapers and non-escapers (p¼ .229). Participants were next asked about the purpose of those objects. Of the 103 partici- pants who specified a purpose, 81 mentioned something to do with safety, hiding, or protection; 3 additional participants mentioned “bunkers” or “hangars” without specifically men- tioning the concept of hiding or safety. The remaining 19 participants said they did not know or mentioned a different concept such as “borders” or places for refueling. The con- cept of safety was expressed significantly more often by escapers (78 of 93) than by non-escapers (3 of 10; Yates-cor- rected chi-square, v ¼12.56, df¼ 1, p< .001, Cramer’s V¼ .39); however, there were no differences as a function of gender, group, or PTSS status (all p> .100). Figure 4. Avoidance hiding during the 12 extinction trials. Error bars represent standard error of the mean. Discussion The central finding of the current study was that, while most participants learned an escape response, there were group Only one participant specifically mentioned the concept of differences in how well participants learned an anticipatory learning to avoid or hide from danger. Asked whether they had noticed objects at the lower cor- avoidance response. There was an interaction of trial with ners of the screen (i.e. the safe areas), 91 of the 104 PTSS, indicating that PTSS participants acquired avoidance STRESS 291 faster and to a greater degree than noPTSS participants. This above appeared primarily due to greater avoidance in PTSS result suggests that, while avoidance of reminders of the females compared to noPTSS females, with little difference trauma is a core feature of PTSD, a propensity for avoidance between male groups. To our knowledge, this represents the can be observed even in the context of a fairly innocuous first time that an interaction with gender has been observed computer game. This in turn suggests that avoidance symp- in a behavioral study assessing avoidance in those with PTSS. toms may reflect a general cognitive bias, not limited to This, together with a recent study that found gender differen- learning about trauma or fear. ces in avoidance in opioid addicts (Sheynin et al., 2016), There are several possible factors that could drive a group emphasize the importance of studying gender in mental difference in avoidance. First, it is possible that individuals disorders, and that the course and expression of avoidance with PTSS simply learn faster in general. This would be con- may differ in men and women, which of course could have sistent with prior work that has shown faster learning by indi- important implications for optimizing treatment by patient viduals with PTSS in a computer task where the goal is to gender. earn points and avoid point loss (Myers et al., 2013), although Finally, there was no evidence of differences in avoidance other studies have found no such effects of PTSD or PTSS between veterans and civilians, or between combat-exposed burden on computer-based tasks where the goal is to earn and non-combat exposed veterans. As noted earlier, PTSD points (but there is no threat of point loss; Levy-Gigi et al., risk may be higher in veterans than in civilians, and higher in 2012; Kostek et al., 2014; Anastasides et al., 2015). This idea is combat-exposed than non-exposed veterans, and indeed the also generally consistent with a number of other studies current study also found lower PCL scores in the civilian showing better associative learning in PTSD patients on tasks group than in the two veteran groups, and higher PTSS rates that involve learning to avoid explicitly aversive stimuli, such among combat than non-combat veterans. Despite this, the as mild electric shocks (Blechert et al., 2007; Orr et al., 2000), current study did not find evidence of differences in how airpuffs to the eye (Burriss et al., 2007), trauma-specific pic- avoidance is acquired and expressed among these subgroups. tures (Wessa & Flor, 2007), or loud noise bursts (Peri et al., This might suggest that different life experiences, leading to 2000). However, in the current task, subjects typically first different rates and types of traumatic exposure, might affect learn to escape from punishment (i.e. hiding once the moth- vulnerability to PTSD, without necessarily affecting the course ership starts shooting, to terminate point loss), and then to or expression of avoidance symptoms in those who do avoid punishment altogether (via anticipatory hiding initiated develop the disorder. Obviously, further work should explore during the warning period). Results showed no difference this question further. between PTSS and noPTSS participants in escape responding, Several limitations of the current study raise open ques- nor any difference between participants who did vs. did not tions that could be addressed in future work. First, although learn to escape (escapers vs. non-escapers) in PCL scores. This our study included males and females, as well civilians and indicates that individuals with severe PTSD symptoms were veterans, cell size was imbalanced. Most obviously, there not faster to learn to escape; however, they were significantly was low inclusion of female combat veterans. This is unsur- faster to learn the avoidance response. This in turn appears prising given the demographics of the population of combat to argue against a general facilitation of (all types of) learning veterans; nevertheless, this imbalance doubtless hindered the in the PTSS group, but rather a selective facilitation in learn- ability to investigate interactions between gender and history ing avoidance responses. of exposure to combat. Future studies might redress this Another factor that could drive group differences is vari- issue, particularly as the pool of female combat veterans con- ability in reward and punishment sensitivity. Successful per- tinues to increase. formance on the spaceship task involves balancing the need Second, while the spaceship task was validated in young to hide to avoid punishment, and the need to stay out in the adults, and later tested in opioid-addicted patients (Sheynin open in order to shoot and gain points. Prior computational et al., 2014a, 2014b, 2016), the current work is the first to modeling of behavior in the spaceship task suggests that the report performance on this task in participants with PTSS. performance is modulated by both the absolute sensitivity to In addition, PTSS status was assigned based on PCL scores, punishment, as well as the relative sensitivity to reward and representing symptom self-assessment, rather than a result punishment (Sheynin et al., 2015). of clinical diagnostic status. Prior studies have suggested Finally, it is possible that greater acquisition of avoidance in that PCL scores are highly predictive of clinician-rated PTSD the PTSS group could simply reflect increased motivation to in veterans (Lunney et al., 2014; Weathers et al., 1993). perform well, or better understand the goals of the game, com- Nevertheless, self-report questionnaires are obviously subject pared to the noPTSS group. Consistent with this, the PTSS to limitations including demand characteristics, which can group did acquire more total points, although they did not dif- lead to both underreporting and overreporting of symptoms. fer from noPTSS participants in other performance measures. Additionally, clinical diagnosis includes additional factors such In addition, although the post-task questionnaire is only an as duration and impact on daily life, not directly assessed by indirect measure of understanding, there was no evidence that PCL. Future studies are necessary to further validate the either group could verbalize that the purpose of the game was spaceship task in PTSD, and extend it to clinically diagnosed to assess avoidance learning, nor any evidence that the PTSS patients. group had more familiarity with computer games in general. Additionally, participants in the current study were not The second key finding of the current study was the inter- assessed for, nor excluded based on, presence of comorbid action with gender. In particular, the effect of PTSS discussed disorders such as depression or anxiety, or for the presence 292 J. SHEYNIN ET AL. of psychoactive drugs including antidepressant medication, Funding all of which might differ across groups and contribute to dif- This work was supported by Merit Review Award I01 CX000771 from the ference in learning and behavior. This is particularly salient U. S. 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Journal

Stress: The International Journal on the Biology of Stress – Taylor & Francis

Published: May 4, 2017

Keywords: Avoidance; posttraumatic stress disorder; gender differences; computer-based task; assessment tool

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