Physiological emotional under-arousal in individuals with mild head injury.

http://informahealthcare.com/bij ISSN: 0269-9052 (print), 1362-301X (electronic) Brain Inj, 2014; 28(1): 51–65 ! 2014 Informa UK Ltd. DOI: 10.3109/02699052.2013.857787

ORIGINAL ARTICLE

Physiological emotional under-arousal in individuals with mild head injury Julie M. Baker1 and Dawn E. Good1,2 1

Neuropsychology Cognitive Research Laboratory, Department of Psychology and 2Centre for Neuroscience, Brock University, St. Catharines, Ontario, Canada Abstract

Keywords

Primary objectives: This study examined the potential emotional sequelae following selfreported mild head injury (MHI; e.g. ‘altered state of consciousness’ [ASC]) in university students with a particular focus on arousal status and responsivity to experimental manipulation of arousal. Research design: A quasi-experimental design (n ¼ 91) was used to examine arousal status (self-reported and physiological indices) and response to manipulated arousal (i.e. induced psychosocial stress/activation; reduced activation/relaxation) between persons who acknowledged prior MHI and persons with no-MHI. Main outcome and results: University students who self-reported MHI were physiologically under-aroused and less responsive to stressors (both laboratory and environmental) compared to their no-MHI cohort. Those with reported loss of consciousness demonstrated the most attenuated emotional arousal responses (i.e. flattened electrodermal responsivity) relative to those with only a reported ASC, followed by those with no-MHI. Conclusions: The under-arousal in traumatic brain injury has been hypothesized to be associated with ventromedial prefrontal cortex disruption. This under-arousal may be mirrored in persons who self-report experiencing subtle head trauma. Students who reported MHI may be less able to physiologically respond and/or cognitively appraise stressful experiences as compared to their no-MHI cohort; and experience subtle persistent consequences despite the subtle nature of the reported head trauma.

arousal, electrodermal activity, mild head injury, stress

Head injuries are common in prevalence and are a prominent concern [1]. Sources report that 75–80% of all head injuries are classified as mild [1–3], with accidental falls, motor vehicle collisions and sports activities being among the leading causes [4–7]. Moreover, many mild head injuries (MHI) do not result in hospital visits or admissions and typically go unreported [8, 9]. As such, the incidence of milder head trauma is greatly under-estimated. These considerations suggest that the prevalence and outcomes following mild head trauma may be better examined via retrospective reports rather than clinical case study selection. However, there are possible biases or inaccuracies with retrospective reports of head trauma [9–11] and clinical case study selection may be a more reliable method of obtaining head injury information [12]. Regardless of the method of obtaining this information, many young adults and adolescents experience head trauma [1–6]. For example, a recent survey

Correspondence: Julie Baker, PhD Candidate, Psychology Department, Neuropsychology Cognitive Research Lab, Brock University, 500 Glenridge Avenue, St. Catharines, Ontario, L2S 3A1, Canada. Tel: 905-688-5550 x3034. Fax: 905-688-6922. Email: [email protected]

Received 5 November 2012 Revised 22 August 2013 Accepted 17 October 2013 Published online 11 December 2013

of High School students illustrated that 20% self-reported a head trauma incident at some point in their lifetime [10]. As well, even many university students acknowledge a prior head trauma, with 80% of these reports classified as mild [11]. It is well documented that trauma to the head may result in changes in cognition, emotion and physical presentations [13, 14], especially with moderate or severe traumatic brain injury (TBI). Although the severity of head trauma and/or neural disruption may be viewed on a continuum [2, 15] ranging from mild-to-severe (MHI, concussion, post-concussive syndrome [PCS], MTBI, moderate-to-severe brain injury), the persistence of these changes for injuries at the milder end of the continuum of severity of injury has long been controversial and at times is still poorly understood [16–21]. Most often the research has suggested that symptoms following milder head traumas are most often resolved by 3 months [22, 23]; however, there has been accumulating evidence to suggest that complaints or impairments following MHI or MTBI may not be transient for a sub-population of persons. Subtle neuropsychological deficits (e.g. memory, attention, processing speed, etc.) and head injury-related impairments including emotional, behavioural, and occupational difficulties may persist in a sub-group of persons who have sustained subtle, but significant, trauma to the head [17, 23–30].

20 13

Introduction

History

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J. M. Baker and D. E. Good

Similarly, disturbances in emotional responding have been documented [31–33] in patients with moderate-to-severe TBI, especially for those with disruption to the ventromedial prefrontal cortex (VMPFC) [34]. These changes in emotional functioning include deficits in emotion recognition ability [35], decreased emotional reactivity post-injury [36, 37] and impaired socioemotional functioning [38] and may be captured in the umbrella terms of hyperarousal (e.g. increased emotional reactivity; increased prevalence of anxiety disorders [39]) or hypoarousal (e.g. apathy; attenuated emotional responding/flattened affect; increased prevalence of depressive disorders [34, 37, 40]). As well, persons with TBI report increased experiences of life stressors [41]. Although much research has demonstrated that persons with TBI are often emotionally labile and/or demonstrate reduced capacity for emotional experiences [36, 37, 42], emotional functioning following milder head trauma has not been explored to the same extent [32, 43–45], especially with respect to physiological indices of emotional arousal. The research regarding changes in emotional functioning following mild head trauma has been inconclusive. For example, a meta-analysis found small or minimal effects on emotional functioning following mild TBI [46]. However, other research [45, 47] has shown significant changes in emotional functioning in terms of increased anxiety [48] or depressive episodes [47] following mild TBI. Therefore, similar to persons with moderate/ severe TBI [41, 49–51], it is possible that altered emotional functioning may be associated with even mild head trauma, especially if head trauma is considered on a continuum of severity of injury [2, 15]. The findings have been variable [45, 46], but may mirror that of persons with moderate or severe TBI [52–54]. Of particular interest, studies of persons with moderateto-severe disruption to the VMPFC have demonstrated significantly attenuated emotional arousal, as indicated by electrodermal activity (EDA) [34, 55, 56], an index of sympathetic nervous system activation [57]. Sympathetic activation has been closely linked to emotional processes [56, 58, 59]. EDA is a widely used and sensitive, objective index of emotional arousal [57–59]. Therefore, persons with disruption to the VMPFC may have altered emotional arousal [56]. The VMPFC is vulnerable to damage due to its close proximity to the bony protrusions of the skull and, in particular, axonal disruption [13, 60] can result in altered communication with the brainstem, hypothalamus and amygdala [61, 62]. Disrupted communication between prefrontal and sub-cortical regions involved in emotional arousal and emotional processing are suggested to impact behaviour [56, 59, 63, 64]. For example, the somatic marker hypothesis [63, 64] provides a model of poor decision-making which is hypothesized to be a function of disrupted physiological/ visceral feedback following VMPFC injury. Based on their finding that patients with bilateral VMPFC disruption have reduced EDA to stimuli with an emotional component [63, 64], Damasio et al. [63, 64] suggest that persons with VMPFC disruption have attenuated responses to emotionallycharged stimuli. Similarly, Hopkins et al. [37] found that persons with closed head injury demonstrated hypo-responsivity in EDA to negative emotional stimuli (i.e. facial expressions). Extending Damasio et al.’s [63, 64] theory, it is

Brain Inj, 2014; 28(1): 51–65

plausible that persons with MHI, like those with severe neural disruption, may also experience a reduction in arousal and affective status which could be related to lessened feedback involving ‘emotional’ somatic markers to or from the OFC/VMPFC. Lastly, it is possible that persons with MHI may demonstrate altered responses to emotional stressors [33, 56]. Physiological indices of emotional arousal, such as EDA, have been shown to attenuate to stimuli with an emotional component for persons with moderate or severe disruption to the brain [37, 63, 64], however, to the authors’ knowledge, limited, if any, research has examined if differential emotional arousal may be related to a history of self-reported mild head trauma. The research has been silent with respect to arousal levels of persons with MHI and their responses to emotional events such as stressors. As such, across several studies this study tried to determine whether persons with self-reported MHI (i.e. sufficient to produce an ‘altered state of consciousness’; dizzy, dazed or confused [66]), similar to persons with moderate or severe TBI, present with altered emotional arousal and its potential impact on their cognitive and psychosocial functioning. Studies conducted by the Brock University Neuropsychology Cognitive Research (NCR) Lab [67, 68] have examined the emotional arousal status of university students with self-reported MHI and its relation to cognitive performance. Notably, this research was based on the Yerkes-Dodson Law [69], in that performance is enhanced by arousal until an optimum level is reached, then performance decreases again, forming the ubiquitous inverted-U shaped relationship (see Lupien et al. [70] for review). One study [67] investigated the effects of induced psychosocial stress on cognitive performance (attention, working memory) in university students with and without self-reported MHI. Psychological stress was induced by having participants prepare and present a speech while being videotaped (i.e. modified Trier Social Stress Test [TSST] procedure [71]). The results indicated that students with MHI were under-aroused both physiologically (i.e. lower heart rate and blood pressure) and affectively (i.e. lower levels of anxiety via standardized self-report; State-Trait Anxiety Inventory, STAI [72]) prior to, and after, the implementation of the psychosocial stressor. As expected [69, 70], for students with no reported MHI, excessive stress was related to impaired attentional performance (Colour Word Naming Interference Task [73]); whereas, increases in stress/arousal was related to improved performance for students who reported previous MHI. A consecutive study [68] examined self-reported anxiety (STAI [72]), as a measure of arousal and its relation to memory performance in university students with and without self-reported MHI. Overall, students with self-reported MHI acknowledged significantly lower levels of state anxiety than students without MHI. Further, there was a significant interaction of state anxiety with self-reported history of head trauma on memory performance (Logical Memory I and II [74]; Rey Complex Figure test [75]). Students with no previous self-reported history of MHI and higher levels of self-reported anxiety performed more poorly on memory tasks and performance improved when anxiety was reported

Emotional under-arousal

DOI: 10.3109/02699052.2013.857787

to be lower. In contrast, students who acknowledged sustaining MHI demonstrated improved memory performance with higher self-reported anxiety and performed more poorly when less anxious. In summary, the research from this lab [67, 68] has shown that university students with self-reported MHI may be relatively under-aroused compared to students with no history of head trauma and that they may be less responsive to stressors in their environment as compared to students who do not report a history of head trauma. Therefore, the current study was designed to validate the relationships between emotional arousal and self-reported MHI. This study investigated whether persons with selfreported MHI present, both physiologically and via selfreport, in a manner similar to that of persons who have experienced extensive disruption to the VMPFC with respect to emotional arousal. It was expected that persons who have self-reported history of MHI would elicit attenuated physiological and self-reported indices of emotional arousal (i.e. EDA [58, 59]) as a function of variations in manipulated arousal (i.e. induced-stress/heightened arousal or inducedrelaxation/lowered arousal) relative to persons who did not report a history of head trauma.

Hypotheses Hypothesis 1: University students who reported a history of MHI were expected to be under-aroused physiologically and affectively compared to those without head injury, despite experiencing significantly more life stressors. Hypothesis 2: Due to the expected overall reduced underarousal of persons with MHI, it was predicted that responsivity to the arousal manipulations (psychosocial stress or relaxation) would be relatively greater for persons who did not report prior head trauma. Hypothesis 3: Consistent with the Yerkes-Dodson Law [69], induced-psychosocial stress (i.e. heightened arousal) was expected to hinder cognitive performance in persons without self-reported head injury and, in contrast, inducedpsychosocial stress may facilitate cognitive abilities for persons with MHI who were expected to initially, and typically, be under-aroused relative to their cohorts. Conversely, cognitive skills would benefit from inducedrelaxation for individuals without head injury and impair performance for persons with head injury.

Method Participants Ninety-one post-secondary students (Mage ¼ 21 years, SD ¼ 3.20; 28 male, 63 female) were recruited to participate in a ‘Cognitive Abilities and Arousal State Study’ via the local Psychology Department Research Website (SONA) and through poster advertisements. It is important to note that participants were not recruited based on a history of head injury, to avoid the impact of diagnosis threat on cognitive performance [76, 77]. The self-reported head injury history questions were embedded within multiple health-related questions in the demographic questionnaire [78].

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Table I. Indicators of severity for self-reported mild head injuries.

Mean age at injury, years Mean years since injury Concussion Received medical treatment Stitches Overnight stay at medical facility Altered state of consciousness Loss of consciousness 5 5 minutes 5 30 minutes

n

SD

16.01 5.01 24 20 7 5 36 15a 14 1

5.43 5.72

%

47.10 39.20 13.70 9.80 70.59 29.40 93.33 6.67

Notes: n ¼ 51 (56%) Missing 5.9% of responses (n ¼ 3) regarding loss of consciousness.

a

Fifty-one students (56%)1 self-identified as having previously experienced a head injury ‘sufficient to alter their state of consciousness’ (e.g. ‘feeling dizzy, dazed or confused’; criteria similar to that of Kay et al. [66]) occurring, most commonly, 2 years ago at 16 years of age. The majority acknowledged only an altered state of consciousness (ASC) and no loss of consciousness (LOC) associated with the injury. Further, a minority noted seeking/receiving medical treatment for their head trauma (refer to Table I). Students most commonly reported sports-related injuries and falls as the cause of injury (refer to Table II). The MHIs were all within the American Congress of Rehabilitation Medicine Mild Traumatic Brain Injury Committee’s criteria for MTBI [66], were of Grade II Concussion or less [82] and are to be considered ‘mild’ with respect to the severity of injury. Reference to the MHI group throughout this paper includes students who acknowledged (at least) an altered state of consciousness (i.e. dizzy, dazed or confused) and/or a loss of consciousness associated with the head trauma event unless otherwise noted. Measures Self-report measures Everyday Living Demographic Questionnaire. This questionnaire [78] collects a variety of demographic information such as sex, age, level of education, lifestyle factors (e.g. exercise and sleep habits), and multiple health-related items. Embedded within these items are inquiries regarding a history of head trauma (i.e. ‘have you ever sustained trauma to the head that was sufficient to produce an altered state of consciousness [ASC]? e.g. feeling dazed, dizzy or confused’). Those who self-reported a history of head trauma provided information regarding the nature of the head injury. Life Stressors Scale. This measure was adapted from the Social Readjustment Rating Scale [83]. Participants were asked to endorse which of 18 events (e.g. relationship difficulties, illness of someone close or loss of job) that had occurred in the past 6 months. Total score was derived by summing the weighted items to reflect the relative amount of exposure to life stressors. Self-report of arousal state. Each participant was asked to provide a self-report of his/her perceived arousal state (1 ¼ very relaxed to 10 ¼ very stressed) prior to,

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Brain Inj, 2014; 28(1): 51–65

Table 2. Self-reported aetiology of mild head injuries. Aetiology of MHI

n

%

Sport-related injury Falling Overhead impact from object in household (e.g. refrigerator door, bookshelf falling) Other (e.g. fights)

30 14 3

58.82 27.45 5.88

4

7.84

after arousal manipulation induction and at various times throughout the testing session. Neuropsychological measures Select neuropsychological sub-tests were administered to provide estimates of intelligence, indices of working memory, attention/inhibitory control and processing speed [24, 84]. Estimate of general intellectual function (sub-tests of WAIS-III [85]). To verify the students’ capacity, an abbreviated measure of ability was given using the Vocabulary and Block Design sub-tests of the WAIS-III. Participants were asked to provide definitions to words that increased in difficulty across trials to assess ‘verbal’ intelligence. For the ‘non-verbal’ measure of intelligence, participants were asked to reproduce visually presented designs using specially designed blocks to assess visuospatial ability. Total accuracy was recorded. Digit Symbol-Coding (WAIS-III [85]). Participants were asked to replicate geometric symbols that were paired with a number (1–9) as quickly and as accurately as possible in 120 seconds. Total accuracy was the primary measure and provides an index of working memory ability. Trail Making Test (DKEFS [73]). Participants were asked to use a pencil to connect dots that were randomly and spatially arranged by following numbers or letters or alternating numbers and letters as quickly and as accurately as possible. Both accuracy and response time measures were recorded and provide an index of attention, sequencing and cognitive flexibility abilities. Colour-Word Naming Interference Test (DKEFS [73]). Participants completed a modified ‘Stroop’ task [86] as measures of selective attention, cognitive flexibility and impulse control/inhibition. Participants were required to: (1) name colours, (2) read words, (3) name the colour of the ink the word was printed in and (4) switch between reading and colour-naming and to do so as quickly and as accurately as possible. Response time is the primary measure for this sub-test. Physiological measures Electrodermal activity. EDA was used as a measure of emotional arousal due to its sensitivity in detecting changes in sympathetic nervous system activation, particularly eccrine sweat gland activity [57, 58]. EDA was recorded in the traditional continuous voltage method described in detail elsewhere [87, 88] via silver–silver chloride plated pads placed on the distal phalynx of the index and fourth fingers of the non-dominant hand.

EDA data were sampled and averaged. Electrodermal responses were measured in terms of amplitude (i.e. the magnitude of the electrodermal response measured in microsiemens [mS]). EDA was recorded in real time via Polygraph Professional equipment [89] using the Datapac USBÔ 16-bit Data Acquisition Instrument for collection and amplification of the channels in concert with Polygraph Professional Suite Software and a 16’’Acer Laptop computer. All data were carefully screened for artifact prior to analysis. Arousal manipulations Participants were randomly assigned to one of two arousal manipulation conditions: (a) activation—via psychosocial stress (using a modified version of TSST [71] derived from [90]) or (b) relaxation (using guided imagery and breathing techniques from the McMaster Guided Imagery Compact Disc [91]). For the stress condition, each participant completed a verbal mathematical subtraction task consisting of five trials (each with a different 4-digit starting number) and was told that his/her competence was being evaluated by a third party observer through a one-way mirror (in reality, however, no one was observing the student’s performance; subjects were debriefed at the end of the experiment as to this misinformation). Every time the participant made an error s/he was asked to start the sequence again from the last correct number. The purpose was to induce psychological stress that mirrored, and is consistent with, the type of stress (presumably less) students would typically experience in their university life (e.g. assignments, examinations, etc.). For the relaxation condition, participants engaged in relaxing breathing techniques accompanied by guided imagery [91] and restful sounds of the ocean, aromatherapy (diffused lavender oil) and dimmed lighting. Both the stress and relaxation inductions took 9 minutes to complete. Procedures This research was conducted at the Lifespan Development Research Center at Brock University, Ontario, Canada. Study protocol received clearance from the institutional Research Ethics Board (#08-236). Subjects were tested individually in a 2.5-hour session and provided informed consent prior to participation. Finger electrodes were applied and EDA was recorded across the session. Arousal state was assessed at seven different intervals across the testing session (initial [baseline], pre-manipulation, during arousal induction [either stress-induction or relaxation depending on experimental condition] as a manipulation check, immediately after experimental arousal induction, 15, 30 and 45 minutes postmanipulation). Note that the baseline physiological recording period lasted 3 minutes and all subsequent recordings were for a period of 2 minutes, except during the arousal manipulation induction for which data was recorded throughout as a manipulation check. Participants also completed pre- and post-arousal manipulation neuropsychological testing blocks with sub-tests from the WAIS-III [85] and DKEFS [73]. All participants completed the self-report measures described above. Participants were debriefed as to the purpose of the study and were only then informed that head injury was a


DOI: 10.3109/02699052.2013.857787

variable of interest in the study. The experimenter was blind to the participant’s history of head trauma. Participants did not receive an honorarium for participation in this study, but were offered the opportunity to receive credit for research participation hours towards applicable courses at the university. Data analyses Data analyses were conducted via Statistical Package for the Social Sciences (SPSS Version 16.0 [92]). Note physiological data averages were computed via Polygraph Professional software [89]. Assumptions for all statistical analyses were examined and are commented on with respect to any violation. Analyses are considered to be significant if p 0.05, however, trends approaching statistical significance are also discussed. Greenhouse-Geisser correction is denoted G-G . While there was more representation of males in the MHI group2, 2 (1, n ¼ 91) ¼ 3.89, p ¼ 0.049, sex was entered as a covariate for all analyses and was not found to impact the results; as such, the results presented here are not adjusted for sex. This study examined the possibility that some persons with self-reported mild head trauma may indeed have ‘minor’ injuries, whereas others may have comparatively more significant ones (e.g. reported loss of consciousness). Therefore, these data were explored for three groups based on self-report of head injury: no-MHI, MHI-with-ASC and MHI-with-LOC. The relationship was examined between changes in physiological arousal (as indicated by EDA response) across time as a function of exposure to the arousal manipulations for persons with varying degrees of head injury severity. Due to the small sample size (n ¼ 14) of students who reported an MHI-with-LOC and the unbalanced distribution of subjects in the design across the arousal manipulations (no-MHI Relaxation group n ¼ 22, Stress group n ¼ 18; MHI-with-ASC Relaxation group n ¼ 18, Stress group n ¼ 19; MHI-with-LOC Relaxation group n ¼ 6; Stress group n ¼ 8), all analyses were conducted on the MHI/no-MHI groups unless otherwise noted.

Results Demographic information across MHI history groups Representation across MHI groups and arousal manipulation Although the experimenter was blind to the students’ history of self-reported head trauma at the time of random assignment, those reporting MHI were not differentially represented in the psychosocial stress and relaxation manipulation conditions: (a) stress MHI (n ¼ 27); (b) relaxation MHI (n ¼ 24); (c) stress no-MHI (n ¼ 18); and (d) relaxation no-MHI (n ¼ 22), 2 (1, n ¼ 91) ¼ 0.57, p ¼ 0.452.

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sleep and their ratings of sleep quality the night prior to participating in the testing session were not found to be differentially represented for self-reported MHI history and arousal manipulation condition; nor did self-reported MHI history differentially predict sleep quality ratings or alertness. Students’ ratings of their experiences prior to the testing session did not differ between those who reported a history of mild head trauma and those who did not report head trauma with respect to the occurrence of unusual events and how busy or pleasant their day had been. Mental health and neurological condition self-reported history Reported diagnoses of a psychiatric or neurological condition was not differentially represented across self-reported MHI status or arousal manipulation conditions, 2 p ¼ 0.452. Note the percentage of students’ reports of psychiatric history in the total sample is 12.10% (n ¼ 11), which is similar to and less than reports of prevalence of psychiatric disorders in other university samples [94, 95] Furthermore, only six of the 11 students (a total of 6.60% of the entire sample) who reported positive psychiatric or neurological history also reported current prescribed medication use for these conditions, which is similar to other reports in university students [96]. Medication use was not differentially represented across MHI groups and arousal manipulation, 2 (1, n ¼ 91) ¼ 0.10, p ¼ 0.999; 2 (1, n ¼ 91) ¼ 2.95, p ¼ 0.111. Hypothesis 1: Emotional arousal at baseline for students with self-reported MHI relative to those with no self-reported head trauma Baseline measures of arousal and reports of life stressors As hypothesized, students who reported an MHI-with-a-LOC demonstrated a pattern of significantly lower self-reported arousal status at baseline than students with a MHI-with-ASC who were also significantly lower than those who did not report MHI, F(2, 85) ¼ 3.06, p ¼ 0.052 (refer to Figure 1). Despite this, students with self-reported MHI acknowledged significantly higher total scores on the Life Stressors Scale relative to their no-MHI cohort, F(2, 88) ¼ 3.54, p ¼ 0.033, (refer to Figure 2); but, in general, did not acknowledge experiencing more stress on a daily basis, F(2, 88) ¼ 0.90, p ¼ 0.410. Multiple comparisons did not demonstrate significant differences between head injury groups, p40.05. Additionally, students who reported a MHI-with-LOC demonstrated significantly attenuated average EDA amplitude at baseline, as did those with MHI-with-ASC, compared to those with no reported head trauma, F(2, 88) ¼ 13.89, p50.001 (refer to Figure 3). Potential factors

Other health-related information Students’ reports of hospitalizations (i.e. for illness, fractures, surgery or other medical complications), stimulant usage (caffeine, cigarettes), use of relaxation techniques and exercise history did not differ across MHI history groups and arousal manipulation conditions (ps40.05). Similarly, arousal indicators such as level of alertness, reports of typical

Other factors may account for the group differences observed (e.g. baseline mood, exercise history). However, the current analyses showed that mood and exercise history do not adequately/statistically account for the group differences observed. Regression analyses revealed that an index of mood (i.e. irritability) did not predict baseline resting EDA or self-reported arousal for those with self-reported

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Hypothesis 2: Responsivity to the arousal manipulation among MHI history groups Self-reported arousal across testing session

Figure 1. Self-reported arousal state as a function of severity of mild head injury at baseline. Note: *p50.05.

Figure 2. Life stressors scale total score as a function of severity of mild head injury. Note: *p50.05.

Separate 3 (MHI History: no-MHI, MHI-with-ASC, MHIwith-LOC) 2 (Arousal Manipulation Condition: Stress, Relaxation) 2 (Time: Pre-manipulation, Post-manipulation) ANOVAs were conducted for the self-report and physiological emotional arousal measures to investigate responsivity to the induction. Students reported significantly higher arousal in the psychosocial stress condition as compared to the relaxation condition, F(1, 85) ¼ 65.62, p50.001, and the ratings of arousal changed across time, FG-G(1, 85) ¼ 13.01, p ¼ 0.001 (refer to Figure 4), particularly for the stress condition, FG-G(1, 85) ¼ 103.22, p50.001. There were no significant interactions. While there was no main effect of time, F(2, 85) ¼ 2.13, p ¼ 0.125, multiple comparisons demonstrated that self-reported arousal did not change postarousal manipulation for those who reported MHI-with-ASC and MHI-with-LOC, whereas subjects with no reported head trauma had a significant increase in arousal rating to the stress induction and a decrease in response to the relaxation manipulation, ps50.05. There were no 2-way interactions. Further examination of self-reported arousal post-manipulation only (time: immediately after the manipulation, 15, 30 and 45 minutes post-manipulation) revealed a tendency for students with MHI to report less arousal in response to the arousal manipulations than students without MHI, F(2, 85) ¼ 2.61, p ¼ 0.080, as well as a significant 3-way interaction across time (post-manipulation only) and manipulation condition by MHI history, FG-G(3, 105) ¼ 2.25, p ¼ 0.050. Follow-up Mixed Model ANOVAs of self-reported arousal for each MHI history group by condition were conducted and demonstrated that relative to their no-MHI cohorts students with MHI-with-LOC acknowledged significantly less self-reported arousal overall in response to the arousal manipulations, FG-G(3, 36) ¼ 15.06, p50.001, than students with MHI-with-ASC, FG-G(3, 105) ¼ 40.60, p50.001, and students with no-MHI, F(3, 114) ¼ 44.39, p50.001. Electrodermal activation magnitude across time

Figure 3. Baseline average electrodermal activation (EDA) amplitude (mS) as a function of severity of mild head injury. Note: *p50.05.

MHI, F(1, 49) ¼ 1.65, p ¼ 0.205; F(1, 49) ¼ 0.203, p ¼ 0.654, or with no reported MHI, F(1, 38) ¼ 0.001, p ¼ 0.993; F(1, 38) ¼ 0.342, p ¼ 0.562, respectively. Similarly, exercise history (frequency of engaging in exercise weekly) was not significantly related to baseline resting EDA for those with self-reported MHI, F(1, 49) ¼ 0.28, p ¼ 0.597, or no reported MHI, F(1, 38) ¼ 0.51, p ¼ 0.480. Frequency of exercise was also not significantly related to baseline self-reported arousal for those with self-reported MHI, F(1, 49) ¼ 0.49, p ¼ 0.488, or those with no reported history of head trauma, F(1, 38) ¼ 0.65, p ¼ 0.426.

Greater EDA amplitude responses were observed in the psychosocial stress condition than in the relaxation condition, F(1, 85) ¼ 17.47, p50.001, and EDA amplitude responses tended to vary across time (pre- to-post-manipulation), FG-G(1, 85) ¼ 3.27, p ¼ 0.074. Similarly, there was a significant interaction of arousal manipulation condition and time, FG-G(1, 85) ¼ 14.40, p50.001. Students in both self-reported MHI groups produced significantly smaller EDA amplitude responses than those without MHI, F(2, 85) ¼ 27.38, p50.001, and there was a significant interaction of MHI history groups by condition, F(2, 85) ¼ 3.66, p ¼ 0.030, such that persons with selfreported MHI elicited less change in EDA amplitude response to the manipulations and these factors produced a significant 3-way interaction, FG-G(2, 85) ¼ 3.61, p ¼ 0.031 (refer to Figure 5).

DOI: 10.3109/02699052.2013.857787


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Figure 4. Self-reported arousal state as a function of arousal manipulation condition and severity of mild head injury across the testing session. B, Baseline; Pre, Pre-arousal manipulation; Post, Post-arousal manipulation; Post-15 mins, 15 minutes post-arousal manipulation; Post-30 mins, 30 minutes post-arousal manipulation; Post-45 mins, 45 minutes post-arousal manipulation.

Follow-up analysis of the significant 3-way interaction (i.e. separate Mixed Model ANOVAs with arousal manipulation condition across time [post-manipulation time course: immediately after the manipulation, 15, 30 and 45 minutes post-manipulation]) were conducted for each of the no-MHI, MHI-with-ASC, MHI-with-LOC groups and showed that EDA amplitude significantly decreased across the testing session for students with no-MHI, FG-G(3, 114) ¼ 6.46, p ¼ 0.001. Further, for students with no-MHI only EDA amplitude differed as a function of arousal manipulation condition, F(1, 38) ¼ 26.22, p50.001, and significantly changed across time by arousal manipulation condition, FG-G(3, 114) ¼ 26.46, p50.001. However, for students with MHI-with-ASC their EDA amplitude signal did not change significantly across time, FG-G(3, 105) ¼ 2.13, p ¼ 0.122, but did differ as a function of arousal manipulation condition, F(1, 35) ¼ 5.02, p ¼ 0.031, and produced a significant interaction across time by arousal manipulation condition, FG-G(3, 105) ¼ 10.94, p50.001, such that modified arousal state was not longlasting across time. Importantly, students with MHI-with-LOC were not significantly responsive to the arousal manipulations, F(1, 12) ¼ 0.17, p ¼ 0.690, and arousal states were not significantly different across time, FG-G(3, 36) ¼ 0.83, p ¼ 0.451; FG-G(3, 36) ¼ 2.25, p ¼ 0.126, and this group demonstrated the lowest EDA amplitude responsiveness compared to the MHIwith-ASC and no-MHI groups. Hypothesis 3: Cognitive performance as a function of modified arousal state and self-reported history of mild head trauma Neuropsychological performance Cognitive performance was examined via 2 (MHI History: MHI, No-MHI) 2 (Arousal Manipulation Condition: Stress,

Relaxation) ANOVAs as well as repeated measures ANOVAs (Time: Pre-manipulation, Post-manipulation), with a main focus on the comparison between those who had reported an MHI relative to those with no history of head trauma. Abbreviated measure of function. Measures of general

general intellectual intellectual functioning (Block Design, Vocabulary; WAIS-III [85]) were conducted prior to other cognitive tasks and the arousal manipulation. Neither measure differed significantly between students who self-reported mild head trauma and those who did not report head trauma (Block Design: F(1, 87) ¼ 0.09, p ¼ 0.768; Vocabulary: F(1, 87) ¼ 1.85, p ¼ 0.177) in terms of visuospatial (Block Design) and verbal (Vocabulary) performance. Further, there was no significant difference in educational level between those who self-reported MHI compared to those with no reported history of head trauma, 2(1, n ¼ 91) ¼ 1.61, p ¼ 0.901.

Pre- and post-manipulation comparisons of cognitive performance Attention/inhibitory control. Prior to the arousal manipula-

tion, attention measures differed as a function of MHI history. Students with self-reported MHI were significantly slower in completing the complex attentional switching task (ColourWord Interference Task; DKEFS [53]), F(1, 87) ¼ 4.67, p ¼ 0.033, colour-naming task, F(1, 87) ¼ 3.06, p ¼ 0.084, and word reading task, F(1, 87) ¼ 4.94, p ¼ 0.029, than students with no history of MHI. However, again, those with MHI were significantly slower than their no-MHI counterparts on both measures, respectively, F(1, 87) ¼ 4.98, p ¼ 0.028; F(1, 87) ¼ 3.90, p ¼ 0.052, with repeated testing (i.e. pre–post manipulation). Participants were significantly

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Figure 5. Electrodermal activation (EDA) amplitude (mS) as a function of arousal manipulation condition and severity of mild head injury across the testing session. B, Baseline; Pre, Pre-arousal manipulation; During, During arousal manipulation; Post, Post-arousal manipulation; Post-15 mins, 15 minutes post-arousal manipulation; Post-30 mins, 30 minutes post-arousal manipulation; Post-45 mins, 45 minutes post-arousal manipulation.

faster at completing the more complex attentional switching task, F(1, 87) ¼ 63.85, p50.001, and naming the colour of the ink, F(1, 87) ¼ 33.10, p50.001 (Colour-Word Naming Interference Task; DKEFS [73]) when it was given for a second time. Students did not read the words (DKEFS [73]) more proficiently the second time this task was given, F(1, 87) ¼ 1.15, p ¼ 0.287, not surprisingly, since this measure often approaches a ceiling due to the ease of the task. Students read faster in the stress condition than in the relaxation condition, F(1, 87) ¼ 4.47, p ¼ 0.037. Prior to the arousal manipulation there were no significant differences on the inhibition task observed between those who reported MHI and those who did not report head trauma, F(1, 87) ¼ 1.55, p ¼ 0.217. Students demonstrated significantly increased proficiency for the inhibition task (i.e. naming the colour of the ink the word is printed in while inhibiting the pre-potent response of reading the word), F(1, 87) ¼ 51.33, p50.001, with repeated testing. Performance on this task did not differ between MHI history groups, F(1, 87) ¼ 2.57, p ¼ 0.113, despite a similar pattern of slower response times. Working memory. Students with a self-reported history

of MHI tended to perform worse on working memory tasks than their no-MHI counterparts. More specifically, prior to the arousal manipulation, students with self-reported MHI tended to make more errors on the Trail Making Test (numbers only) (DKEFS [73]) than students without reported MHI, F(1, 87) ¼ 3.38, p ¼ 0.069, but performance did not differ across time (pre- to post-manipulation), F(1, 87) ¼ 0.48, p ¼ 0.492, nor produce a significant interaction. Processing speed for the Trail Making Test did not differ between self-reported MHI groups pre-manipulation, F(1, 87) ¼ 2.43, p ¼ 0.123; however, overall students with

self-reported MHI were significantly faster compared to students who did not report a head trauma, F(1, 87) ¼ 4.02, p ¼ 0.048. While students produced significantly more symbols (Digit Symbol-Copy; WAIS-III [85]) with repeated testing, F(1, 87) ¼ 94.52, p50.001; there was and remained a main effect of MHI history such that students with MHI produced less symbols on the Digit Symbol-Copy test, F(1, 87) ¼ 4.81, p ¼ 0.031. Despite a consistent pattern of students with MHI tending to perform more poorly on working memory and attentional tasks prior to the arousal induction, overall there were no significant interactions of modified arousal and history of head trauma on cognitive performance ps40.05.

Discussion The purpose of this study was to investigate emotional arousal (as measured via self-report and physiological arousal measures) of university students who self-reported sustaining a MHI as compared to students without a reported history of head trauma; to examine possible differences in responsivity to arousal manipulations (i.e. psychosocial stressor, relaxation) between those who self-reported a history of mild head trauma and students who did not report MHI; and to investigate the effects of experimentally modified arousal state on cognitive performance in these students. This study also examined the prevalence and aetiology of self-reported MHI in university students, as research on this age-group is limited. In line with the expectations based on literature of persons with substantive and documented neural disruption [33, 41, 56, 64], students who reported having previously sustained MHI demonstrated less emotional arousal (both self-report and autonomic responses) relative to their no-MHI cohort,

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despite reporting significantly more experiential life stressors. More specifically, prior to any arousal manipulation, students with a self-reported history of MHI rated themselves as having a significantly lower arousal state and demonstrated less autonomic emotional arousal (i.e. attenuated average EDA amplitude) than students who had not reported MHI despite reporting multiple stressful life events (i.e. relationship or financial difficulties). Consistent with these findings, an impressively reduced range of physiological response to the psychosocial stressor was found for students who reported previous MHI relative to those who did not report a history of prior head trauma, in that students with self-reported MHI demonstrated flatter EDA and self-reported responses than students who did not report prior head trauma. There was striking evidence of a gradient of under-arousal among the head injury groups. Students with self-reported MHI-with-ASC, but more so students with MHI-with-LOC, demonstrated reduced emotional arousal responsivity in terms of physiological activity to the manipulation conditions across time as compared to those with no history of MHI. These findings are similar to that shown in persons with moderate-to-severe TBI. For example, Tranel and Damasio [33] demonstrated that patients with damage to the VMPFC had poorer electrodermal skin conductance responses, particularly in response to affective/psychological stimuli (highly-charged visual stimuli) [37]. Notably, these findings are unique with respect to the differential responses to psychosocial stressors of persons with mild head trauma relative to persons with no reported history of head injury. Emotional events such as a psychosocial stressor triggers neural activity (especially involving the amygdala, which initiates the stress response [98]) and a cascade of changes in autonomic and endocrine systems. Ultimately, this activity is interpreted as an emotional experience [50]. The sympathetic index of emotional arousal used in this study (i.e. EDA) differed between students who reported a history of mild head trauma when compared to students who did not report any head trauma. Furthermore, those students who acknowledged a loss of consciousness associated with their self-reported MHI elicited the most attenuated physiological response, followed by those who reported only an ASC (i.e. only feeling dazed, dizzy or confused following the head trauma event) compared to the students with no reported history of head injury. This finding suggests that emotional responses to stressors, particularly physiological activity (i.e. sympathetic), may differ, albeit subtly but significantly, even for persons with self-reported history of head trauma in a fashion similar to that of persons with moderate or severe neural disruption. This finding also supports a continuum of severity of injury. The attenuated emotional arousal of students who self-reported prior mild head trauma relative to their peers with no reported MHI may be suggested to be a residual change in autonomic functioning. It is possible that this under-arousal may be related to subtle VMPFC dysfunction which may have occurred with the previous self-reported head trauma, as this region is especially vulnerable to damage [13, 60]. Research of persons with moderate-to-severe disruption to the VMPFC has shown this region to be important in the modulation of autonomic


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and emotional responses; and is associated with diminished physiological arousal to emotionally-evocative stimuli with disruption [34, 35]. However, given that there is no medical documentation or neuroimaging data to support the behavioural observations of attenuated emotional arousal of students with self-reported MHI relative to their peers with no reported history of head trauma, the following is acknowledged to be theoretical in nature. If the VMPFC is mildly damaged or its connectivity to other areas (e.g. limbic, sensory, etc.) is disrupted in mild head trauma, this could possibly be related to the mild under-arousal in persons with self-reported MHI. Theoretically in concert with Damasio et al.’s [63, 64] somatic marker hypothesis, students with self-reported MHI may experience a lessened ability to interpret emotional signals [64] or may be less impacted by stressors in their environment, which is reflected in the mismatch between increased reports of life stressors and lower self-reported and physiological arousal. As previously discussed, the amygdala has rich connections with the hypothalamus, pre-ganglionic sympathetic nervous system, as well as the VMPFC (see Kringelbach and Rolls [99] and Wallis [100] for reviews) and damage to the VMPFC may result in altered communication with the amygdala which typically initiates the stress response. As such, it is possible that persons with MHI may be less likely to have heightened autonomic arousal at resting state and/or differential stress responsivity to stressor manipulations as was evidenced in the current study. Of particular interest, a study by Bay et al. [52] reported that cortisol profiles in persons with mild-to-moderate TBI were dysregulated, which indicated dysfunctional stress responsivity similar to that found in the current study. Persons with mild-to-moderate TBI reported experiencing more stressors in their life, but produced hypocortisolemia (i.e. reduced release/ presence of cortisol in saliva) with demonstrated flat diurnal trends. Bay et al. interpreted the hypocortisolemia of patients with brain injury as potentially the result of chronic stress (reduced cortisol production due to depleted stores and capacity); although it is similar to these findings and may reflect dysregulation. The current findings suggest that neuropsychological testing and/or symptom reporting following even mild head trauma should include some assessment of current stressors as well as their ability to respond to emotional events (such as psychosocial stressors). Moreover, the minimized responses to stress in the self-reported MHI group in the current study could have consequences for adaptive behaviour in the social realm. For example, emotional functioning may be reflected in social interactions [38, 50] and it is possible that, for persons with mild head trauma with minimized responses to emotionally-evocative events, may be viewed as disinterested and/or insensitive, at worst. Potentially, this decreased emotional responsiveness may mildly affect social relationships and interactions with others. Furthermore, the development of rehabilitation techniques for managing stress (e.g. coping strategies, relaxation) may be informed by the current study and future investigations of stress responsivity in persons with head trauma. The possibility was explored that students with a selfreported history of mild head trauma would perform less well

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on neuropsychological measures prior to any arousal manipulation relative to their no-MHI cohort. Subtle differences were observed on working memory and attentional tasks for students who self-reported head trauma relative to those who did not report prior head trauma, in that students with selfreported MHI performed less well on these tasks. In line with these findings, a study by Vanderploeg et al. [9] demonstrated subtle, poorer attentional and working memory performance for persons with mild TBI relative to healthy controls, even 8 years post-injury, in a non-referred, community sample of veterans. However, other research has demonstrated minimal, if any, differences in cognitive functioning of healthy controls relative to persons with mild head trauma post-acute phase. For example, a meta-analysis by Schretlen and Shapiro [101] demonstrated that by 30–89 days post-injury the effect sizes of mild head trauma on cognitive functioning were negligible. Another meta-analysis by Rohling et al. [102] similarly revealed that the neuropsychological functioning of persons with MTBI was indistinguishable from that of healthy controls 3 months post-injury. However, Pertab et al. [103] suggested that meta-analyses may obscure residual impairments in neuropsychological functioning after mild head trauma. In summary, the long-term neuropsychological consequences of mild head trauma continue to be debated. Moreover, based on the literature regarding arousal and cognitive abilities (e.g. see Lupien et al. [70] for reviews) as per Yerkes-Dodson Law [69], performance on the neuropsychological measures was expected to vary post-arousal manipulation and for this pattern to differ for students with and without self-reported MHI. Specifically, it was predicted [24, 25, 27–30] that students who reported a history of MHI would be subtly disadvantaged compared to their selfreported no-MHI cohort on working memory and attentional tasks and further that the cognitive performance of persons with self-reported MHI would benefit via increased arousal through the introduction of a psychosocial stressor and would be impaired following a relaxation induction, in contrast to students without MHI. Despite a pattern of performance for students with self-reported MHI on cognitive measures pre-manipulation, evidence was not found, at least in this study, of modified arousal relating to cognitive ability. There is no doubt that a multitude of factors influence outcome from mild head trauma. Similarly, many factors likely contributed to the lack of finding cross-over interactions of arousal manipulation and self-reported MHI history on cognitive measures. The limited responsivity of students with MHI-with-LOC as compared to students with MHI-with-ASC and those with no-MHI may have restricted the hypothesized arousal manipulation condition and MHI history interaction with cognitive performance. Although physiological and self-report measures demonstrated that the manipulations were effective in inducing changes in arousal status, the effect may have been insufficient in terms of longevity to modify cognitive performance over the testing session. Further, the stressor was mild compared to some manipulations (e.g. videotaping performance) and brief (i.e. most other tests using this manipulation last 30 minutes—see Dickerson and Kemeny [97]). As well, the relaxation manipulation may have reached a floor—which

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prohibited any further change. Moreover, the long-term neuropsychological profile of mild head trauma is hotly debated [21, 22, 24, 101–103] and it is possible that the negligible differences on neuropsychological measures post-arousal manipulation reflect the disunity and variability in long-term outcomes following mild head trauma. Furthermore, it is also acknowledged that other factors may account for the group differences observed (e.g. baseline mood, exercise history). However, analyses showed that mood and exercise history do not adequately/statistically account for the group differences observed in emotional arousal in the current study. Lastly, other factors such as personality characteristics and so forth may play a role in emotional arousal, but are beyond the scope of this study to analyse. This approach to examining persons with mild head trauma is different from most in that other investigations assess patients who have been diagnosed with or without complicated MTBI (i.e. complaints of post-concussive symptoms who have been referred, typically by the treating medical facility or sports team, for assessment to a neuropsychologist or to an out-patient clinic for treatment [4, 18, 24, 104–109]. These approaches have typically assessed persons in the acute post-injury period, perhaps because the literature regarding long-standing impairments in cognitive function and other domains following milder brain injuries has been highly controversial (refer to [16–18, 102] for discussion). The inclusion criteria were much more broad (only 39% of the sample reported medical/formal documentation of his/her injury) and assessed subjects months post-injury (i.e. 60 months on average) in order to avoid injury recovery [110–112] and other confounds. Further, in studies using medically substantiated or pre-screened subjects, symptom reporting and overall performance may be affected due to possible litigation (i.e. over reporting [113, 114]), sport career consequences (i.e. under-reporting [112, 115]) or bias/ expectations (i.e. awareness of study purpose [76, 77]). Finally, most compare performance to that of an assigned control group that pre-selects subjects for age, education, sex, intelligence capacity or other factors to match patients or athletes with head trauma. Although mild head trauma events were self-reported in this study, they are similar to the information obtained in a clinical interview. Even though the head trauma reporting may be subject to bias, the physiological and cognitive measures used in this study are not retrospective variables—these behavioural measures are objective and were obtained in an experimental setting. Nonetheless, limitations of this method of obtaining medical history include inaccurate recall and methods that include collateral information (i.e. medical documentation) may improve the retrospective reports of head trauma in that documentation permits an alternative source of verification of status. Furthermore, in this study, the approach, however, did not recruit participants on the basis of head injury history; nor were they informed that the purpose of the study was to examine various cognitive, emotional and physical aspects of self-reported head trauma until all testing was completed, in order to avoid the impact of diagnosis threat on performance [76, 77]; participants were high-functioning university


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students (regardless of history of MHI) and, to the authors’ knowledge, they were not involved in litigation as a result of their head injury; students were not pre-selected or matched on any measures, but rather represented the general population of students and instead were assigned to their head injury status group post-experiment. This sample is representative of retrospective self-report of mild head injury in university students and, given the aforementioned considerations, is unique. This research contributes to the limited information available regarding the prevalence of MHI for the high risk period of birth to 25 years of age [116]. As previously discussed, the prevalence of self-reported MHI was found to be 56% in this sample. Notably, the majority reported only an ASC and no LOC. It is acknowledged that self-reports of head injury may be inaccurate and gaining information from collateral sources (i.e. hospital records, family members, witnesses of the head injury and so forth) may be more reliable. However, less than half of this sample reported receiving medical treatment for their injury and, of those who did seek treatment, 90% did not stay overnight in a medical facility. This finding is similar to another study that found that 81% of university students reported they were not admitted to the treating medical facility for a self-reported head injury [117]. The MHI criteria used in this study was not based on hospital admissions and, thus, revealed a larger proportion reporting history of MHI [7] and may present a more realistic picture of reports of sustaining a head injury sufficient to produce an ASC in this population. Furthermore, head injuries occur quite frequently for young adults as compared to other age groups [3, 6] and, thus, the increased prevalence in this sample could be a function of the selection of post-secondary students. Nonetheless, the aetiology of MHI in this sample followed similar patterns to that of others examining this age group [5, 116], with sports-related injuries most commonly reported, followed by falls; however, motor vehicle collisions were not found to be a common cause of injury in this study. Regardless of the manner in which the history of sustaining a head injury was acquired (i.e. self-report and not via medical records) and, perhaps even more impressively, these results show that simply endorsing criteria of a history of an altered state of consciousness as a result of injury to the head presents with a profile different than that of students who did not report such history. The generalizability of the current study is limited in that the sample is restricted to university students with subtle, self-reported injury. The sample does not capture those students who have had to drop out due to academic difficulties possibly as a function of previous head injury. Those students may be hypersensitive to their environment and may have found the university setting too stimulating. Therefore, it remains possible that this self-reported MHI sample consists of only those who are hypo-aroused and perhaps this is why they present with an under-aroused profile. Nonetheless, for those that do remain, they are different from their university cohort and similar to their moderate and severe brain injury peers in terms of emotional arousal and stress responsivity. As well, two-thirds of this sample was female, whereas head-injured individuals are more likely to be male [3]. This reversed effect reflects the

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university population, but under-represents the TBI population and may reflect an arousal difference due to sex [98]. However, post-hoc analysis examining the results within sex do not support any effects due to sex. Another limitation of this study is that there was no systematic attempt to measure emotional arousal prior to any reported head injury given the cross-sectional, retrospective nature of the study. Longitudinal and prospective research can better address the causality confounds encountered with cross-sectional, correlational research. As such, it may be argued and it is possible that other factors contribute to the reduced emotional arousal observed in the current study. Due to the cross-sectional approach used in the current study, it may be argued that the persons in this sample with MHI possess personality trait(s) that may be related to their lowered arousal. For example, sensation seeking (a risk-taking characteristic) could pre-dispose an individual to sustaining a MHI may also contribute to (or reflect) pre-injury lowered arousal status. Other personality characteristics may also be associated with emotional arousal and/or responsiveness to emotional events [118, 119]. Although it is acknowledged that this may be the case, given the consistency of the findings of under-arousal and a gradient of under-arousal based on injury severity (i.e. no injury, ASC only, LOC and ASC in this study; then moderate through severe injury in other studies) across various measures (i.e. EDA, self-report ratings), it is no more confounding in this study than in studies with more serious and documented neural trauma. Therefore, these findings of differential emotional arousal may be related to prior self-reported history of mild head trauma and may suggest frontal lobe involvement. However, the findings of this study require replication with clinically diagnosed populations. Explicit manipulation of stressors and arousal could be replicated with clinically diagnosed populations and it would be expected that the discrepancies in arousal would be even more pronounced in individuals with less subtle injury. Even so, the findings from this study are striking, especially because of the liberal criteria of self-reported ASC accompanying head trauma.

Conclusions The findings from this study have consistently supported the hypotheses of under-arousal and lessened stress responsivity of persons who report prior MHI. Most outstanding is the finding that emotional arousal status and response to psychosocial stress differed between students who reported MHI relative to those who did not report a prior head trauma event and appears to mirror that of persons with moderateto-severe VMPFC disruption, albeit subtly. These findings are interpreted as demonstrating that students who reported experience of mild, but notable, injury to the head may have a lessened ability to interpret and respond to stress, possibly as a function of subtle disruption to the VMPFC, as this region has been implicated in modulating emotional and autonomic responses [50, 64, 100]. Hypothetically, the decreased perception of stress, despite increased reports of life stressors, may suggest that persons who report prior MHI may be less impacted by emotional events potentially related to reduced feedback to the VMPFC [64], which

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may be associated with potential difficulties in everyday life. To the authors’ knowledge this is the only study with a detailed examination of physiological and self-reported emotional arousal in persons with milder head injuries and their response to stress. Further examination of these findings of differential emotional arousal will lead to a better understanding of the potential difficulties persons with milder head injuries encounter.

Declaration of interest The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper. JB held funding from the Social Sciences and Humanities Research Council of Canada (SSHRC) Joseph Bombardier Canada Graduate Scholarship, Ontario Graduate Scholarship (OGS) and American Psychological Foundation (APF)/ Council of Graduate Departments of Psychology (COGDOP) Graduate Research Scholarship during the collection and preparation of this research. DG holds funding from the Ontario Neurotrauma Foundation and is affiliated with the Ontario Brain Injury Association. The authors acknowledge that portions of this research have been presented at national and international conferences and abstracts related to this work have been published from conference proceedings [120–122].

Notes 1. Although the prevalence of MHI makes up more than half of this sample, previous research (e.g. 39.4% MHI [79]; 51% MHI [80]; 30% MHI [68]; 41% MHI [81]) has shown similar proportions when using this liberal criterion of ‘altered state of consciousness’ in a university student population. 2. Studies [5,93] have reported that males are 1.5-times more likely to incur a head injury than females; further, males are twice as likely as females to incur a mild head injury, especially from 15–24 years of age.

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Post-traumatic and emotional symptoms in different subgroups of patients with mild head injury.

Mild head injury classification.

Minor and severe head injury emotional sequelae.

Sustained attention following mild closed-head injury.

Mild closed head injury and seizures.

Daily stressors and emotional reactivity in individuals with mild cognitive impairment and cognitively healthy controls.

Circulating proteasome activity following mild head injury in children.

Office management of mild head injury in children and adolescents.

Cognitive effects of mild head injury in children and adolescents.

Olfactory function after mild head injury in children.

A strategy to optimize CT use in children with mild blunt head trauma utilizing clinical risk stratification; could we improve CT use in children with mild head injury?

Neurobehavioral aspects of postconcussive symptoms after mild head injury.

Symptoms following mild head injury: expectation as aetiology.

A conceptual model of emergency physician decision making for head computed tomography in mild head injury.

Comparative evaluation of MRS and SPECT in prognostication of patients with mild to moderate head injury.

Neuropsychological deficits in patients with minor head injury after concussion and mild concussion.

Models of mild traumatic brain injury: translation of physiological and anatomic injury.

Enhanced attention capture by emotional stimuli in mild traumatic brain injury.

Expected Emotional Usefulness and Emotional Preference in Individuals with Major Depressive Disorder.

A novel closed-head model of mild traumatic brain injury caused by primary overpressure blast to the cranium produces sustained emotional deficits in mice.

Psychological well-being in individuals with mild cognitive impairment.

Motor, visual and emotional deficits in mice after closed-head mild traumatic brain injury are alleviated by the novel CB2 inverse agonist SMM-189.

[Mild head injury in children and adults: Diagnostic challenges in the emergency department].

Changes in saccadic eye movement and memory function after mild closed head injury in children.