Loss of Emotional Experience After Traumatic Brain Injury: Findings With the Startle Probe Procedure

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1 Neuropsychology Copyright 2006 by the American Psychological Association 2006, Vol. 20, No. 2, /06/$12.00 DOI: / Loss of Emotional Experience After Traumatic Brain Injury: Findings With the Startle Probe Procedure Jennifer Clare Saunders, Skye McDonald, and Rick Richardson University of New South Wales The authors used affective modulation of the eyeblink startle response to examine the impact of traumatic brain injury (TBI) on emotional reactions to pictures. Participants were 13 individuals with severe TBI and 24 controls. Participants were presented with pictures that differed in affective valence (e.g., mutilated bodies, erotic couples, and household objects) while the eyeblink startle response to an acoustic probe was measured. Startle amplitude was used to assess valence of emotional response, and startle latency was used to index interest in the pictures. Subjective ratings of the affect and arousal elicited by the various pictures were also obtained. TBI impaired startle potentiation to unpleasant pictures but not startle attenuation to pleasant pictures. Further, subjective ratings indicated that TBI participants found unpleasant pictures less arousing than did controls. The results are consistent with recent evidence of differential impairment in negative versus positive emotions after TBI and are discussed in relation to 2 competing explanations of startle modulation. Keywords: traumatic brain injury, affective processing, startle reflex Jennifer Clare Saunders, Skye McDonald, and Rick Richardson, School of Psychology, University of New South Wales, Sydney, Australia. Collection of data for this study was facilitated by Discovery Grant DP from the Australian Research Council. We express our gratitude to the staff of Ryde, Liverpool, and Westmead brain injury units for facilitating access to patients within their service. We are indebted to the people with traumatic brain injury and to their families as well as to our community participants, who gave willingly of their time to make this research possible. Correspondence concerning this article should be addressed to Skye McDonald, School of Psychology, University of New South Wales, Sydney, 2052 Australia. s.mcdonald@unsw.edu.au Traumatic brain injury (TBI), often sustained as a consequence of motor vehicle accidents, results in both multifocal and diffuse brain damage. Although there is heterogeneity in the localization and severity of damage between individuals, the ventrolateral and inferior orbital frontal cortices and the temporal lobes are particularly vulnerable to injury (Courville, 1945; Gentry, Godersky, & Thompson, 1988; Hadley et al., 1988). Neuropsychological impairments are common after TBI, as are difficulties in psychosocial functioning (e.g., Tate, Lulham, Broe, Strettles, & Pfaff, 1989). Although cognitive and behavioral deficits (e.g., rigid thinking, increased aggressive behavior, mood and personality changes; Lezak, 1978; Prigatano, 1986) have been surmised to cause these psychosocial deficits, another potential contributing factor is an impairment of emotional processing (Hornak, Rolls, & Wade, 1996). Recent research has established that TBI disturbs the individual s ability to understand important emotional cues such as facial expressions (e.g., Green, Turner, & Thompson, 2004; Hornak et al., 1996; McDonald & Flanagan, 2004; Milders, Fuchs, & Crawford, 2003; Spell & Frank, 2000), with preliminary evidence suggesting greater impairment in recognizing negative relative to positive emotions (Croker & McDonald, 2005; Hopkins, Dywan, & Segalowitz, 2002; Jackson & Moffat, 1987; McDonald, Flanagan, Rollins, & Kinch, 2003). In addition, individuals with TBI have been reported to have increased emotional lability and decreased ability to experience different emotional states (Croker & McDonald, 2005; Hornak et al., 1996; Prigatano, 1986). Processing of emotions, especially negative emotions, appears to be mediated by a system encompassing the limbic system and the orbitofrontal cortex (Adolphs, 2002). Within this temporofrontal system, it has been suggested that discrete neural systems mediate different emotions (Adolphs, Damasio, Tranel, & Damasio, 1996; for a review, see Adolphs, 2002). For example, the prefrontal cortex has been implicated in the recognition of anger (Harmer, Thilo, Rothwell, & Goodwin, 2001), the insula and basal ganglia are important for the recognition and experience of disgust (Calder, Keane, Manes, Antoun, & Young, 2000), and the amygdala has been implicated in fear and defensive behavior (Adolphs, Tranel, Damasio, & Damasio, 1995; LeDoux, 2000). Furthermore, neuroimaging, clinical, and experimental studies suggest that there may be hemispheric asymmetry in the processing of different emotions (e.g., Adolphs et al., 1996; Borod, 1993; Ley & Bryden, 1979; Reuter-Lorenz & Davidson, 1981), leading to a view that the right hemisphere is dominant either for all emotions (e.g., Borod, 1992) or for negative emotions specifically (e.g., Davidson & Irwin, 1999). Of relevance to the present study is the potential link between emotion perception and emotional responsivity. Recent neuropsychological models of emotion have suggested that a neural system entailing the amygdala, insula, ventral striatum, ventral regions of the anterior cingulate gyrus, and prefrontal cortex may mediate both the identification of emotionally significant stimuli and the production of affective states and autonomic responses to those stimuli (Phillips, Drevets, Rauch, & Lane, 2003). Indeed, it has been suggested that an empathic, emotional responses to facial expressions assists the perceiver to understand the particular emotion displayed (Wild, Erb, & Bartels, 2001). The idea that the identification of and response to emotional stimuli are mediated by the same neural system is supported by reports that individuals 224

2 EMOTIONAL EXPERIENCE AND THE STARTLE REFLEX IN TBI 225 with TBI have both impairments in emotion recognition and altered subjective emotional feeling. Croker and McDonald (2005), for example, reported a significant association between the capacity to match facial expressions and self-reported loss of emotional experience; that is, those who were poorest at recognizing emotional expressions reported the greatest reduction in their emotional experiences in general. Although this finding is suggestive, self-report measures of altered emotional experience may be inaccurate, especially as lack of insight and concern often accompanies frontal dysfunction. More objective evidence of a lack of emotional responsivity such as provided by physiological correlates of responsiveness to emotional stimuli is required. A few studies have examined the effect of both localized frontal damage and TBI on physiological responses to emotional stimuli and have demonstrated abnormal electrodermal activity (EDA). For example, Damasio, Tranel, and Damasio (1990) found that passive viewing of neutral and emotionally charged pictures did not elicit the same pattern of EDA in participants with orbitomedial prefrontal damage as seen in control participants. Further, Hopkins et al. (2002) reported that individuals with TBI displayed marked electrodermal hyporesponsivity to negative facial expressions, compared with controls. Although such research is intriguing, traditional psychophysiological measures do not measure emotional valence. EDA varies primarily with the degree of (emotional) arousal elicited by the stimulus (e.g., Lang, 1995; Lang, Bradley, & Cuthbert, 1990); that is, highly attractive stimuli increase EDA as much as highly aversive stimuli. Similarly, cardiovascular activity indexes metabolic activity and attentional demands (Lacey, 1967), and facial electromyogram (EMG) is influenced by facial (emotional) expression (e.g., Dimberg, 1990). In contrast to these measures, individuals startle responses when viewing emotional material are sensitive to valence (Lang et al., 1990; Vrana, Spence, & Lang, 1988). Furthermore, the startle reflex is automatic and independent of conscious behavior and voluntary control. Unlike facial expression it is unaffected by demand characteristics and subject reporting (Bradley, Cuthbert, & Lang, 1999; Cook, 1999; Vanman, Dawson, & Brennan, 1998). It is a reliable finding that positive foreground stimuli inhibit, and negative stimuli potentiate, the amplitude of the startle reflex (e.g., Bradley, Cuthbert, & Lang, 1990). Because affective modulation of startle is highly replicable, it has been a useful tool for investigating affective processing in various clinical populations (e.g., fear and phobia: Hamm, Cuthbert, Globisch, & Vaitl, 1997; psychopathy: Patrick, Bradley, & Lang, 1993; schizophrenia: Schlenker, Cohen, & Hopmann, 1995). The dominant theoretical account of affective modulation of the startle response has been framed within the notion of motivational priming: The startle reflex (a defensive response) is enhanced or inhibited depending on whether the foreground stimulus evokes a state of aversive readiness, matching the reflex, or an appetitive state, counteracting the reflex (Lang et al., 1990). Stimuli that most strongly activate a motivational system (i.e., stimuli that are highly aversive or appetitive) produce the strongest startle modulation effects (Bradley et al., 1999). An alternative explanation has been proposed that suggests that startle modulation reflects attention. That is, startle attenuation is caused by attention being directed toward a different (typically visual) modality from that of the (typically acoustic) startle probe, leaving few resources available to process the probe when it occurs (Anthony & Graham, 1985). Although attention may mediate some effects, it is clear that, at least at extreme points along the valence spectrum (extremely aversive or pleasant), the valence of the foreground stimulus reliably predicts the direction of the modulation of the startle response. The neural pathway mediating the basic startle reflex is well understood: The expression of the reflex itself is controlled at the brainstem level (Yeomans & Frankland, 1995; for a review, see Davis, Walker, & Lee, 1999). Its modulation, however, implies that there are secondary neural circuits that influence the basic reflex pathway. Substantial evidence in both animal and human research suggests that subcortical structures, notably the amygdala, are involved in potentiating the startle response during exposure to aversive stimuli (see Grillon & Baas, 2003; Lang, 1995). Although the neural pathway mediating attenuation of the startle reflex during exposure to pleasant stimuli is less studied, it is known that pleasure attenuation of startle is disrupted, at least in rats, by lesions to the nucleus accumbens but not by lesions to the amygdala (Koch, Schmid, & Schnitzler, 1996), suggesting different neural bases for startle modulation by pleasant and aversive stimuli. Only a few studies have used the startle probe procedure to examine emotional experience in brain-injured populations. The normal pattern of startle magnitude (pleasant neutral unpleasant) has been reported in patients with left temporal lobe lesions but not right temporal lobe lesions (Funayama, Grillon, Davis, & Phelps, 2001), and a lack of potentiation to unpleasant pictures has been reported in one patient with a right amygdala lesion (Angrilli et al., 1996) as well as patients with right, left, or bilateral anteromedial temporal lobectomy (Buchanan, Tranel, & Adolphs, 2004). Further, patients with right temporal lobe lesions showed the usual pleasure attenuation effect; however, those with left temporal lesions did not (Buchanan et al., 2004). Taken together, these studies suggest an important role for the right amygdala, in particular, in negative emotional states, although they remain inconclusive with regard to the role of the right hemisphere in positive emotional states and to the role of the left hemisphere in mediating either negative or positive emotional states. Current Study The startle paradigm provides an objective measure of emotional experience and would seem to be an appropriate measure of such experience in the TBI population, but to date, it has not been used with this population. Doing so was the main aim of the present investigation. More specifically, we investigated whether TBI altered the normal pattern of affective modulation of the startle reflex. Given reported impairments in emotion recognition and subjective emotional experience in the TBI population, it was expected that individuals with TBI would not demonstrate the same affective modulation of the startle response as seen in control participants. Further, because of the emerging evidence that TBI differentially affects the processing of negative emotions, it was expected that individuals with TBI would not show the usual potentiated startle response when viewing negative emotional stimuli. It was more difficult to predict the nature of the effects of positive emotions on the startle reflex in the TBI group.

3 226 SAUNDERS, MCDONALD, AND RICHARDSON Participants Method Participants were 14 male volunteers with a TBI and 25 male control participants. The sample was restricted to men, as TBI is more common in men and an all-male group preempted the difficulty of finding stimuli that were equivalent in pleasant and unpleasant dimensions across gender. TBI participants were recruited from three brain injury units in Sydney, Australia, and volunteered their time. TBI participants were recruited on the basis that (a) they had sustained a severe TBI (posttraumatic amnesia greater than 1 day); (b) they were at least 1 year postinjury and therefore neurologically stable; (c) they knew sufficient English to comprehend the instructions; and (d) according to clinical records, they were not suffering from visual, auditory, or facial motor disturbances or from psychosis or other psychiatric conditions. Control participants were first-year psychology students and received course credit in return for participation in the study. It was not necessary to match the two groups on demographic variables, as the dependent variable is a basic physiological response that is not moderated by conscious or controlled processes. Indeed, similar startle patterns have been found in university students and nonpsychopathic prison inmates (Bradley et al., 1990; Levenston, Patrick, Bradley, & Lang, 2000). Data from 1 control and 1 TBI participant were excluded owing to excessive EMG background levels and equipment difficulties, respectively. The clinical information regarding the 13 TBI participants included in the analyses is detailed in Table 1. Clinical information was obtained from clinical notes, pathology reports on initial admission, and self-report. Causes of injury included motor vehicle accidents (n 7), assault (n 4), and falls (n 2). The average length of posttraumatic amnesia was 78 days (range days), and the mean time postinjury was 6 years 9 months (range 1 17 years). Pathology on initial admission included skull fractures (n 1), contusions (n 5), intracerebral or subarachnoid hemorrhages (n 5), and subdural and extradural hemorrhages (n 5). Four participants reported left-focused injuries, 7 reported right-focused injuries, and 2 had bilateral injuries. Specific frontal lobe injuries were reported in 7 participants. Initial evidence of cerebral pathology is only a rudimentary measure of injuries sustained, with more recent and sophisticated measures of cerebral pathology being unavailable at the time of the study. On average, the TBI participants had achieved 14 years of education. Prior to injury they had been employed in occupations ranging from unskilled (n 1) to skilled trade (n 7), clerical (n 1), professional or managerial (n 1), or full-time study (n 3). At time of recruitment, 9 TBI participants were unemployed or working as volunteers, 3 were studying, and 1 was working full time in a clerical setting. Stimuli The acoustic startle stimulus was a 50-ms, 100-dB burst of white noise with an instantaneous rise/fall time. Startle stimuli were produced by a Coulbourn audio source module (V85-05; Coulbourn Instruments, Allentown, PA) and Pioneer stereo amplifier (A-109) and were presented binaurally through Philips stereo headphones (SBC HP 600). Onset, duration, and interval between stimuli were computer controlled. A total of 18 pictures selected from the International Affective Picture System (IAPS; Lang, Bradley, & Cuthbert, 1999) were used in this experiment. Pictures were chosen to represent three affective categories: pleasant, neutral, and unpleasant. Pleasant pictures included opposite-sex nudes and erotica, unpleasant pictures were of mutilated bodies and burn victims, and neutral pictures were of household objects. Picture selection was based on published valence and arousal ratings for male participants (Lang et al., 1999). In addition to the pictures from the IAPS, pictures of faces, six happy and six angry, were selected from the Pictures of Facial Affect (Ekman & Friesen, 1976) to represent two emotions of clearly different valence. These faces were selected on the basis of reliability ratings for the Table 1 Injury Characteristics of Participants With Traumatic Brain Injury Participant Time since injury (years) PTA (days) emotion depicted (Ekman & Friesen, 1976), and one of each type was presented in each block of trials. Because these faces did not affect startle amplitude in either group, the data are not presented. Pictures were presented on an in. PC Direct computer monitor (PC Direct, Sydney, Australia). Picture presentation was computer controlled, with pictures conveyed to the participant s monitor via a Coulbourn real-world interface (V19-91) and Coulbourn video splitter (VGA Switchable VGA Video Splitter). The startle stimulus was presented following five pictures from each category; the other picture from each category was a filler, with no startle stimulus presented. Physiological Recording Brain injuries 1. P.H Injuries reported in right hemisphere. 2. J.C Left extradural hematoma, tube through frontal lobe. Left side skull fracture. 3. L.M Subarachnial hemorrhage and intracerebral hematoma in right ventricular trigone. 4. H.T Right subdural hematoma. Right temporal craniotomy, partial temporal lobectomy. 5. J.J Injuries reported in right hemisphere. 6. A.Z Right temporal encephalomacia, right frontal low-density extradural collection. 7. A.S Right parietal contusion. 8. D.B Left anterior frontal lobe hematoma. 9. J.R Right temporal extradural hematoma and contusion. Bilateral frontal contusions, subarachnoid hemorrhage. 10. E.K. 2 1 Bilateral subarachnoid space in temporal poles. Right frontal contusion. 11. W.K Left parieto-occipital subdural hematoma. Midline shift, partial collapse of left lateral ventricle. 12. J.J Right temporal and right frontal hematomas. 13. J.M Left frontal contusion. Note. Recent brain scan information was not available; descriptions of brain injuries were based on computed tomography scan results at time of first hospital admission and from information taken from clinical notes. As such, these descriptions may not be an accurate reflection of the brain regions suffering sustained damage. PTA posttraumatic amnesia. The eyeblink component of the startle reflex was recorded electromyographically from the orbicularis oculi muscle beneath the left eye, using two Ag/AgCl electrodes with sensor diameters of 4 mm. A ground electrode was attached to the forehead. Skin sites were prepared with Nuprep abrasive gel to reduce impedance. Electrode placement followed recommendations of Fridlund and Cacioppo (1986). Electrodes were filled with Microlyte electrode gel and attached with adhesive collars. The raw EMG signal was amplified by 50,000 and bandpass filtered at 90 1,000 Hz using a Coulbourn isolated bioamplifier (V75-04). The amplified signal was then rectified and integrated using a Coulbourn multifunction integrator (V76-

4 EMOTIONAL EXPERIENCE AND THE STARTLE REFLEX IN TBI A) with a time constant of 10 ms, as recommended by Berg and Balaban (1999). Digital sampling occurred at 1,000 Hz for 200 ms after the onset of each startle stimulus. Valence and Arousal Ratings Participants gave an average rating for the six pictures from each category separately on 9-point scales for valence and arousal. The valence scale was rated from very unpleasant (1) to very pleasant (9). The arousal scale was rated from not very arousing (1) to very arousing (9). These scales were developed as a verbal version of the pictorial-based Self- Assessment Manikin (SAM; Lang, 1980, cited in Lang, Bradley, & Cuthbert, 1997). This modification was used to take into account difficulties within the TBI population in understanding depictions of facial affect (e.g., Jackson & Moffat, 1987). Procedure On arriving at the laboratory, the participant was seated in a small room and briefed about the experimental procedure. Informed consent was obtained, and the participant was given the opportunity to voice any questions or concerns. After the electrodes were attached, an equipment test was undertaken and a stabilization period of 10 min allowed. Participants were instructed that they would see a series of pictures varying in emotional content and were asked to view each picture for the entire presentation time. Participants were informed they would hear occasional brief loud noises over the headphones but were instructed to ignore these noises. Finally, participants were asked to keep their head and body still throughout the study, as movement would interfere with the recordings. Electrode leads were secured with tape to reduce electrode movement. The experimenter exited the room for the picture viewing period (14 min). Thirty pictures six from the three categories of pleasant, unpleasant, and neutral, as well as the six happy and six angry faces were presented in five blocks, with each block containing one picture from each category as well as a filler picture (i.e., six pictures). The order of picture presentation was counterbalanced across blocks and was the same for all participants. Each picture was presented for 7 9 s with a random s intertrial interval (mean intertrial interval was 20 s). The startle probe was presented 3 5 s following picture onset (except for filler pictures). A period of s separated each block of pictures. After physiological testing was completed, the electrodes were removed. Participants were then presented with cards each depicting the six pictures from one of the categories (e.g., pleasant, unpleasant, and neutral). Participants were asked to rate the pictures for valence and arousal. Verbal instructions were standardized across participants. Participants were then debriefed regarding the aims and hypotheses of the study and thanked for their time. Data Reduction and Analysis Eyeblink amplitude and latency were computer scored. The primary startle response was defined as the amplitude of the eyeblink that occurred ms after startle probe onset. This was calculated as the peak EMG amplitude (maximum integrated EMG activity) during the ms period after startle probe onset relative to the average amount of integrated EMG activity in the first 20 ms after probe onset. Eyeblink amplitude was used to index affective modulation of startle. In accordance with past research (Cook, Hawk, Davis, & Stevenson, 1991), eyeblink latency was used as a measure of attention and was defined as the duration between startle probe onset and peak EMG. Following data collection, eyeblink amplitude and latency values were manually reviewed. Trials with excessive EMG activity during the first 20 ms following startle probe were rejected. Fewer than 0.01% of the trials were discarded. A repeated measures analysis of variance revealed a significant linear decrease in peak startle amplitude over the five stimulus blocks, F(4, 35) 21.63, p.01, 2.38, suggesting a significant effect of habituation to the startle probe over time that was similar for both groups (i.e., there was no Group Stimulus Block interaction; see Figure 1). Eyeblink responses were z-transformed within-subjects to control for individual differences. Responses were standardized across all picture categories within each stimulus block to control for the habituation effect noted above. No standardized blink responses were more than 2 standard deviations above the mean. Eyeblink response data were analyzed using repeated measures analyses of variance, with participant group (TBI vs. control) as a between-subjects variable and picture category as a within-subject variable averaged across blocks. Planned contrasts tested the pattern of participants eyeblink response while viewing different picture categories. Analogous analyses were conducted for eyeblink latency data and for subjective ratings of valence and arousal. Correlational analyses between valence ratings and eyeblink amplitude, latencies, and arousal ratings were conducted using Spearman s correlation coefficient. Results Affective Modulation of Startle The pattern of startle modulation obtained across the various picture categories for control and TBI participants is depicted in Figure 2. As illustrated, control participants appeared to show a pattern of EMG responses consistent with the linear trend often reported in the literature (pleasant neutral unpleasant). In contrast, TBI participants showed a nonlinear pattern. In particular, responses of the TBI participants to both pleasant and unpleasant pictures were attenuated. Surprisingly, responses of the TBI participants were actually greatest when viewing neutral, household objects. Because of this unusual and unexplained result, the statistical analyses focused on a comparison of pleasant with unpleasant pictures in TBI and control participants. Pleasant and Unpleasant Pictures TBI participants differed from controls in the magnitude of their eyeblink response when viewing pleasant versus unpleasant pictures, as evidenced by a significant Group Picture interaction, F(1, 35) 4.87, p.04, That is, control participants exhibited an attenuation of the startle eyeblink response while viewing pleasant pictures and a potentiation of the response while viewing unpleasant pictures, and TBI participants demonstrated an attenuated startle eyeblink while viewing both pleasant and un- Raw EMG response (µv) Stimulus block TBI Control Figure 1. Habituation to startle across stimulus block for participants with traumatic brain injury (TBI; n 13) and control participants (n 24). EMG electromyogram.

5 228 SAUNDERS, MCDONALD, AND RICHARDSON Eyeblink response (standardized) pleasant pictures. Examination of 95% confidence intervals for the group means indicated a significant difference between the groups on their response to negative items but not positive items. Eyeblink Latency TBI participants were significantly slower to reach peak eyeblink response when viewing both positive and negative pictures than were control participants, F(1, 35) 8.30, p.01, Latency to respond did not differ as a function of the foreground stimuli. The Group Picture interaction was not significant either. Subjective Ratings Subjective ratings of stimuli, summarized in Table 2, generally confirmed the a priori classifications of stimuli. Valence Ratings Both groups rated pleasant pictures as more pleasant than neutral pictures, F(1, 33) 71.64, p.01, Unpleasant pictures were rated as less pleasant than neutral pictures, F(1, 33) , p.01, There was, however, a significant Group Picture interaction, F(1, 33) 6.69, p.02, Inspection of 95% confidence intervals around group means indicated that TBI participants rated pleasant scenes as more pleasant than controls but rated neutral pictures similarly. There were no other significant Group Picture interactions. Arousal Ratings Control Both TBI and control groups rated pleasant and unpleasant pictures as significantly more arousing than neutral pictures, F(1, 33) , p.01, 2.86, and F(1, 33) 37.80, p.01, 2.53, respectively. However, the pattern of arousal ratings differed between TBI and control participants for unpleasant pictures, as evidenced by a significant Group Picture interaction, F(1, 33) 4.69, p.04, Inspection of 95% confidence intervals around cell means revealed that although there was no difference between TBI and control participants in their ratings of TBI Pleasant Neutral Unpleasant Figure 2. Modulation of startle while viewing pleasant, neutral, and unpleasant pictures for control participants (n 24) and participants with traumatic brain injury (TBI; n 13). neutral pictures, TBI participants rated negative pictures as less arousing than did control participants. There were no significant Group Picture interactions for pleasant pictures. Normative Comparisons of Valence and Arousal Ratings Mean valence and arousal ratings obtained from control and TBI participants in the current study were compared with valence and arousal ratings reported by Lang and colleagues (1999) for the same pictures. With few exceptions, valence and arousal ratings were very similar in the current study to those found in the normative sample, as illustrated in Table 2. One-sample t tests revealed that the pleasant pictures were not judged as arousing or as pleasant by control participants in the current study compared with ratings obtained by Lang and colleagues, t(21) 3.34, p.01, and t(21) 4.60, p.01, for arousal and valence, respectively. In spite of this, the present control participants evidenced significant blink attenuation to pleasant pictures. There was no significant difference between the ratings the TBI participants gave for pleasant pictures and those obtained by Lang et al. (1999). TBI participants rated the unpleasant pictures as less arousing than the controls reported by Lang and colleagues, t(12) 2.60, p.03. These differences must be interpreted with some caution, however, as the measure used to assess valence and arousal ratings in the current study was a verbal version of the picture-based SAM used by Lang and colleagues. Differences in sample size may also account for variations. Correlational Analyses There were no significant Spearman correlations between subjective valence ratings and eyeblink peak, latency, or subjective arousal ratings within either the TBI or the control group. Nor was there any correlation between severity of injury (as indexed by length of posttraumatic amnesia) and any startle or subjective rating variable. Table 2 Valence and Arousal Ratings for the Current Study Compared With SAM Ratings Obtained by Lang and Colleagues (1999) for Men: Mean and Standard Deviation for Each Picture Category Picture category and rating Current controls Current TBIs Lang et al. (1999) Pleasant (erotic couples) Valence 6.71 (1.26) a 7.82 (1.34) 7.95 (1.27) Arousal 6.26 (1.56) a 7.34 (1.46) 7.37 (1.69) Unpleasant (mutilated bodies) Valence 1.80 (0.96) 1.59 (0.75) 1.79 (1.30) Arousal 6.75 (2.25) 4.29 (3.37) a 6.72 (2.24) Neutral (household objects) Valence 4.87 (1.23) 4.36 (1.03) 4.80 (1.01) Arousal 2.12 (1.51) 2.08 (1.70) 1.96 (1.48) Note. Standard deviations are in parentheses. The range of scores for these ratings is 1 9, where 1 is the lowest rating of arousal/pleasantness and 9 is the highest. SAM Self-Assessment Manikin; TBI traumatic brain injury. a Significant ( p.05) two-tailed t test between current ratings and Lang et al. s (1999) ratings.

6 EMOTIONAL EXPERIENCE AND THE STARTLE REFLEX IN TBI 229 Discussion The primary intent of this study was to examine the impact of TBI on the modulation of the acoustic startle response by emotional pictures. As hypothesized, TBI participants did not evidence the pattern of startle modulation observed in the control group. Although pleasant pictures produced the usual attenuation of the eyeblink startle response, unpleasant pictures failed to induce the usual potentiation of the response. Indeed, unpleasant pictures also attenuated the startle response in the TBI participants. In addition, TBI participants exhibited a marked and unanticipated potentiated response while viewing neutral household objects. In comparison, and consistent with previous findings, control participants startle response increased linearly across pleasant, neutral, and unpleasant pictures. Subjective ratings of stimulus valence were equivalent across both participant groups, with the exception that TBI participants rated pleasant pictures as more highly pleasant compared with control participants. Although all participants found affective pictures more arousing than neutral pictures, TBI participants found unpleasant scenes significantly less arousing than did controls. These findings are consistent with predictions based on the hypothesis that people with TBI have abnormal affective responsivity, that is, motivational priming, to aversive stimuli. However, there are other explanations that need to be considered before accepting this account. First, lack of potentiation of the startle response in the context of negative stimuli may have reflected a different baseline of responding in the TBI group. In the current study, raw EMG responses in the TBI group were lower overall than those in the control group; similar EMG baseline levels have been reported with other brain-injured populations (temporal lobectomy patients: Buchanan et al., 2004; patients with amygdala lesion: Funayama et al., 2001). The modulatory effects of pleasant and unpleasant stimuli may not be easily detected when baseline EMG responses are so low. Thus, it may be that the current results reflect a failure to detect potentiation in startle rather than an impairment in the TBI participants ability to demonstrate potentiated startle. However, low baseline EMG responses should dampen all startle modulation, and modulation of startle per se was not impaired in the TBI group, as evidenced by a significant habituation effect across the five trial blocks (as well as unusual potentiation during exposure to neutral stimuli). Given that genuine differences in startle were observed, the question must be raised as to whether some mechanism other than affect, such as attention, may account for the findings. For example, according to attentional accounts of startle modulation (e.g., Anthony & Graham, 1985), foreground stimuli influence the startle response according to whether they share the same sensory modality. If the probe is in a different modality to the foreground stimuli, fewer resources are available to process the probe, and the eyeblink response is attenuated. Using an attentional account, it could be argued that the neutral household objects were easily discerned but failed to sustain the TBI participants interest, increasing attentional capacity for the acoustic probe (thus potentiating the startle response). In contrast, pleasant pictures were reasonably simple to discern but absorbed the TBI participants interest, reducing attentional resources for the acoustic probe. The unpleasant pictures mutilated bodies by their very nature were not instantly recognizable and therefore may have required effort to decipher them, also leaving few attentional resources for the acoustic probe. Although an attentional account could thus explain the pattern of modulation observed in the TBI group, it does not accord with the subjective ratings. TBI participants rated the unpleasant pictures as less arousing than pleasant stimuli. It does not seem likely that these participants would direct their attentional resources toward stimuli they found unarousing. Further, given the prevalence of disorders of sustained attention in the TBI population, it seems unlikely that these participants would direct attention toward stimuli that were difficult to decipher. On the contrary, they would be more likely to lose interest in pictures that required substantial attentional resources to encode. Eyeblink latency is thought to be a measure of attention on the basis that an individual s eyeblink latencies are shorter when viewing more interesting (arousing) pictures (Cook et al., 1991). Yet eyeblink latency did not differ across pleasant or unpleasant or, indeed, the neutral picture categories for either the TBI or control groups. In sum, although the attention account of startle modulation may explain the responses of TBI participants to pleasant and neutral pictures, it does not accord with the arousal and latency data and does not provide a satisfactory explanation for the startle modulation effects of unpleasant stimuli. However, further research examining the relation between startle modulation effects and conventional measures of attention in the TBI population is warranted. This leaves the motivational priming account of startle modulation to account for the present results; that is, the lack of potentiation of the eyeblink startle response when TBI participants viewed unpleasant pictures was because the unpleasant stimuli failed to arouse an aversive affective reaction in this group. The TBI participants lowered subjective ratings of arousal for unpleasant stimuli support this view. Indeed, previous studies have reported that unarousing negative pictures tend to attenuate rather than potentiate startle (see Lang, 1995). Thus, the findings of this study are consistent with the position that TBI impairs neural structures and pathways important for the aversive defensive motivational system, thus affecting reactivity to unpleasant stimuli. That is, the process of defensive priming that normally causes startle potentiation is impaired following TBI. In contrast, TBI did not appear to disrupt the attenuating effects of pleasant material on the startle response. Thus, the results of this study lend partial support to the notion that the aversive and appetitive motivational systems involved in startle modulation have different neural bases. The current data do not directly address the question of which particular neural areas mediate affective modulation of the startle response. The TBI population, in general, is heterogeneous in terms of location and severity of injury, though it is clear that aspects of the frontal and temporal lobes (including important limbic structures such as the amygdala) are particularly vulnerable to damage. Previous findings suggest that the anteromedial temporal lobe is necessary for potentiation of the startle reflex by unpleasant emotional experience (Buchanan et al., 2004; Funayama et al., 2001). Further specification of the neural structures critical for startle potentiation may be found by comparing the TBI pattern of results with those from other clinical populations.

7 230 SAUNDERS, MCDONALD, AND RICHARDSON Conclusion In sum, control participants demonstrated the linear pattern of startle modulation to pleasant and unpleasant stimuli that has often been reported in the literature. In contrast, TBI participants failed to show startle potentiation when viewing unpleasant pictures, though pleasant pictures attenuated their startle response. TBI participants gave similar valence ratings to unpleasant pictures as did controls but rated these pictures as significantly less arousing compared with controls. Though other accounts for the current findings cannot entirely be ruled out, the most parsimonious explanation for the lack of potentiation of the startle response when an individual views unpleasant pictures as well as low arousal ratings for these pictures is that TBI disrupts neural pathways critical for the aversive motivational system. Previous research has demonstrated deficits in emotion following TBI, for example impaired perception of emotional facial expressions (Hopkins et al., 2002; Jackson & Moffat, 1987), impaired feelings of emotion (Croker & McDonald, 2005; Hornak et al., 1996), and physiological hyporesponsivity to emotional stimuli (Hopkins et al., 2002). Furthermore, these studies have provided preliminary evidence that TBI differentially impairs negative emotion. The current study corroborated this view of differential impairment in response to negative emotions by demonstrating abnormal startle modulation to negatively valenced pictures in contrast to the normal modulation observed when an individual views pleasant pictures. Further investigations are necessary to establish the neural bases underlying this differential impairment and to further explore the processes involved in startle modulation in this population. References Adolphs, R. (2002). Recognizing emotion from facial expressions: Psychological and neurological mechanisms. Behavioral and Cognitive Neuroscience Reviews, 1, Adolphs, R., Damasio, H., Tranel, D., & Damasio, A. R. (1996). Cortical systems for the recognition of emotion in facial expressions. Journal of Neuroscience, 16, Adolphs, R., Tranel, D., Damasio, H., & Damasio, A. (1995). Fear and the human amygdala. Journal of Neuroscience, 15, Angrilli, A., Mauri, A., Palomba, D., Flor, H., Birbaumer, N., Sartori, G., & di Paola, F. (1996). Startle reflex and emotion modulation impairment after a right amygdala lesion. Brain, 119, Anthony, B. J., & Graham, F. (1985). Blink reflex modification by selective attention: Evidence for the modulation of automatic processing. Biological Psychology, 21, Berg, W. F., & Balaban, M. T. (1999). Startle elicitation: Stimulus parameters, recording techniques, and quantification. In M. E. Dawson, A. M. Schell, & A. H. Böhmelt (Eds.), Startle modification: Implications for neuroscience, cognitive science, and clinical science (pp ). New York: Cambridge University Press. Borod, J. C. (1992). Interhemispheric and intrahemispheric control of emotion: A focus on unilateral brain damage. Journal of Consulting and Clinical Psychology, 60, Borod, J. C. (1993). Cerebral mechanisms underlying facial, prosodic, and lexical emotional expression: A review of neuropsychological studies and methodological issues. Neuropsychology, 7, Bradley, M. M., Cuthbert, B. N., & Lang, P. J. (1990). Startle reflex modification: Emotion or attention? Psychophysiology, 27, Bradley, M. M., Cuthbert, B. N., & Lang, P. J. (1999). Affect and the startle reflex. In M. E. Dawson, A. M. Schell, & A. H. Böhmelt (Eds.), Startle modification: Implications for neuroscience, cognitive science, and clinical science (pp ). New York: Cambridge University Press. Buchanan, T. W., Tranel, D., & Adolphs, R. (2004). Anteromedial temporal lobe damage blocks startle modulation by fear and disgust. Behavioral Neuroscience, 118, Calder, A. J., Keane, J., Manes, F., Antoun, N., & Young, A. W. (2000). Impaired recognition and experience of disgust following brain injury. Nature Neuroscience, 3, Cook, E. W., III. (1999). Affective individual differences, psychopathology, and startle reflex modification. In M. E. Dawson, A. M. Schell, & A. H. Böhmelt (Eds.), Startle modification: Implications for neuroscience, cognitive science, and clinical science (pp ). New York: Cambridge University Press. Cook, E. W., III, Hawk, L. W., Davis, T. L., & Stevenson, V. E. (1991). Affective individual differences and startle reflex modulation. Journal of Abnormal Psychology, 100, Courville, C. B. (1945). Pathology of the nervous system (2nd ed.). Mountain View, CA: California Pacific Press. Croker, V., & McDonald, S. (2005). Recognition of emotion from facial expression following traumatic brain injury. Brain Injury, 19, Damasio, A. R., Tranel, D., & Damasio, H. (1990). Individuals with sociopathic behavior caused by frontal damage fail to respond autonomically to social stimuli. Behavioural Brain Research, 41, Davidson, R. J., & Irwin, W. (1999). The functional neuroanatomy of emotion and affective style. Trends in Cognitive Science, 3, Davis, M., Walker, D. L., & Lee, Y. (1999). Neurophysiology and neuropharmacology of startle and its affective modulation. In M. E. Dawson, A. M. Schell, & A. H. Böhmelt (Eds.), Startle modification: Implications for neuroscience, cognitive science, and clinical science (pp ). New York: Cambridge University Press. Dimberg, U. (1990). Facial electromyography and emotional reactions. Psychophysiology, 27, Ekman, P., & Friesen, W. (1976). Pictures of facial affect. Palo Alto, CA: Consulting Psychologists Press. Fridlund, A. J., & Cacioppo, J. T. (1986). Guidelines for human electromyographic research. Psychophysiology, 23, Funayama, E. S., Grillon, C., Davis, M., & Phelps, E. A. (2001). A double dissociation in the affective modulation of startle in humans: Effects of unilateral temporal lobectomy. Journal of Cognitive Neuroscience, 13, Gentry, L. R., Godersky, J. C., & Thompson, B. (1988). MR imaging of head trauma: Review of the distribution and radiopathologic features of traumatic lesions. American Journal of Roentgenology, 150, Green, R. E. A., Turner, G. R., & Thompson, W. F. (2004). Deficits in facial emotion perception in adults with recent traumatic brain injury. Neuropsychologia, 42, Grillon, C., & Baas, J. (2003). A review of the modulation of the startle reflex by affective states and its application in psychiatry. Clinical Neurophysiology, 114, Hadley, D. M., Teasdale, G. M., Jenkins, A., Condon, B., MacPherson, P., Patterson, J., & Rowan, J. O. (1988). Magnetic resonance imaging in acute head injury. Clinical Radiology, 39, Hamm, A. O., Cuthbert, B. N., Globisch, J., & Vaitl, D. (1997). Fear and the startle reflex: Blink modulation and autonomic response patterns in animal and mutilation fearful subjects. Psychophysiology, 34, Harmer, C. J., Thilo, K. V., Rothwell, J. C., & Goodwin, G. M. (2001). Transcranial magnetic stimulation of medial-frontal cortex impairs the processing of angry facial expressions. Nature Neuroscience, 4, Hopkins, M. J., Dywan, J., & Segalowitz, J. (2002). Altered electrodermal response to facial expression after closed head injury. Brain Injury, 16,

8 EMOTIONAL EXPERIENCE AND THE STARTLE REFLEX IN TBI 231 Hornak, J., Rolls, E. T., & Wade, D. (1996). Face and voice expression identification in patients with emotional and behavioural changes following ventral frontal lobe damage. Neuropsychologia, 34, Jackson, H. F., & Moffat, N. J. (1987). Impaired emotional recognition following severe head injury. Cortex, 23, Koch, M., Schmid, A., & Schnitzler, H. U. (1996). Pleasure-attenuation of startle is disrupted by lesions of the nucleus accumbens. NeuroReport, 7, Lacey, J. I. (1967). Somatic response patterning and stress: Some revisions of activation theory. In M. H. Appley & R. Trumbull (Eds.), Psychological stress: Issues and research (pp. 4 44). New York: Appleton- Century-Croft. Lang, P. J. (1995). The emotion probe: Studies of motivation and attention. American Psychologist, 50, Lang, P. J., Bradley, M. M., & Cuthbert, B. N. (1990). Emotion, attention, and the startle reflex. Psychological Review, 97, Lang, P. J., Bradley, M. M., & Cuthbert, B. N. (1997). International Affective Picture System (IAPS): Technical manual and affective ratings. Gainesville, FL: Center for Research in Psychophysiology, University of Florida. Lang, P. J., Bradley, M. M., & Cuthbert, B. N. (1999). International Affective Picture System (IAPS): Instruction manual and affective ratings (Tech. Rep. No. A-4). Gainesville, FL: Center for Research in Psychophysiology, University of Florida. LeDoux, J. E. (2000). Emotion circuits in the brain. Annual Review of Neuroscience, 23, Levenston, G. K., Patrick, C. J., Bradley, M. M., & Lang, P. J. (2000). The psychopath as observer: Emotion and attention in picture processing. Journal of Abnormal Psychology, 109, Ley, R. G., & Bryden, M. P. (1979). Hemispheric differences in processing emotions and faces. Brain and Language, 7, Lezak, M. D. (1978). Living with the characterologically altered braininjured patient. Journal of Clinical Psychology, 39, McDonald, S., & Flanagan, S. (2004). Social perception deficits after traumatic brain injury: Interaction between emotion recognition, mentalizing ability, and social communication. Neuropsychology, 18, McDonald, S., Flanagan, S., Rollins, J., & Kinch, J. (2003). TASIT: A new clinical tool for assessing social perception after traumatic brain injury. Journal of Head Trauma Rehabilitation, 18, Milders, M., Fuchs, S., & Crawford, J. R. (2003). Neuropsychological impairments and changes in emotional and social behavior following severe traumatic brain injury. Journal of Clinical and Experimental Neuropsychology, 25, Patrick, C. J., Bradley, M. M., & Lang, P. J. (1993). Emotion in the criminal psychopath: Startle reflex modification. Journal of Abnormal Psychology, 102, Phillips, M. L., Drevets, W. C., Rauch, S. L., & Lane, R. (2003). Neurobiology of emotion perception: I. The neural basis of normal emotion perception. Society of Biological Psychiatry, 54, Prigatano, G. P. (1986). Personality and psychosocial consequences of brain injury. In G. P. Prigatano, D. J. Fordyce, H. K. Zeiner, J. R. Roveche, M. Pepping, & B. Casewood (Eds.), Neuropsychological rehabilitation after brain injury (pp ). Baltimore: Johns Hopkins University Press. Reuter-Lorenz, P., & Davidson, R. J. (1981). Differential contributions of the two cerebral hemispheres to the perception of happy and sad faces. Neuropsychologia, 19, Schlenker, R., Cohen, R., & Hopmann, G. (1995). Affective modulation of the startle reflex in schizophrenic patients. European Archives of Psychiatry and Clinical Neuroscience, 245, Spell, L. A., & Frank, E. (2000). Recognition of nonverbal communication of affect following traumatic brain injury. Journal of Nonverbal Behavior, 24, Tate, R. L., Lulham, J. M., Broe, G. A., Strettles, B., & Pfaff, A. (1989). Psychosocial outcome for the survivors of severe blunt head injury: The results from a consecutive series of 100 patients. Journal of Neurology, Neurosurgery, and Psychiatry, 52, Vanman, E. J., Dawson, M. E., & Brennan, P. A. (1998). Affective reactions in the blink of an eye: Individual differences in subjective experience and physiological responses to emotional stimuli. Personality and Social Psychology Bulletin, 24, Vrana, S. R., Spence, E. L., & Lang, P. J. (1988). The startle probe response: A new measure of emotion? Journal of Abnormal Psychology, 97, Wild, B., Erb, M., & Bartels, M. (2001). Are emotions contagious? Evoked emotions while viewing emotionally expressive faces: Quality, quantity, time course and gender differences. Psychiatry Research, 102, Yeomans, J. S., & Frankland, P. W. (1995). The acoustic startle reflex: Neurons and connections. Brain Research Review, 21, Received May 17, 2005 Revision received August 1, 2005 Accepted August 22, 2005