Autonomic and neural correlates of dysregulated arousal in severe traumatic brain injury

Severe traumatic brain injury (TBI) in adults is associated with abnormalities in arousal and emotional responsivity, which are observed physiologically, behaviourally and via self-report measures. While an accurate measure of physiological arousal is debated, ,  and  have consistently shown an inverse relationship between skin conductance level (SCL), and mean alpha power (alpha) during an eyes-closed resting condition (EC), accompanied by an increase in SCL and corresponding decrease in alpha during eyes-open (EO). Thus, alpha may provide a novel index of autonomic arousal. This study aimed to elucidate the neural and autonomic correlates of arousal disturbances in TBI.     

Diurnal autonomic variations and emotional reactivity

Diurnal temporal variations of emotional reactivity were investigated in relationship with fluctuations of psychophysiological state, evaluated by tonic autonomic activity. Neutral and unpleasant pictures, selected to constitute seven matched sets, were evaluated by 12 participants during seven sessions in the course of daytime. Skin conductance level (SCL) was recorded at the beginning of each session, whereas skin conductance responses (SCRs), affective evaluation and emotional experience were measured during or after each session. Data show significant temporal variations for SCL, SCRs and emotional experience which follow similar patterns during the daytime. Discussion highlights the role of temporal patterns of autonomic activity as an interesting basis to better understand the emotional regulation and affective disorders.     

Resting physiological arousal is associated with the experience of music-induced chills

In the study of emotion and autonomic nervous system functioning, resting physiological arousal is usually considered a negative characteristic. The present study examined the relationship between resting physiological arousal and positive emotional experience linked to psychophysiological arousal. We assessed resting physiological arousal using markers as high skin conductance level and low respiratory sinus arrhythmia, measured just before participants listened to their favorite music. Participants reported the sensation of chills (goose bumps, shivers) by pressing a mouse button while listening. The results indicated that individuals with resting physiological arousal frequently experience music-induced chills, which evoked unambiguous pleasurable feelings and an increase in skin conductance response. The current results, and the previously demonstrated relationship between resting physiological arousal and negative emotionality linked to psychophysiological arousal (e.g., anxiety, panic), suggest that resting physiological arousal may reflect sensitivity to psychophysiological arousal with both intense positive and negative emotions.     

Oxytocin response in a trust game and habituation of arousal

Oxytocin may be implicated in various sophisticated human processes, including attachment, trust, social perception, memory, and fear regulation. In this study, we explored the relationship between plasma oxytocin level measured after a task requiring intimate trust (secret sharing) and habituation of autonomic arousal (skin conductance response) in sixty healthy volunteers. Results revealed that oxytocin was elevated in the trust-related condition relative to a neutral baseline. In a cognitive stress condition (mental arithmetic task), there was no significant oxytocin elevation relative to the neutral condition. After controlling for age, gender, education, state anxiety and depression, we found a significant positive relationship between trust-related oxytocin level and habituation of autonomic arousal. This relationship was absent in the case of neutral (trust-unrelated) oxytocin level. These results suggest that the habituation of autonomic arousal is closely related to oxytocin released during trust-related social interactions.     

Autonomic arousal explains social cognitive abilities in high-functioning adults with autism spectrum disorder

Empirical research into behavioural profiles and autonomic responsivity in individuals with autism spectrum disorders (ASDs) is highly variable and inconsistent. Two preliminary studies of children with ASDs suggest that there may be subgroups of ASDs depending on their resting arousal levels, and that these subgroups show different profiles of autonomic responsivity. The aim of the present study was to determine whether (i) adults with high-functioning ASDs may be separated into subgroups according to variation in resting arousal; and (ii) these ASD arousal subgroups differ in their behavioural profiles for basic emotion recognition, judgements of trustworthiness, and cognitive and affective empathy. Thirty high-functioning adults with ASDs and 34 non-clinical controls participated. Resting arousal was determined as the average skin conductance (SCL) across a 2 min resting period. There was a subgroup of ASD adults with significantly lower resting SCL. These individuals demonstrated poorer emotion recognition, tended to judge faces more negatively, and had atypical relationships between SCL and affective empathy. In contrast, low cognitive empathy was a feature of all ASD adults. These findings have important implications for clinical interventions and future studies investigating autonomic functioning in ASDs.     

Reliability of psychophysiological assessment within temperament-groups

Four groups of 16 people selected for their relatively extreme scores (greater or equal to 1 S.D. from the mean) on both the E and N scales of the Eysenck Personality Inventory visited the laboratory for four separate but identical testing sessions. Three physiological indices were recorded at each session: heart rate (HR), basal skin conductance level (SCL), and the number of spontaneous skin conductance responses (SCR). Test-retest correlation coefficients were calculated within E x N groups across days. HR and SCR showed moderate to good reliabilities across all groups. The most interesting finding was that SCL was a consistently reliable index for extraverts but not for introverts. Correlations between days were statistically significant for extraverts but not for introverts. A speculative explanation for these results is that SCL is affected by cognitive activity rather than autonomic arousal per se. This study suggests that there are systematic effects of temperament on physiological measures that are important and should not be relegated to error variance.     

The influence of attention and arousal on emotion perception in adults with severe traumatic brain injury

Many people with traumatic brain injury (TBI) have poor emotion recognition, with negative emotions more frequently impaired. They can also display abnormal affective responses to emotionally charged material, however, the mechanisms underpinning such deficits are unclear. This study examined whether affective responsivity can be improved by focusing attention and whether responsivity is associated with perception accuracy. Eighteen adults with moderate-to-severe TBI and 18 control participants viewed facial expressions while skin conductance (SCR) and evoked cardiac deceleration (ECD) (used as indices of orientation) and skin conductance levels (SCL) (used as an index of phasic arousal) were monitored. They viewed two blocks of faces (8 angry and 8 happy per block), passively in the first block and with the instruction to identify the emotional expression in the second. No differences between conditions, emotions or groups were found using SCR. Both groups demonstrated increasing ECD for the attend condition relative to the passive condition. For the passive task the control group showed increasing SCL (sensitisation) over trials when viewing angry faces and decreasing SCL (habituation) to happy faces. No differences between emotions were shown for the TBI group who rapidly habituated to both expressions. For the attend task, there was no evidence of habituation for either expression for either the control or TBI participants. Physiological measures did not correlate to accuracy in recognising emotions. The results suggest that increasing attentional demands improves orientation and emotional engagement (arousal) to emotional faces following TBI. However, the relationship to this and emotion perception accuracy remains unclear.     

What our eyes tell us about feelings: Tracking pupillary responses during emotion regulation processes

Emotion regulation is essential for adaptive behavior and mental health. Strategies applied to alter emotions are known to differ in their impact on psychological and physiological aspects of the emotional response. However, emotion regulation outcome has primarily been assessed via self‐report, and studies comparing regulation strategies with regard to their peripheral physiological mechanisms are limited in number. In the present study, we therefore aimed to investigate the effects of different emotion regulation strategies on pupil dilation, skin conductance responses, and subjective emotional responses. Thirty healthy females were presented with negative and neutral pictures and asked to maintain or up‐ and downregulate their upcoming emotional responses through reappraisal or distraction. Pupil dilation and skin conductance responses were significantly enhanced when viewing negative relative to neutral pictures. For the pupil, this emotional arousal effect manifested specifically late during the pupillary response. In accordance with subjective ratings, increasing negative emotions through reappraisal led to the most prominent pupil size enlargements, whereas no consistent effect for downregulation was found. In contrast, early peak dilations were enhanced in all emotion regulation conditions independent of strategy. Skin conductance responses were not further modulated by emotion regulation. These results indicate that pupil diameter is modulated by emotional arousal, but is initially related to the extent of mental effort required to regulate automatic emotional responses. Our data thus provide first evidence that the pupillary response might comprise two distinct temporal components reflecting cognitive emotion regulation effort on the one hand and emotion regulation success on the other hand.     

Timing of caffeine's impact on autonomic and central nervous system measures: clarification of arousal effects

The timing of caffeine effects on arousal levels was examined. From previous work in our laboratory, an increase in skin conductance level (SCL) was used as the marker of arousal increase, and we sought to identify the timing of this and related effects following caffeine ingestion. A single oral dose of caffeine (250 mg) was used in a randomised double-blind placebo-controlled repeated-measures cross-over study. Eyes-closed resting electroencephalogram (EEG) and autonomic data (SCL, heart rate, respiration rate, and systolic and diastolic blood pressure) during 2 min epochs that commenced every 4 min after ingestion, were analysed. The SCL placebo data were used to identify potential arousal measures prior to examining caffeine effects. Caffeine was associated with increased SCL, increased respiratory rate and a global reduction in alpha power. There were no significant cardiovascular effects of caffeine-induced arousal. These caffeine results are consistent with our recent electrodermal and EEG studies of arousal, and confirm the potential use of caffeine as a simple means of experimentally modifying arousal levels without task-related confounds.     

Physiological blunting during pregnancy extends to induced relaxation

There is accumulating evidence that pregnancy is accompanied by hyporesponsivity to physical, cognitive, and psychological challenges. This study evaluates whether observed autonomic blunting extends to conditions designed to decrease arousal. Physiological and psychological responsivity to an 18-min guided imagery relaxation protocol in healthy pregnant women during the 32nd week of gestation (n = 54) and non-pregnant women (n = 28) was measured. Data collection included heart period (HP), respiratory sinus arrhythmia (RSA), tonic and phasic measures of skin conductance (SCL and NS-SCR), respiratory period (RP), and self-reported psychological relaxation. As expected, responses to the manipulation included increased HP, RSA, and RP and decreased SCL and NS-SCR, followed by post-manipulation recovery. However, responsivity was attenuated for all physiological measures except RP in pregnant women, despite no difference in self-reported psychological relaxation. Findings support non-specific blunting of physiological responsivity during pregnancy.     

Emotional response in patients with frontal brain damage: effects of affective valence and information content

The authors investigated the role of the frontal lobes in the emotional response in 19 patients with brain damage and 23 control subjects. They studied the modulation of the startle blink reflex by affective pictures, and other autonomic responses. Patients showed a dissociation between the startle reflex and the affective valence ratings of the pictures, as a result of a low inhibition of the startle reflex by pleasant pictures. Pictures elicited lower skin conductance responses (SCRs) in patients than in controls, whereas the groups did not differ in the SCRs prompted by less significant acoustic stimuli. The findings point to the frontal lobe as a structure involved in the emotional response and in the physiological emotional arousal related to the complexity of the stimuli.     

The temporal stability of electrodermal variables over a one-year period in patients with recent-onset schizophrenia and in normal subjects

Test-retest stability of electrodermal (EDA) variables indexing both general autonomic arousal (e.g., skin conductance level, number of nonspecific skin conductance responses) and attention to external stimuli (e.g., number of skin conductance orienting responses, electrodermal responder/nonresponder status) was assessed in 71 young, recent-onset schizophrenia patients and 36 demographically matched normal subjects. Significant stability over a 1-year period was found for both patients and normal subjects for most EDA variables and for responder/nonresponder status, with test-retest correlations generally being higher for normal subjects. The lower reliability for patients was not attributable to symptomatic fluctuations during the follow-up period and may reflect poorer arousal regulation among the patients. Among measures of responding to nontask stimuli, a simple count of the number of orienting responses occurring was more stable than was a traditional trials-to-habituation measure.     

A Multiple-Response Evaluation of EMG Biofeedback Performance During Training and Stress-Induction Conditions

The present study evaluated multiple system physiological responding which accompanied EMG biofeedback performance under two conditions—during EMG biofeedback training sessions, and during the utilization of that training in the presence of a stressor. Twelve subjects were randomly assigned to one of two groups: 1) an EMG biofeedback group, or 2) a false-EMG biofeedback group. During the training sessions, significant frontalis EMG decreases were produced by the biofeedback group. This performance was associated with a concomitant decrease in heart rate and respiration rate, but an increase in skin conductance level. The biofeedback group was also able to maintain a low level of EMG activity during a stress-induction procedure. However, this low level of activity did not generalize to other physiological responses. Heart rate and skin conductance levels both increased, which coincided with the subjects' self-report of anxiety during this phase of the study. These data clearly demonstrate that single-system arousal reduction produced by EMG biofeedback training, rather than producing cross-system arousal reduction, produces specificity of a single response change under a stress-inducing situation.     

Respiratory sinus arrhythmia as an index of emotional response in young adults

The relationship between respiratory sinus arrhythmia (RSA) and valence and arousal remains unclear. In the present study, the associations between emotion responses and tonic or task-related changes in RSA were assessed. Specifically, the sensitivities of changes in interbeat interval, RSA, and skin conductance to the valence and arousal values of emotional stimuli were examined. This study also explored the association between tonic RSA and subjective, expressive, and physiological emotional responses. Response measures were collected from 56 adults during baseline and film-viewing periods. Tonic RSA was not significantly related to any of the response measures. Increased skin conductance and decreased RSA were associated with arousal independent of valence. Interbeat interval was related to affective valence and not arousal. These findings suggest that RSA may be a useful adjunct to skin conductance measures in assessing emotional arousal.     

Cognitive flexibility,heart rate variability,and resilience predict fine‐grained regulation of arousal during prolonged threat

Emotion regulation in the ongoing presence of a threat is essential for adaptive behavior. Threatening situations change over time and, as a consequence, require a fine‐tuned, dynamic regulation of arousal to match the current state of the environment. Constructs such as cognitive flexibility, heart rate variability, and resilience have been proposed as resources for adaptive emotion regulation, especially in a moment‐to‐moment fashion. Nevertheless, none of these constructs has been empirically related to the dynamic regulation of arousal as it unfolds over the course of a prolonged threatening episode. Here, we do so by placing participants in a threatening and evolving immersive virtual environment called Room 101, while recording their skin conductance. Subsequently, participants rated their subjective arousal continuously over the course of the experience. Participants who had shown greater cognitive flexibility in a separate task (i.e., fewer task‐switching costs when switching to evaluating the valence of positive stimuli) showed better regulation of physiological arousal (skin conductance level), during less‐threatening phases of Room 101. Individuals with higher trait resilience and individuals with higher resting heart rate variability showed more regulation in terms of their subjective arousal experience. The results indicate that emotional, cognitive, and physiological flexibility support nuanced adaptive regulation of objective and experienced arousal in the ongoing presence of threats. Furthermore, the results indicate that these forms of flexibility differentially affect automatic and objective versus reflective and subjective processes.     

Sympathetic arousal during the processing of dysphoric affect by youths at high and low familial risk for depression

Youths at high risk for depression have been shown to have problems in repairing their own sad mood. Given that sympathetic arousal has been implicated both in the experience and regulation of affect, an atypical pattern of arousal may be one of the factors that contribute to mood repair problems. In the current study, we measured sympathetic arousal of never-depressed youths at high (n = 56) and low (n = 67) familial risk for depression during sad mood induction and instructed mood repair. Sympathetic arousal was indexed by skin conductance level (SCL) and cardiac pre-ejection period (PEP); mood repair outcome was indexed by self-rated affect. High-risk youths demonstrated increased SCL during sadness induction, which persisted during mood repair; low-risk youths evidenced increased SCL only during mood repair. Shortened PEP was evident only among high-risk youths and only during mood repair. Furthermore, shortened PEP during mood induction predicted less successful mood repair in the low-risk but not in the high-risk group. The findings suggest that: (a) depression-prone youths differ from control peers in patterns of sympathetic responses to emotional stimuli, which may impair their ability to relieve sadness, and (b) activation patterns differ across subsystems (SCL vs. PEP) of sympathetic activity, in conjunction with depression risk status.     

Subjective and physiological responses to emotion-eliciting pictures in male schizophrenic patients.

Several studies have shown that schizophrenic patients have difficulties in their ability to recognize emotional facial expressions, whereas other research indicated that they subjectively report the same emotional experience as healthy controls. The purpose of this study was to investigate whether the physiological responses that accompany emotions differ between schizophrenic patients and controls, which would suggest a different basic emotional processing mechanism in these patients. We presented 40 emotion-eliciting pictures to male patients (n=26) and controls (n=21), while measuring heart rate (HR), breathing rate (BR), skin conductance response (SCR) and systolic blood pressure (SBP). Each subject rated each picture for its degree of valence and arousal. Mixed-effects regression models were used to investigate the relationships between the subjective ratings and the physiological responses. In both groups, BR and SCR increased with increasing arousal ratings, suggesting sympathetic activation. The SBP of both groups increased with increases in both the valence and the arousal ratings. However, whereas the patients' HR first decreased with decreasing pleasure ratings and subsequently increased with higher arousal and valence ratings, the HR in the control group was influenced by a complex interaction between valence and arousal ratings. Thus, the schizophrenic patients showed similar relationships between subjective ratings and SCR, BR, and SBP, but a different relationship between subjective ratings and HR compared with the healthy controls.     

Caffeine effects on resting-state arousal in children

From previous work in our laboratory, increases in skin conductance level (SCL), together with global (across-scalp) decreases in electroencephalogram (EEG) alpha power and increases in alpha frequency, are useful indices of arousal increase, and here we sought to identify changes in these indices with caffeine ingestion in children. We explored the effects of a single oral dose of caffeine (80 mg) in a randomised double-blind placebo-controlled repeated-measures cross-over study. Thirty healthy children aged between 8 and 13 years (mean age 10.5 years; 11 females) participated in two sessions, 1 week apart. EEG and SCL from a 3 min eyes-closed epoch, commencing approximately 30 min after ingestion of caffeine or placebo, were examined. Caffeine was associated with increased SCL, and a global reduction in EEG power in the theta and alpha bands, as well as topographically-focused reductions in delta and beta power, and a focal increase in alpha frequency. Only global alpha level demonstrated the expected inverse relationship with SCL in both placebo and caffeine conditions. These results are generally consistent with recent electrodermal and EEG studies of arousal. Together with our previous adult data, they indicate that caffeine can be used to increase arousal in both adults and children, without the potential confounds associated with varying task demands. Caffeine appears useful as a simple tool for manipulating arousal in studies exploring its role in physiological and behavioural functioning. This may be helpful in determining the role of hypothetical arousal anomalies in syndromes such as attention-deficit/hyperactivity disorder.     

Augmenting-Reducing of the Visual Evoked Potential as a Function of Changes in Skin Conductance Level

In the first of two experiments four visual evoked potential (VEP) measures of augmenting-reducing were made consecutively within a single test session on each of 10 student volunteers, on whom palmar skin conductance, taken as an index of arousal, was also monitored continuously. Regression slopes relating VEP amplitude to stimulus intensity for any given individual were found to vary considerably over the session, some subjects changing from augmenting to reducing (or vice versa) during testing. Further analysis of the within-subject data indicated that shifts in augmenting-reducing were related to changes in skin conductance level (SCL) and to the range of SCL over which individuals were operating in relation to the group. Thus, subjects in the high SCL range shifted toward relative reducing as their conductance level increased and those in the low SCL range toward relative augmenting. These effects were exactly replicated in a second experiment using a further 10 subjects and a virtually identical procedure. It was concluded that augmenting-reducing is partly state-dependent, though in a manner which is systematic enough to warrant its further investigation in studies focusing on the dynamic aspects of stimulus modulation.     

Nonlinear relationship between electrodermal activity and heart rate variability in patients with acute schizophrenia

We investigated to what degree tonic skin conductance levels (SCL) and cardiac autonomic dysfunction are interrelated in schizophrenia. Heart rate variability (HRV) and SCL were simultaneously assessed in 18 unmedicated patients and 18 controls matched for age, sex, weight, and smoking habits. For comparison to prior studies, phasic sympathetic skin responses (SPR) were also recorded. Compared to controls, patients had prolonged SPR latency and reduced SPR amplitude with a right-greater-than-left asymmetry, which was inversely correlated with positive symptoms. An autonomic imbalance was reflected in linear and nonlinear measures of HRV and increased SCL. Patients showed a stronger nonlinear association between SCL and heart rate than controls. HRV and SCL findings were strongly affected by group differences in breathing rate. Stronger HRV-SCL coupling in patients may suggest augmented sympathetic modulation in schizophrenia.