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.     

The accessory stimulus effect is mediated by phasic arousal: A pupillometry study

People usually respond faster to a visual stimulus when it is immediately preceded by a task‐irrelevant, auditory accessory stimulus (AS). This AS effect occurs even in choice reaction time tasks, despite the fact that the AS carries no information about the correct response. Researchers often assume that the AS effect is mediated by a phasic arousal burst evoked by the AS, but direct evidence for that assumption is lacking. We conducted a pupillometry study to directly test the phasic arousal hypothesis. Participants carried out a demanding choice reaction time task with accessory stimuli occurring on 25% of the trials. Pupil diameter, a common index of arousal, was measured throughout the task. Standard analyses of task performance and pupil diameter showed that participants exhibited the typical AS effect, and that accessory stimuli evoked a reliable early pupil dilation on top of the more protracted dilation associated with the imperative stimulus. Moreover, regression analyses at the single‐trial level showed that variation in reaction times on AS trials was selectively associated with pupil dilation during the early time window within which the AS had an effect, such that particularly large AS‐evoked dilations were associated with especially fast responses. These results provide the first evidence that the AS effect is mediated by AS‐evoked phasic arousal.     

Effects of intranasal oxytocin on pupil dilation indicate increased salience of socioaffective stimuli

To investigate the mechanisms by which oxytocin improves socioaffective processing, we measured behavioral and pupillometric data during a dynamic facial emotion recognition task. In a double‐blind between‐subjects design, 47 men received either 24 IU intranasal oxytocin (OXT) or a placebo (PLC). Participants in the OXT group recognized all facial expressions at lower intensity levels than did participants in the PLC group. Improved performance was accompanied by increased task‐related pupil dilation, indicating an increased recruitment of attentional resources. We also found increased pupil dilation during the processing of female compared with male faces. This gender‐specific stimulus effect diminished in the OXT group, in which pupil size specifically increased for male faces. Results suggest that improved emotion recognition after OXT treatment might be due to an intensified processing of stimuli that usually do not recruit much attention.     

Manipulating attentional asymmetry affects self-reported arousal

This investigation examined whether manipulating participants' attention toward the left or right visual field would have consequences for mood state. Based on the premise that right parietal activity is related to the arousal dimension of emotion, it was predicted that activating the right parietal region asymmetrically would differentially affect aspects of mood related to arousal. Half of the participants in the experiment completed a leftward-biased attentional orienting task, and half completed a mirror-image rightward-biased task. Consistent with predictions, participants in the left-biased group showed greater changes in self-reported arousal. Results support the notion of bidirectional causal relations between mood and perceptual asymmetries.     

EFFECTS OF A TASK-RELEVANT RESPONSE ON PUPIL SIZE

This experiment examined the effects on pupil size of the relevance of an overt response to a cognitive task. Sixteen Ss were assigned to two experimental groups. In one group Ss were required to judge the pitch equality of tones and, subsequently, indicate their decision by pressing or not pressing a telegraph key. In the other group Ss were required to make the pitch-discriminations, but the key press response was unrelated to the preceding cognitive task. Continuous photographs of each S's pupil were taken during the experiment. Results showed that a small amount of pupillary dilation occurred during the discrimination task in the group where the key press was irrelevant to the pitch-discrimination. In the group where S's behavior indicated task fulfillment, however, a significantly greater increase in pupil size occurred, the amount of dilation being larger when task completion was indicated by the key press response than when fulfillment was indicated by no key press. The findings were discussed in terms of arousal associated with apprehension about evaluation, and muscle tension from anticipation of making the overt response.     

Pupillometry reveals changes in physiological arousal during a sustained listening task

Hearing loss is associated with anecdotal reports of fatigue during periods of sustained listening. However, few studies have attempted to measure changes in arousal, as a potential marker of fatigue, over the course of a sustained listening task. The present study aimed to examine subjective, behavioral, and physiological indices of listening‐related fatigue. Twenty‐four normal‐hearing young adults performed a speech‐picture verification task in different signal‐to‐noise ratios (SNRs) while their pupil size was monitored and response times recorded. Growth curve analysis revealed a significantly steeper linear decrease in pupil size in the more challenging SNR, but only in the second half of the trial block. Changes in pupil dynamics over the course of the more challenging listening condition block suggest a reduction in physiological arousal. Behavioral and self‐report measures did not reveal any differences between listening conditions. This is the first study to show reduced physiological arousal during a sustained listening task, with changes over time consistent with the onset of fatigue.     

Cognitive–emotional hyperarousal in the offspring of parents vulnerable to insomnia: a nuclear family study

Cognitive–emotional hyperarousal is believed to be a predisposing factor for insomnia; however, there is limited information on the association of familial vulnerability to insomnia and cognitive–emotional hyperarousal. The aim of this study was to estimate the heritability of stress‐related insomnia and examine whether parental vulnerability to stress‐related insomnia is associated with cognitive–emotional hyperarousal in their offspring. We studied a volunteer sample of 135 nuclear families comprised of 270 middle‐aged (51.5 ± 5.4 years) fathers and mothers and one of their biological offspring (n = 135, 20.2 ± 1.1 years). We measured vulnerability to stress‐related insomnia (i.e. Ford Insomnia Response to Stress Test: FIRST), perceived stress, depression and anxiety in all participants, and arousability, presleep cognitive and somatic arousal, coping and personality in the offspring. We found a heritability estimate of 29% for FIRST scores. High FIRST parents had three to seven times the odds of having offspring highly vulnerable to stress‐related insomnia. Offspring of high FIRST parents showed higher arousability, presleep cognitive arousal and emotion‐oriented coping. Furthermore, high FIRST mothers contributed to offspring's higher anxiety and lower task‐oriented coping, while high FIRST fathers contributed to offspring's higher presleep somatic arousal and conscientiousness. Vulnerability to stress‐related insomnia is significantly heritable. Parents vulnerable to stress‐related insomnia have offspring with cognitive–emotional hyperarousal who rely upon emotion‐oriented coping. These data give support to the notion that arousability and maladaptive coping are key factors in the aetiology of insomnia.     

Fine‐grained versus categorical: Pupil size differentiates between strategies for spatial working memory performance

Pupillometry provides an accessible option to track working memory processes with high temporal resolution. Several studies showed that pupil size increases with the number of items held in working memory; however, no study has explored whether pupil size also reflects the quality of working memory representations. To address this question, we used a spatial working memory task to investigate the relationship of pupil size with spatial precision of responses and indicators of reliance on generalized spatial categories. We asked 30 participants (15 female, aged 19–31) to remember the position of targets presented at various locations along a hidden radial grid. After a delay, participants indicated the remembered location with a high‐precision joystick providing a parametric measure of trial‐to‐trial accuracy. We recorded participants' pupil dilations continuously during task performance. Results showed a significant relation between pupil dilation during preparation/early encoding and the precision of responses, possibly reflecting the attentional resources devoted to memory encoding. In contrast, pupil dilation at late maintenance and response predicted larger shifts of responses toward prototypical locations, possibly reflecting larger reliance on categorical representation. On an intraindividual level, smaller pupil dilations during encoding predicted larger dilations during late maintenance and response. On an interindividual level, participants relying more on categorical representation also produced larger precision errors. The results confirm the link between pupil size and the quality of spatial working memory representation. They suggest compensatory strategies of spatial working memory performance—loss of precise spatial representation likely increases reliance on generalized spatial categories.     

Arithmetic and algebraic problem solving and resource allocation: The distinct impact of fluid and numerical intelligence

This study investigates cognitive resource allocation dependent on fluid and numerical intelligence in arithmetic/algebraic tasks varying in difficulty. Sixty‐six 11th grade students participated in a mathematical verification paradigm, while pupil dilation as a measure of resource allocation was collected. Students with high fluid intelligence solved the tasks faster and more accurately than those with average fluid intelligence, as did students with high compared to average numerical intelligence. However, fluid intelligence sped up response times only in students with average but not high numerical intelligence. Further, high fluid but not numerical intelligence led to greater task‐related pupil dilation. We assume that fluid intelligence serves as a domain‐general resource that helps to tackle problems for which domain‐specific knowledge (numerical intelligence) is missing. The allocation of this resource can be measured by pupil dilation.     

The influence of stimulus valence on perceptual processing of facial expressions and subsequent response inhibition

The constant interplay between affective processing and cognitive control supports emotion regulation and appropriate social functioning. Even when affective stimuli are processed implicitly, threat-related stimuli are prioritized in the earliest stages of processing; yet, it remains unclear how implicit attention to affect influences subsequent cognitive control functions. The present study evaluated the influence of affective valence on early perceptual processes and subsequent response inhibition in a context where affective properties of the stimuli (facial expressions) were not critical for performing the task. Participants (N = 32) completed an affective stop-signal task (SST) while their scalp EEGs were recorded. The SST assessed response inhibition while participants implicitly attended to happy and afraid facial expressions that were matched for level of arousal. Behavioral performance was measured via response time and accuracy while physiological response was measured via the P100, N170, and N200/P300 ERP components. Decreased gender discrimination accuracy, delayed P100 latency, and more negative N170 amplitude were observed for afraid faces compared to happy faces, suggesting a shift in processing with respect to face valence. However, differences in stopping accuracy or N200/P300 ERP components during response inhibition were not observed, pointing to top-down cognitive processes likely being recruited to override the early automatic response to prioritize threat-related stimuli. Findings highlight that, in this implicit affective attention task, threat-related stimuli are prioritized early during processing, but implicitly attending to differentially valenced stimuli did not modulate subsequent cognitive control functions.     

Probing the psychophysiology of the airways: physical activity, experienced emotion, and facially expressed emotion

This article reviews research on airway reactivity in health and asthma within a psychophysiological context, including the effects of physical activity, emotion induction, and manipulation of facial expression of emotion. Skeletal muscle activation leads to airway dilation, with vagal withdrawal being the most likely mechanism. Emotional arousal, in particular negative affect, leads to airway constriction, with evidence for a vagal pathway in depressive states and ventilatory contributions in positive affect. Laboratory-induced airway responses covary with reports of emotion-induced asthma and with lung function decline during negative mood in the field. Like physical activity, facial expression of emotion leads to airway dilation. However, these effects are small and less consistent in posed emotional expressions. The mechanisms of emotion-induced airway responses and potential benefits of emotional expression in asthma deserve further study.     

Pupil Size and Instructional Set in Recognition and Recall

When Ss were given different pretask instructions prior to engaging in a memory task, pupil size distinguished three phases of cognitive processing. The pretask instructions were formed from the combinations of (a) whether or not S had to perform a rehearsal-interference task prior to a recognition test and (b) whether or not S had to recall the material (digits) after the recognition test. The first phase of cognitive processing indicated by the pupil response was associated with the comprehension of the pretask instructions; there were no differences in amount of dilation for the various instructions during this phase. The second phase was interpreted as a preparedness state; the amount of pupil dilation depended on the type of pretask instruction and the differences in dilation occurred prior to the actual presentation of the material. The third phase was associated with the actual processing of the materials, and the level of dilation and rate of increase were related to the pretask instructions. Pupil size increased more rapidly when S had been given the pretask instruction that recall was required after the recognition test than when only recognition was demanded.     

Time course of attentional bias in anxiety: Emotion and gender specificity

Anxiety is characterized by cognitive biases, including attentional bias to emotional (especially threatening) stimuli. Accounts differ on the time course of attention to threat, but the literature generally confounds emotional valence and arousal and overlooks gender effects, both addressed in the present study. Nonpatients high in self‐reported anxious apprehension, anxious arousal, or neither completed an emotion‐word Stroop task during event‐related potential (ERP) recording. Hypotheses differentiated time course of preferential attention to emotional stimuli. Individuals high in anxious apprehension and anxious arousal showed distinct early ERP evidence of preferential processing of emotionally arousing stimuli along with some evidence for gender differences in processing. Healthy controls showed gender differences at both early and later processing stages. The conjunction of valence, arousal, and gender is critical in the time course of attentional bias.     

Pupillometric investigation into the speed-accuracy trade-off in a visuo-motor aiming task

Convergent lines of evidence suggest that fluctuations in the size of the pupil may be associated with the trade-off between the speed (adrenergic, sympathetic) and accuracy (cholinergic, parasympathetic) of behavior across a variety of task contexts. Here, we explored whether pupil size was related to this trade-off during a visuospatial motor aiming task. Participants were shown visual targets at random locations on a screen and were instructed and incentivized to move a computer mouse-controlled cursor to the center of the targets, either as fast as possible, as accurately as possible, or to strike a balance between the two. Behavioral results showed that these instructions led to typical speed-accuracy trade-off effects on movement reaction times and hit distances to target centers. Pupillometric analyses revealed that movements were faster and less accurate when participants had relatively large baseline pupil sizes, as measured before target onset. Furthermore, trial-evoked pupil dilation was related specifically to a bias toward speed in the trade-off and the speed of the ballistic and error-correction phases of the motor responses such that larger pupils predicted shorter latencies and higher movement speeds. Pupil responses were also associated with performance in a manner that may reflect the combined influence of a number of factors, including the generation of dynamic urgency and an arousal response to negative feedback. Our results generally support a role for pupil-linked arousal in regulating the trade-off between speed and accuracy, while also highlighting how the trial-related pupil response can exhibit multifaceted, temporally discrete associations with behavior.     

Bipolar patients show mood‐congruent biases in sensitivity to facial expressions of emotion when exhibiting depressed symptoms,but not when exhibiting manic symptoms

Introduction?A number of studies have reported mood‐congruent biases in processing facial expressions of emotion in depression and mania. Most of them have failed to establish that mood reliably affects relevant more than irrelevant expressions, or that the effect is specifically mood‐related rather than due to resource or task difficulty artefacts. The aim was to examine, using appropriate statistical methods, whether depressed mood in bipolar patients decreases and manic mood increases sensitivity to facial expressions of happiness and vice versa for facial expressions of negative emotion.

Methods?Sensitivity to facial expression of six basic emotions in bipolar patients when depressed and when manic was compared to closely matched controls.

Results?Mood‐related biases in sensitivity to facial expressions of happiness and of negative affect in general operate in persons with bipolar disorder when depressed. There is little evidence of similar biases in persons with bipolar disorder when manic.

Conclusions?These data show a mood‐congruent bias in sensitivity to facial expressions in bipolar depressed patients.     

Pupillary dilation to simple vs. complex tasks and its relationship to thought disturbance in schizophrenia patients.

Task-evoked pupil dilation is a measure of attentional allocation. Schizophrenia patients have pupil dilation deficits during high cognitive load tasks, which have been attributed to attentional resource deficits. Moreover, this attentional impairment is thought to be linked to cognitive fragmentation and thought disturbance. Previous attempts to associate attentional deficits to thought disturbance have typically measured these domains at distinct times, incorrectly assuming that both are static variables. In this study, we compared the pupil dilation of 24 schizophrenia patients to 15 non-patients during complex (Rorschach blots) vs. simple visual (line drawings) processing tasks while simultaneously assessing their verbal responses for thought disturbance. Schizophrenia patients' dilation to the simple stimuli was similar to the non-patients; however, they demonstrated significantly less dilation to the complex stimuli. Reduced dilation was also significantly correlated with reduced response complexity and more severe thought disorder. The results suggest that, in the face of complex problem-solving situations, greater attentional impairment and cognitive overload in schizophrenia is associated with higher levels of disturbed and impoverished thinking. These findings support the 'resource limitations hypothesis' of schizophrenia and underscore the utility of a simultaneous paradigm when studying the relationship between attentional deficits and thought disturbance.     

Pupil Size, Information Overload, and Performance Differences

As a test of the hypothesis that pupil dilation during performance is partially due to a task related anxiety component, pupillary patterns were measured while subjects (Ss) processed digit strings of various lengths for immediate recall. Information overload resulted in a leveling of the dilation pattern which suggested a momentary suspension of processing effort. In addition, significant correlations were observed between individual differences in pupil size and recall performance.     

Impulsivity and the association between the feedback‐related negativity and performance on an inhibitory control task in young at‐risk children

Identifying neurocognitive processes associated with effective inhibitory control is particularly relevant for individuals at high risk for disruptive behaviors, such as maltreated children. Performance feedback processing during a flanker task was investigated in maltreated preschool‐aged children (N = 67) via an event‐related potential component, the feedback‐related negativity (FRN). The functionality of the FRN in children with high impulsivity was of interest, as impulsivity was associated with an exaggerated FRN in previous research. Results showed that high impulsivity was associated with an exaggerated FRN and greater post‐error slowing. For children with high impulsivity, there was a correlation between the FRN and accuracy, which was not found in children with low impulsivity. This suggests that an exaggerated FRN is particularly important for children with high impulsivity to maintain effective inhibitory control.     

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.     

Covariation of mood and blood pressure during daily activities

The relationship between blood pressure (BP) and self-reported mood states was examined for 49 subjects in their natural environment. Subjects performed their usual activities during a 2-day period and recorded their BP using a semiautomated BP monitor at predetermined intervals. Adjective checklists describing mood states and perceptions of the environment as stressful were completed concurrent with each BP measurement. A correlational analysis of average BP and average mood state ratings was performed along with a paired t-test analysis of mood states associated with high versus low BP. The results show that holding anger in correlated positively with average SBP and negatively with average HR. Neither anger arousal nor the expression of anger arousal was able to distinguish between high and low BP readings. The Type A adjective cluster discriminated between high and low SBP as well as between high and low HR readings. The cluster of negative moods also discriminated between high and low SBP. Perceptions of the environment as hostile and demanding discriminated high versus low SBP and high versus low DBP. The discussion focuses upon the value of repeated-measures designs in examining mood/BP relationships as individuals ambulate in their natural environment.This article is based on the first author's dissertation, which was supervised by the second author and submitted to Virginia Polytechnic Institute and State University in partial fulfillment of the requirements for the doctoral degree.Portions of this article were presented at the 8th Annual Meeting of the Society of Behavioral Medicine, Washington, D.C., 1987.