Pupil Dilation Response Research Articles

Toward a more comprehensive understanding of the impact of masker type and signal-to-noise ratio on the pupillary response while performing a speech-in-noise test

Difficulties arising in everyday speech communication often result from the acoustical environment, which may contain interfering background noise or competing speakers. Thus, listening and understanding speech in noise can be exhausting. Two experiments are presented in the current study that further explored the impact of masker type and Signal-to-Noise Ratio (SNR) on listening effort by means of pupillometry. In both studies, pupillary responses of participants were measured while performing the Danish Hearing in Noise Test (HINT; Nielsen and Dau, 2011). The first experiment aimed to replicate and extend earlier observed effects of noise type and semantic interference on listening effort (Koelewijn et al., 2012). The impact of three different masker types, i.e. a fluctuating noise, a 1-talker masker and a 4-talker masker on listening effort was examined at a fixed speech intelligibility. In a second experiment, effects of SNR on listening effort were examined while presenting the HINT sentences across a broad range of fixed SNRs corresponding to intelligibility scores ranging from 100% to 0% correct performance. A peak pupil dilation (PPD) was calculated and a Growth Curve Analysis (GCA) was performed to examine listening effort involved in speech recognition as a function of SNR. The results of two experiments showed that the pupil dilation response is highly affected by both masker type and SNR when performing the HINT. The PPD was highest, suggesting the highest level of effort, for speech recognition in the presence of the 1-talker masker in comparison to the 4-talker babble and the fluctuating noise masker. However, the disrupting effect of one competing talker disappeared for intelligibly levels around 50%. Furthermore, it was demonstrated that the pupillary response strongly varied as a function of SNRs. Listening effort was highest for intermediate SNRs with performance accuracies ranging between 30% and 70% correct. GCA revealed time-dependent effects of the SNR on the pupillary response that were not reflected in the PPD.

Impact of SNR, masker type and noise reduction processing on sentence recognition performance and listening effort as indicated by the pupil dilation response

Recent studies have shown that activating the noise reduction scheme in hearing aids results in a smaller peak pupil dilation (PPD), indicating reduced listening effort, at 50% and 95% correct sentence recognition with a 4-talker masker. The objective of this study was to measure the effect of the noise reduction scheme (on or off) on PPD and sentence recognition across a wide range of signal-to-noise ratios (SNRs) from +16 dB to −12 dB and two masker types (4-talker and stationary noise). Relatively low PPDs were observed at very low (−12 dB) and very high (+16 dB to +8 dB) SNRs presumably due to ‘giving up’ and ‘easy listening’, respectively. The maximum PPD was observed with SNRs at approximately 50% correct sentence recognition. Sentence recognition with both masker types was significantly improved by the noise reduction scheme, which corresponds to the shift in performance from SNR function at approximately 5 dB toward a lower SNR. This intelligibility effect was accompanied by a corresponding effect on the PPD, shifting the peak by approximately 4 dB toward a lower SNR. In addition, with the 4-talker masker, when the noise reduction scheme was active, the PPD was smaller overall than that when the scheme was inactive. We conclude that with the 4-talker masker, noise reduction scheme processing provides a listening effort benefit in addition to any effect associated with improved intelligibility. Thus, the effect of the noise reduction scheme on listening effort incorporates more than can be explained by intelligibility alone, emphasizing the potential importance of measuring listening effort in addition to traditional speech reception measures.

Can pupillometry index auditory attentional capture in contexts of active visual processing?

ABSTRACTThe rare presentation of a sound that deviates from the auditory background tends to capture attention, which is known to impede cognitive functioning. Such disruption is usually measured using performance on a concurrent visual task. Growing evidence recently showed that the pupillary dilation response (PDR) could index the attentional response triggered by a deviant sound. Given that the pupil diameter is sensitive to several vision-related factors, it is unclear whether the PDR could serve to study attentional capture in such contexts. Hence, the present study aimed at verifying whether the PDR can be used as a proxy for auditory attentional capture while a visual serial recall task (Experiment 1) or a reading comprehension task (Experiment 2) – respectively producing changes in luminance and gaze position – is being performed. Results showed that presenting a deviant sound within steady-state standard sounds elicited larger PDRs than a standard sound. Moreover, the magnitude of these PDRs was positively related to the amount of performance disruption produced by deviant sounds in Experiment 1. Performance remained unaffected by the deviants in Experiment 2, thereby implying that the PDR may be a more sensitive attention-capture index than behavioural measures. These results suggest that the PDR can be used to assess attentional capture by a deviant sound in contexts where the pupil diameter can be modulated by the visual environment.

Emotion lies in the eye of the listener: Emotional arousal to novel sounds is reflected in the sympathetic contribution to the pupil dilation response and the P3

Novel sounds in the auditory oddball paradigm elicit a biphasic dilation of the pupil (PDR) and P3a as well as novelty P3 event-related potentials (ERPs). The biphasic PDR has been hypothesized to reflect the relaxation of the iris sphincter muscle due to parasympathetic inhibition and the constriction of the iris dilator muscle due to sympathetic activation. We measured the PDR and the P3 to neutral and to emotionally arousing negative novels in dark and moderate lighting conditions. By means of principal component analysis (PCA) of the PDR data we extracted two components: the early one was absent in darkness and, thus, presumably reflects parasympathetic inhibition, whereas the late component occurred in darkness and light and presumably reflects sympathetic activation. Importantly, only this sympathetic late component was enhanced for emotionally arousing (as compared to neutral) sounds supporting the hypothesis that emotional arousal specifically activates the sympathetic nervous system. In the ERPs we observed P3a and novelty P3 in response to novel sounds. Both components were enhanced for emotionally arousing (as compared to neutral) novels. Our results demonstrate that sympathetic and parasympathetic contributions to the PDR can be separated and link emotional arousal to sympathetic nervous system activation.

The Pupil Dilation Response During Speech Perception in Dark and Light: The Involvement of the Parasympathetic Nervous System in Listening Effort

Recently, the measurement of the pupil dilation response has been applied in many studies to assess listening effort. Meanwhile, the mechanisms underlying this response are still largely unknown. We present the results of a method that separates the influence of the parasympathetic and sympathetic branches of the autonomic nervous system on the pupil response during speech perception. This is achieved by changing the background illumination level. In darkness, the influence of the parasympathetic nervous system on the pupil response is minimal, whereas in light, there is an additional component from the parasympathetic nervous system. Nineteen hearing-impaired and 27 age-matched normal-hearing listeners performed speech reception threshold tests targeting a 50% correct performance level while pupil responses were recorded. The target speech was masked with a competing talker. The test was conducted twice, once in dark and once in a light condition. Need for Recovery and Checklist Individual Strength questionnaires were acquired as indices of daily-life fatigue. In dark, the peak pupil dilation (PPD) did not differ between the two groups, but in light, the normal-hearing group showed a larger PPD than the hearing-impaired group. Listeners with better hearing acuity showed larger differences in dilation between dark and light. These results indicate a larger effect of parasympathetic inhibition on the pupil dilation response of listeners with better hearing acuity, and a relatively high parasympathetic activity in those with worse hearing. Previously observed differences in PPD between normal and impaired listeners are probably not solely because of differences in listening effort.

Classification of BCI Users Based on Cognition.

Brain-Computer Interfaces (BCI) are systems originally developed to assist paralyzed patients allowing for commands to the computer with brain activities. This study aims to examine cognitive state with an objective, easy-to-use, and easy-to-interpret method utilizing Brain-Computer Interface systems. Seventy healthy participants completed six tasks using a Brain-Computer Interface system and participants' pupil dilation, blink rate, and Galvanic Skin Response (GSR) data were collected simultaneously. Participants filled Nasa-TLX forms following each task and task performances of participants were also measured. Cognitive state clusters were created from the data collected using the K-means method. Taking these clusters and task performances into account, the general cognitive state of each participant was classified as low risk or high risk. Logistic Regression, Decision Tree, and Neural Networks were also used to classify the same data in order to measure the consistency of this classification with other techniques and the method provided a consistency between 87.1% and 100% with other techniques.

Effects of Ketamine on Pupillary Reflex Dilation: A Case Report.

Ketamine is an important component of multimodal treatment and a commonly used anesthetic drug. However, its analgesic effects have not been fully assessed intraoperatively because of difficulties in measuring this effect. In this case report, a woman underwent general anesthesia with ketamine and its pupillary reflexes were measured to detect autonomic changes in response to pain. With increasing doses of ketamine, the pupillary light reflex and the pupillary dilation response decreased. This could be caused by N-methyl-D-aspartate receptor antagonism in the pupillary reflexes pathway or by the analgesic effects of ketamine.

The Pupil Dilation Response to Auditory Stimuli: Current State of Knowledge.

The measurement of cognitive resource allocation during listening, or listening effort, provides valuable insight in the factors influencing auditory processing. In recent years, many studies inside and outside the field of hearing science have measured the pupil response evoked by auditory stimuli. The aim of the current review was to provide an exhaustive overview of these studies. The 146 studies included in this review originated from multiple domains, including hearing science and linguistics, but the review also covers research into motivation, memory, and emotion. The present review provides a unique overview of these studies and is organized according to the components of the Framework for Understanding Effortful Listening. A summary table presents the sample characteristics, an outline of the study design, stimuli, the pupil parameters analyzed, and the main findings of each study. The results indicate that the pupil response is sensitive to various task manipulations as well as interindividual differences. Many of the findings have been replicated. Frequent interactions between the independent factors affecting the pupil response have been reported, which indicates complex processes underlying cognitive resource allocation. This complexity should be taken into account in future studies that should focus more on interindividual differences, also including older participants. This review facilitates the careful design of new studies by indicating the factors that should be controlled for. In conclusion, measuring the pupil dilation response to auditory stimuli has been demonstrated to be sensitive method applicable to numerous research questions. The sensitivity of the measure calls for carefully designed stimuli.

Pain or nociception? Subjective experience mediates the effects of acute noxious heat on autonomic responses

Nociception reliably elicits an autonomic nervous system (ANS) response. Because pain and ANS circuitry interact on multiple spinal, subcortical, and cortical levels, it remains unclear whether autonomic responses are simply a reflexive product of noxious stimulation regardless of how stimulation is consciously perceived or whether the experience of pain mediates ANS responses to noxious stimulation. To test these alternative predictions, we examined the relative contribution of noxious stimulation and individual pain experience to ANS responses in healthy volunteers who underwent 1 or 2 pain assessment tasks. Participants received 8 seconds of thermal stimulation of varied temperatures and judged pain intensity on every trial. Skin conductance responses and pupil dilation responses to stimulation served as measures of the heat-evoked autonomic response. We used multilevel modelling to examine trial-by-trial relationships between heat, pain, and ANS response. Although both pain and noxious heat stimulation predicted skin conductance response and pupil dilation response in separate analyses, the individual pain experience statistically mediated effects of noxious heat on both outcomes. Furthermore, moderated mediation revealed that evidence for this process was stronger when stimulation was perceived as painful compared with when stimulation was perceived as nonpainful. These findings suggest that pain appraisal regulates the heat-evoked autonomic response to noxious stimulation, documenting the flexibility of the autonomic pain response to adjust to perceived or actual changes in environmental affordances above and beyond nociceptive input.

Eyes have ears: Indexing the orienting response to sound using pupillometry

The rare occurrence of a sound deviating from the auditory background tends to trigger attentional orienting. While some sympathetic physiological responses can be used to index this orienting response, findings surrounding the pupillary dilation response (PDR) as a proxy for the orienting response are conflicting. The current study was tailor-designed to examine whether the PDR satisfies specific criteria of an orienting response index, namely the classic habituation pattern and a sensitivity to the size of the deviation. The PDR decrement to a repeated standard sound, recovery to a deviant sound, and dishabituation to the re-presentation of the standard were assessed for small and large deviations embedded in irrelevant auditory sequences. The PDR not only showed habituation and dishabituation, but also recovered in correspondence with the magnitude of the acoustic deviation. This consistency between variations of the PDR and orienting response's properties indicates that the PDR is a valid index of the auditory orienting response.

P 98 Emotional arousal evoked by novel sounds is reflected in increased sympathetic activation – developmental effects, pupil dilation, and the P3a component

Unexpected novel sounds occurring outside the current focus of attention can involuntarily capture attention. The underlying mechanisms can be investigated measuring the pupil dilation response (PDR) and the event-related potential (ERP) component P3a in the EEG (for review see, Wetzel and Schroger, 2014 ). Emotional sounds have a high relevance and might cause a stronger orienting of attention and evaluation for novelty than neutral sounds. Emotional arousal was previously associated with increased sympathetic activity ( Bradley et al., 2008 ). In a first study we tested a current theory on the generation of the P3a that suggests that P3a and the autonomic response reflect the co-activation of the locus coeruleus-norepinephrine system and the peripheral sympathetic nervous system (SNS; Nieuwenhuis et al., 2011 ). We measured the PDR and the P3a while presenting emotional and neutral novel sounds within a sequence of repeated standard sounds (auditory oddball paradigm). In order to dissociate the contributions of the muscles controlled by the parasympathetic and sympathetic nervous system to the PDR we varied the lighting conditions. Results revealed that only the contribution of sympathetic activation but not parasympathetic inhibition as well as the P3a amplitude were enhanced in response to emotional compared to neutral novel sounds supporting the introduced hypothesis. In a second pupillometry study we presented an auditory oddball paradigm including emotional and other distractor sounds to infants and an adult control group. Distractor sounds elicited a biphasic PDR in both age groups. A principal component analysis revealed a significant increase from the faster component (associated with the parasympathetic inhibition) to the slower component (associated with the sympathetic activation) of the PDR in response to emotional distractor sounds in infants only. Results indicate that infants are more sensitive to emotionally high arousing novel sounds than adults. In sum, our results indicate that (1) emotional arousal is reflected in increased sympathetic activation, (2) the P3a is associated with the SNS activation, and (3) there are developmental differences in the response to emotionally arousing distractor sounds. Importantly, the successful dissociation between the parasympathetic and sympathetic contribution to the PDR enables us to study processes of attention and cognition in particular in children, patients, or other populations where pupil diameter can be measured significantly easier than other psychophysiological parameters.

Pupil response and attention skills in Down syndrome

Down syndrome (DS) is characterized by attentional problems. Little is known about the neural correlates of attention problems in DS due to difficulties in evaluation. Pupil dilation, associated with an increase in cognitive load and locus coeruleus-noradrenaline system activity in humans, is a neurophysiological measurement that may help to characterize such problems. The aim of this research was to investigate the link between a phasic pupil dilation response and target detection in people with DS, as compared with a control group with typical development (TD) matched by mental age. Participants performed an “oddball” task by means of an eye-tracker and a series of neuropsychological tests. Although the DS and control group demonstrated similar attentional skills and behavioral performance, the participants with DS showed greater pupil dilation. This result suggests that people with DS expend extra cognitive effort to achieve performance similar to those with TD. This finding is discussed in light of the attentional process in DS and the reliability of pupil dilation measurement in the study of attention and other cognitive processes in DS.

Effects of attention on the speech reception threshold and pupil response of people with impaired and normal hearing

For people with hearing difficulties, following a conversation in a noisy environment requires substantial cognitive processing, which is often perceived as effortful. Recent studies with normal hearing (NH) listeners showed that the pupil dilation response, a measure of cognitive processing load, is affected by ‘attention related’ processes. How these processes affect the pupil dilation response for hearing impaired (HI) listeners remains unknown. Therefore, the current study investigated the effect of auditory attention on various pupil response parameters for 15 NH adults (median age 51 yrs.) and 15 adults with mild to moderate sensorineural hearing loss (median age 52 yrs.). Both groups listened to two different sentences presented simultaneously, one to each ear and partially masked by stationary noise. Participants had to repeat either both sentences or only one, for which they had to divide or focus attention, respectively. When repeating one sentence, the target sentence location (left or right) was either randomized or blocked across trials, which in the latter case allowed for a better spatial focus of attention. The speech-to-noise ratio was adjusted to yield about 50% sentences correct for each task and condition. NH participants had lower (‘better’) speech reception thresholds (SRT) than HI participants. The pupil measures showed no between-group effects, with the exception of a shorter peak latency for HI participants, which indicated a shorter processing time. Both groups showed higher SRTs and a larger pupil dilation response when two sentences were processed instead of one. Additionally, SRTs were higher and dilation responses were larger for both groups when the target location was randomized instead of fixed. We conclude that although HI participants could cope with less noise than the NH group, their ability to focus attention on a single talker, thereby improving SRTs and lowering cognitive processing load, was preserved. Shorter peak latencies could indicate that HI listeners adapt their listening strategy by not processing some information, which reduces processing time and thereby listening effort.

Multisensory integration in orienting behavior: Pupil size, microsaccades, and saccades

Signals from different sensory modalities are integrated in the brain to optimize behavior. Although multisensory integration has been demonstrated in saccadic eye movements, its influence on other orienting responses, including pupil size and microsaccades, is still poorly understood. We examined human gaze orienting responses following presentation of visual, auditory, or combined audiovisual stimuli. Transient pupil dilation and microsaccade inhibition were evoked shortly after the appearance of a salient stimulus. Audiovisual stimuli evoked larger pupil dilation, greater microsaccade inhibition, and faster saccade reaction times compared to unimodal conditions. Trials with faster saccadic reaction times were accompanied with greater pupil dilation responses. Similar modulation of pre-stimulus pupil-size-change rate was observed between stimulus-evoked saccadic and pupillary responses. Thus, multisensory integration impacts multiple components of orienting, with coordination between saccade and pupil responses, implicating the superior colliculus in coordinating these responses because of its central role in both orienting behavior and multisensory integration.

The time course of pupil dilation evoked by visual sexual stimuli: Exploring the underlying ANS mechanisms.

The early processing of visual sexual stimuli shows signs of automaticity. Moreover, there is evidence for sex-specific patterns in cognitive and physiological responding to erotica. However, little is known about the time course of rapid pupillary responses to sexual stimuli and their correspondence with other measures of autonomic activity in women and men. To study pupil dilation as an implicit measure of sexual arousal at various stages of picture processing, we presented 35 heterosexual participants with pictures showing either erotic couples or single (male/female) erotic nudes, contrasted with people involved in everyday situations. Brightness-adjusted grayscale pictures were shown for a duration of 2,500 ms within the central visual field, alternating with perceptually matched patches. Left pupil diameter was recorded at 500 Hz using a video-based eye tracker. Skin conductance and heart rate were coregistered and correlated with latent components of pupil dilation (dissociated by temporal PCA). Whereas stimulus-evoked changes in pupil size indicated virtually no initial constriction, a rapid effect of appetence emerged (dilation to erotica within 500 ms). Responses at early stages of processing were remarkably consistent across both sexes. In contrast, later phases of pupil dilation, subjective ratings, and skin conductance responses showed a sex-specific pattern. Moreover, evidence for an association of early-onset pupil dilation and heart rate acceleration was found, suggestive of parasympathetic inhibition, whereas the late component was mainly related to sympathetically mediated skin conductance. Taken together, our results indicate that different temporal components of pupil responses to erotic stimuli may reflect divergent underlying neural mechanisms.

Functional dissociation of stimulus intensity encoding and predictive coding of pain in the insula.

The computational principles by which the brain creates a painful experience from nociception are still unknown. Classic theories suggest that cortical regions either reflect stimulus intensity or additive effects of intensity and expectations, respectively. By contrast, predictive coding theories provide a unified framework explaining how perception is shaped by the integration of beliefs about the world with mismatches resulting from the comparison of these beliefs against sensory input. Using functional magnetic resonance imaging during a probabilistic heat pain paradigm, we investigated which computations underlie pain perception. Skin conductance, pupil dilation, and anterior insula responses to cued pain stimuli strictly followed the response patterns hypothesized by the predictive coding model, whereas posterior insula encoded stimulus intensity. This novel functional dissociation of pain processing within the insula together with previously observed alterations in chronic pain offer a novel interpretation of aberrant pain processing as disturbed weighting of predictions and prediction errors.

Pupil responses and pain ratings to heat stimuli: Reliability and effects of expectations and a conditioning pain stimulus

BackgroundThe locus coeruleus (LC) signals salience to sensory stimuli and these responses can modulate the experience of pain stimuli. The pupil dilation response (PDR) to noxious stimuli is thought to be a surrogate for LC responses, but PDR response to Peltier-controlled noxious heat stimuli, the most commonly used method in experimental pain research, has not been described. New methodHealthy volunteers were presented with randomly presented heat stimuli of 5 sec duration and provided pain intensity ratings to each stimulus. Pupillometry was performed and a method developed to quantify the PDR relevant to these stimuli. The stimulus response, reliability, and effect of commonly used manipulations on pain experience were explored. ResultsA method of artifact removal and adjusting for lag from stimulus initiation to PDR response was developed, resulting in a close correlation between pain intensity rating and PDR across a large range of heat stimuli. A reliable assessment of PDR within an individual was achieved with fewer presentations as heat stimulus intensity increased. The correlation between pain rating and PDR was disrupted when cognitive load is increased by manipulating expectations or presenting a second pain stimulus. Comparison with existing methodsThe PDR began later after skin heating than electrical stimuli and this is the first examination of the PDR using standard nociceptive testing and manipulations of expectations and competing noxious stimulation. ConclusionsA method is described applying PDR to standard heat nociceptive testing, demonstrating stimulus response, reliability, and disruption by cognitive manipulation.

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.

Gay, Mostly Gay, or Bisexual Leaning Gay? An Exploratory Study Distinguishing Gay Sexual Orientations Among Young Men.

This exploratory study assessed physiological, behavioral, and self-report measures of sexual and romantic indicators of sexual orientation identities among young men (mean age=21.9years) with predominant same-sex sexual and romantic interests: those who described themselves as bisexual leaning gay (n=11), mostly gay (n=17), and gay (n=47). Although they were not significantly distinguishable based on physiological (pupil dilation) responses to nude stimuli, on behavioral and self-report measures a descending linear trend toward the less preferred sex (female) was significant regarding sexual attraction, fantasy, genital contact, infatuation, romantic relationship, sex appeal, and gazing time to the porn stimuli. Results supported a continuum of sexuality with distinct subgroups only for the self-report measure of sexual attraction. The other behavioral and self-report measures followed the same trend but did not significantly differ between the bisexual leaning gay and mostly gay groups, likely the result of small sample size. Results suggest that romantic indicators are as good as sexual measures in assessing sexual orientation and that a succession of logically following groups from bisexual leaning gay, mostly gay, to gay. Whether these three groups are discrete or overlapping needs further research.

Detecting auditory changes by pupillary response

Detecting changes is an essential function that helps the organism to constantly monitor and update the information from the environment. In this talk, I will review our recent work, demonstrating that the human pupillary response can be used as a physiological marker for certain aspects of auditory change detection, in both simple and complex acoustic streams. In study 1, using simple repetitive tones with occasionally presented deviants (oddballs), we found that the oddball induces a pupillary dilation response (PDR), that is modulated by the stimulus properties irrespective of whether attention is directed to the sounds (Liao et al. 2016). In study 2, we examined whether PDR also reflects changes in complex acoustic patterns. We adopted the stimuli in Barascud et al. (2016) which contain transitions between random and regular tone-pip patterns. Results revealed an asymmetry: the PDR was observed only to changes from a regular to a random pattern, but not vice-versa. Overall, the results suggest that th...