Somatosensory omissions reveal action-related predictive processing.

The intricate relation between action and somatosensory perception has been studied extensively in the past decades. Generally, a forward model is thought to predict the somatosensory consequences of an action. These models propose that when an action is reliably coupled to a tactile stimulus, unexpected absence of the stimulus should elicit prediction error. Although such omission responses have been demonstrated in the auditory modality, it remains unknown whether this mechanism generalizes across modalities. This study therefore aimed to record action-induced somatosensory omission responses using EEG in humans. Self-paced button presses were coupled to somatosensory stimuli in 88% of trials, allowing a prediction, or in 50% of trials, not allowing a prediction. In the 88% condition, stimulus omission resulted in a neural response consisting of multiple components, as revealed by temporal principal component analysis. The oN1 response suggests similar sensory sources as stimulus-evoked activity, but an origin outside primary cortex. Subsequent oN2 and oP3 responses, as previously observed in the auditory domain, likely reflect modality-unspecific higher order processes. Together, findings straightforwardly demonstrate somatosensory predictions during action and provide evidence for a partially amodal mechanism of prediction error generation.

On the relationship of arousal and attentional distraction by emotional novel sounds.

Unexpected and task-irrelevant sounds can impair performance in a task. It has been shown that highly arousing emotional distractor sounds impaired performance less compared to moderately arousing neutral distractor sounds. The present study tests whether these differential emotion-related distraction effects are directly related to an enhancement of arousal evoked by processing of emotional distractor sounds. We disentangled costs of orienting of attention and benefits of increased arousal levels during the presentation of highly arousing emotional and moderately arousing neutral novel sounds that were embedded in a sequence of repeated standard sounds. We used sound-related pupil dilation responses as a marker of arousal and RTs as a marker of distraction in a visual categorization task in 57 healthy young adults. Multilevel analyses revealed increased RT and increased pupil dilation in response to novel vs. standard sounds. Emotional novel sounds reduced distraction effects on the behavioral level and increased pupil dilation responses compared to neutral novel sounds. Bayes Factors revealed strong evidence against an inverse proportional relationship between behavioral distraction effects and sound-related pupil dilation responses for emotional sounds. Given that the activity of the locus coeruleus has been linked to both changes in pupil diameter and arousal, it may embody an indirect relationship as a common antecedent by the release of norepinephrine into brain networks involved in attention control and control of the pupil. The present study provides new insights into the relation of changes in arousal and attentional distraction during the processing of emotional task-irrelevant novel sounds.

Salient omissions-pupil dilation in response to unexpected omissions of sound and touch.

Introduction: Recent theories describe perception as an inferential process based on internal predictive models adjusted by means of prediction violations (prediction error). To study and demonstrate predictive processing in the brain the use of unexpected stimulus omissions has been suggested as a promising approach as the evoked brain responses are uncontaminated by responses to stimuli. Here, we aimed to investigate the pupil's response to unexpected stimulus omissions in order to better understand surprise and orienting of attention resulting from prediction violation. So far only few studies have used omission in pupillometry research and results have been inconsistent. Methods: This study adapted an EEG paradigm that has been shown to elicit omission responses in auditory and somatosensory modalities. Healthy adults pressed a button at their own pace, which resulted in the presentation of sounds or tactile stimuli in either 88%, 50% or 0% (motor-control) of cases. Pupil size was recorded continuously and averaged to analyze the pupil dilation response associated with each condition. Results: Results revealed that omission responses were observed in both modalities in the 88%-condition compared to motor-control. Similar pupil omission responses were observed between modalities, suggesting modality-unspecific activation of the underlying brain circuits. Discussion: In combination with previous omission studies using EEG, the findings demonstrate predictive models in brain processing and point to the involvement of subcortical structures in the omission response. Our pupillometry approach is especially suitable to study sensory prediction in vulnerable populations within the psychiatric field.

Processing of task-irrelevant sounds during typical everyday activities in children.

Our ability to focus on a task and ignore task-irrelevant stimuli is critical for efficient cognitive functioning. Attention control is especially required in the auditory modality as sound has privileged access to perception and consciousness. Despite this important function, little is known about auditory attention during typical everyday activities in childhood. We investigated the impact of task-irrelevant sounds on attention during three everyday activities - playing a game, reading a book, watching a movie. During these activities, environmental novel sounds were presented within a sequence of standard sounds to 7-8-year-old children and adults. We measured ERPs reflecting early sound processing and attentional orienting and theta power evoked by standard and novel sounds during these activities. Playing a game versus reading or watching reduced early encoding of sounds in children and affected ongoing information processing and attention allocation in both groups. In adults, theta power was reduced during playing at mid-central brain areas. Results show a pattern of immature neuronal mechanisms underlying perception and attention of task-irrelevant sounds in 7-8-year-old children. While the type of activity affected the processing of irrelevant sounds in both groups, early stimulus encoding processes were more sensitive to the type of activities in children.

Attentional control in middle childhood is highly dynamic-Strong initial distraction is followed by advanced attention control.

The ability to shield against distraction while focusing on a task requires the operation of executive functions and is essential for successful learning. We investigated the short-term dynamics of distraction control in a data set of 269 children aged 4-10 years and 51 adults pooled from three studies using multilevel models. Participants performed a visual categorization task while a task-irrelevant sequence of sounds was presented which consisted of frequently repeated standard sounds and rarely interspersed novel sounds. On average, participants responded slower in the categorization task after novel sounds. This distraction effect was more pronounced in children. Throughout the experiment, the initially strong distraction effects declined to the level of adults in the groups of 6- to 10-year-olds. Such a decline was neither observed in the groups of the 4- and 5-year-olds, who consistently showed a high level of distraction, nor in adults, who showed a constantly low level of distraction throughout the experimental session. Results indicate that distraction control is a highly dynamic process that qualitatively and quantitatively differs between age groups. We conclude that the analysis of short-term dynamics provides valuable insights into the development of attention control and might explain inconsistent findings regarding distraction control in middle childhood. In addition, models of attention control need to be refined to account for age-dependent rapid learning mechanisms. Our findings have implications for the design of learning situations and provide an additional source of information for the diagnosis and treatment of children with attention deficit disorders.

The effect of background speech on attentive sound processing: A pupil dilation study.

Listening to task-irrelevant speech while performing a cognitive task can involuntarily deviate our attention and lead to decreases in performance. One explanation for the impairing effect of irrelevant speech is that semantic processing can consume attentional resources. In the present study, we tested this assumption by measuring performance in a non-linguistic attentional task while participants were exposed to meaningful (native) and non-meaningful (foreign) speech. Moreover, based on the tight relation between pupillometry and attentional processes, we also registered changes in pupil diameter size to quantify the effect of meaningfulness upon attentional allocation. To these aims, we recruited 41 native German speakers who had neither received formal instruction in French nor had extensive informal contact with this language. The focal task consisted of an auditory oddball task. Participants performed a duration discrimination task containing frequently repeated standard sounds and rarely presented deviant sounds while a story was read in German or (non-meaningful) French in the background. Our results revealed that, whereas effects of language meaningfulness on attention were not detectable at the behavioural level, participants' pupil dilated more in response to the sounds of the auditory task when background speech was played in non-meaningful French compared to German, independent of sound type. In line with the initial hypothesis, this suggested that semantic processing of the native language required attentional resources, which lead to fewer resources devoted to the processing of the sounds of the focal task. Our results highlight the potential of the pupil dilation response for the investigation of subtle cognitive processes that might not surface when only behaviour is measured.

A tutorial on the use of temporal principal component analysis in developmental ERP research - Opportunities and challenges.

Developmental researchers are often interested in event-related potentials (ERPs). Data-analytic approaches based on the observed ERP suffer from major problems such as arbitrary definition of analysis time windows and regions of interest and the observed ERP being a mixture of latent underlying components. Temporal principal component analysis (PCA) can reduce these problems. However, its application in developmental research comes with the unique challenge that the component structure differs between age groups (so-called measurement non-invariance). Separate PCAs for the groups can cope with this challenge. We demonstrate how to make results from separate PCAs accessible for inferential statistics by re-scaling to original units. This tutorial enables readers with a focus on developmental research to conduct a PCA-based ERP analysis of amplitude differences. We explain the benefits of a PCA-based approach, introduce the PCA model and demonstrate its application to a developmental research question using real-data from a child and an adult group (code and data openly available). Finally, we discuss how to cope with typical challenges during the analysis and name potential limitations such as suboptimal decomposition results, data-driven analysis decisions and latency shifts.

Sound omission related brain responses in children.

Action is an important way for children to learn about the world. Recent theories suggest that action is inherently accompanied by the sensory prediction of its effects. Such predictions can be revealed by rarely omitting the expected sensory consequence of the action, resulting in an omission response that is observable in the EEG. Although prediction errors play an important role in models of learning and development, little is known about omission-related brain responses in children. This study used a motor-auditory omission paradigm, testing a group of 6-8-year-old children and an adult group (N = 31 each). In an identity-specific condition, the sound coupled to the motor action was predictable, while in an identity unspecific condition the sound was unpredictable. Results of a temporal principal component analysis revealed that sound-related brain responses underlying the N1-complex differed considerably between age groups. Despite these developmental differences, omission responses (oN1) were similar between age groups. Two subcomponents of the oN1 were differently affected by specific and unspecific predictions. Results demonstrate that children, independent from the maturation of sound processing mechanisms, can implement specific and unspecific predictions as flexibly as adults. This supports theories that regard action and prediction error as important drivers of cognitive development.

Tablet PC use directly affects children's perception and attention.

Children currently grow up with a marked increase in interactive digital mobile media. To what extent digital media directly modulate children's perception and attention is largely unknown. We investigated the processing of task-irrelevant auditory information while 37 children aged 6;8-9;1-years played the identical card game on a tablet PC or with the experimenter in reality. The sound sequence included repeated standard sounds and occasionally novel sounds. Event-related potentials in the EEG, that reflect sound-related processes of perception and attention, were measured. Sounds evoked increased amplitudes of the ERP components P1, P2 and P3a during the interaction with the tablet PC compared to the human interaction. This indicates enhanced early processing of task-irrelevant information and increased allocation of attention to sounds throughout the interaction with a tablet PC compared to a human partner. Results suggest direct effects of typical situations, where children interact with a tablet PC, on neuronal mechanisms that drive perception and attention in the developing brain. More research into this phenomena is required to make specific suggestions for developing digital interactive learning programs.

Cross-modal predictive processing depends on context rather than local contingencies.

Visual symbols or events may provide predictive information on to-be-expected sound events. When the perceived sound does not confirm the visual prediction, the incongruency response (IR), a prediction error signal of the event-related brain potentials, is elicited. It is unclear whether predictions are derived from lower-level local contingencies (e.g., recent events or repetitions) or from higher-level global rules applied top-down. In a recent study, sound pitch was predicted by a preceding note symbol. IR elicitation was confined to the condition where one of two sounds was presented more frequently and was not present with equal probability of both sounds. These findings suggest that local repetitions support predictive cross-modal processing. On the other hand, IR has also been observed with equal stimulus probabilities, where visual patterns predicted the upcoming sound sequence. This suggests the application of global rules. Here, we investigated the influence of stimulus repetition on the elicitation of the IR by presenting identical trial trains of a particular visual note symbol cueing a particular sound resulting either in a congruent or an incongruent pair. Trains of four different lengths: 1, 2, 4, or 7 were presented. The IR was observed already after a single presentation of a congruent visual-cue-sound combination and did not change in amplitude as trial train length increased. We conclude that higher-level associations applied in a top-down manner are involved in elicitation of the prediction error signal reflected by the IR, independent from local contingencies.

Distraction of attention by novel sounds in children declines fast.

New task-irrelevant sounds can distract attention. This study specifies the impact of stimulus novelty and of learning on attention control in three groups of children aged 6-7, 8, and 9-10 years and an adult control group. Participants (N = 179) were instructed to ignore a sound sequence including standard sounds and novel or repeated distractor sounds, while performing a visual categorization task. Distractor sounds impaired performance in children more than in adult controls, demonstrating the long-term development of attention control. Children, but not adults, were more distracted by novel than by repeated sounds, indicating increased sensitivity to novel information. Children, in particular younger children, were highly distracted during the first presentations of novel sounds compared to adults, while no age differences were observed for the last presentations. Results highlight the age-related impact of auditory novel information on attention and characterize the rapid development of attention control mechanisms as a function of age and exposure to irrelevant novel sounds.

Comparison of Pupil Dilation Responses to Unexpected Sounds in Monkeys and Humans.

Pupil dilation in response to unexpected stimuli has been well documented in human as well as in non-human primates; however, this phenomenon has not been systematically compared between the species. This analogy is also crucial for the role of non-human primates as an animal model to investigate neural mechanisms underlying the processing of unexpected stimuli and their evoked pupil dilation response. To assess this qualitatively, we used an auditory oddball paradigm in which we presented subjects a sequence of the same sounds followed by occasional deviants while we measured their evoked pupil dilation response (PDR). We used deviants (a frequency deviant, a pink noise burst, a monkey vocalization and a whistle sound) which differed in the spectral composition and in their ability to induce arousal from the standard. Most deviants elicited a significant pupil dilation in both species with decreased peak latency and increased peak amplitude in monkeys compared to humans. A temporal Principal Component Analysis (PCA) revealed two components underlying the PDRs in both species. The early component is likely associated to the parasympathetic nervous system and the late component to the sympathetic nervous system, respectively. Taken together, the present study demonstrates a qualitative similarity between PDRs to unexpected auditory stimuli in macaque and human subjects suggesting that macaques can be a suitable model for investigating the neuronal bases of pupil dilation. However, the quantitative differences in PDRs between species need to be investigated in further comparative studies.

The impact of novelty and emotion on attention-related neuronal and pupil responses in children.

Focusing on relevant and ignoring irrelevant information is essential for many learning processes. The present study investigated attention-related brain activity and pupil dilation responses, evoked by task-irrelevant emotional novel sounds. In the framework of current theories about the relation between attention and the locus coeruleus-norepinephrine (LC-NE) system, we simultaneously registered event-related potentials (ERPs) in the EEG and changes in pupil diameter (PDR). Unexpected emotional negative and neutral environmental novel sounds were presented within a sequence of repeated standard sounds to 7-10-year-old children and to adults, while participants focused on a visual task. Novel sounds evoked distinctive ERP components, reflecting attention processes and a biphasic PDR in both age groups. Amplitudes of the novel-minus-standard ERPs were increased in children compared to adults, indicating immature neuronal basis of auditory attention in middle childhood. Emotional versus neutral novel sounds evoked increased responses in the ERPs and in the PDR in both age groups. This demonstrates the increased impact of emotional sounds on attention mechanisms and indicates an advanced level of emotional information processing in children. The similar pattern of novel-related PDR and ERPs is conforming to recent theories, emphasizing the role of the LC-NE system in attention processes adding a developmental perspective.

Omission related brain responses reflect specific and unspecific action-effect couplings.

When an auditory stimulus is predicted but unexpectedly omitted, an omission response can be observed in the EEG. This endogenous response to the absence of a stimulus demonstrates the important role of prediction in perception. SanMiguel et al. (2013a) showed that in order to observe an omission response, a specific prediction concerning the identity of an upcoming stimulus is necessary. They used button presses coupled to either a single sound (predictable identity), or a random sound (unpredictable identity). In the event-related potentials, a sequence of omission responses consisting of oN1, oN2, and oP3 was observed in the single condition but not in the random condition. Given the importance of omission studies to understand the role of prediction in perception, we replicated this study. We enhanced statistical power by doubling the sample size and adjusting data pre-processing, and applied temporal principal component analysis and replication Bayes statistics. Results in the single sound condition were successfully replicated. Principal component analysis additionally revealed attenuated oN1 and oP3 omission responses in the random sound condition. These results suggest the existence of both specific and unspecific predictions along the sound processing hierarchy, where precision weighting possibly influences the strength of prediction error. Results are discussed in the framework of predictive coding and are congruent with everyday life, where uncertainty often requires broader or more general predictions.

Picture-evoked changes in pupil size predict learning success in children.

Episodic memory, the ability to remember past events in time and place, develops during childhood. Much knowledge about the underlying neuronal mechanisms has been gained from methods not suitable for children. We applied pupillometry to study memory encoding and recognition mechanisms. Children aged 8 and 9 years (n = 24) and adults (n = 24) studied a set of visual scenes to later distinguish them from new pictures. Children performed worse than adults, demonstrating immature episodic memory. During memorization, picture-related changes in pupil diameter predicted later successful recognition. This prediction effect was also observed on a single-trial level. During retrieval, novel pictures showed stronger pupil constriction than familiar pictures in both age groups. The statistically independent effects of objective familiarity (previously presented pictures) versus subjective familiarity (pictures evaluated as familiar independent of the prior presentation) suggest dissociable underlying brain mechanisms. In addition, we isolated principal components of the picture-related pupil response that were differently affected by the memorization and retrieval effects. Results are discussed in the context of the maturation of the medial temporal lobe and prefrontal networks. Our results demonstrate the dissociation of distinct contributions to episodic memory with a psychophysiological method that is suitable for a wide age spectrum.

Can't Ignore-Distraction by Task-Irrelevant Sounds in Early and Middle Childhood.

Attention control abilities are relevant for learning success. Little is known about the development of audio-visual attention in early childhood. Four groups of children between the ages of 4 and 10 years and adults performed an audio-visual distraction paradigm (N = 106). Multilevel analyses revealed increased reaction times in a visual categorization task when task-irrelevant novel sounds were presented, demonstrating involuntary distraction of attention. This distraction effect decreased with age and significantly differed between age groups. In addition, the two youngest age groups responded with a delay in trials following a distractor trial, indicating delayed reallocation of attention to the task at hand. Results indicate a significant maturation of audio-visual attention control within a few years during early childhood that continues throughout middle childhood.

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.

Infants' and adults' looking behavior does not indicate perceptual distraction for constrained modelled actions - An eye-tracking study.

When observing a novel action, infants pay attention to the model's constraints when deciding whether to imitate this action or not. Gergely et al. (2002) found that more 14-month-olds copied a model's use of her head to operate a lamp when she used her head while her hands were free than when she had to use this means because it was the only means available to her (i.e., her hands were occupied). The perceptional distraction account (Beisert et al., 2012) claims that differences between conditions in terms of the amount of attention infants paid to the modeled action caused the differences in infants' performance between conditions. In order to investigate this assumption we presented 14-month-olds (N=34) with an eye-tracking paradigm and analyzed their looking behavior when observing the head-touch demonstration in the two original conditions. Subsequently, they had the chance to operate the apparatus themselves, and we measured their imitative responses. In order to explore the perceptional processes taking place in this paradigm in adulthood, we also presented adults (N=31) with the same task. Apart from the fact that we did not replicate the findings in imitation with our participants, the eye-tracking results do not support the perceptional distraction account: infants did not statistically differ - not even tendentially - in their amount of looking at the modeled action in both conditions. Adults also did not statistically differ in their looking at the relevant action components. However, both groups predominantly observed the relevant head action. Consequently, infants and adults do not seem to attend differently to constrained and unconstrained modelled actions.

Distraction by Novel and Pitch-Deviant Sounds in Children.

The control of attention is an important part of our executive functions and enables us to focus on relevant information and to ignore irrelevant information. The ability to shield against distraction by task-irrelevant sounds is suggested to mature during school age. The present study investigated the developmental time course of distraction in three groups of children aged 7-10 years. Two different types of distractor sounds that have been frequently used in auditory attention research-novel environmental and pitch-deviant sounds-were presented within an oddball paradigm while children performed a visual categorization task. Reaction time measurements revealed decreasing distractor-related impairment with age. Novel environmental sounds impaired performance in the categorization task more than pitch-deviant sounds. The youngest children showed a pronounced decline of novel-related distraction effects throughout the experimental session. Such a significant decline as a result of practice was not observed in the pitch-deviant condition and not in older children. We observed no correlation between cross-modal distraction effects and performance in standardized tests of concentration and visual distraction. Results of the cross-modal distraction paradigm indicate that separate mechanisms underlying the processing of novel environmental and pitch-deviant sounds develop with different time courses and that these mechanisms develop considerably within a few years in middle childhood.

Infant and adult pupil dilation in response to unexpected sounds.

Surprisingly occurring sounds outside the focus of attention can involuntarily capture attention. This study focuses on the impact of deviant sounds on the pupil size as a marker of auditory involuntary attention in infants. We presented an oddball paradigm including four types of deviant sounds within a sequence of repeated standard sounds to 14-month-old infants and to adults. Environmental and noise deviant sounds elicited a strong pupil dilation response (PDR) in both age groups. In contrast, moderate frequency deviants elicited a significant PDR in adults only. Moreover, a principal component analysis revealed two components underlying the PDR. Component scores differ, depending on deviant types, between age groups. Results indicate age effects of parasympathetic inhibition and sympathetic activation of the pupil size caused by deviant sounds with a high arousing potential. Results demonstrate that the PDR is a sensitive tool for the investigation of involuntary attention to sounds in preverbal children.