Respiratory sinus arrhythmia and auditory processing in autism: Modifiable deficits of an integrated social engagement system?

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Abstract

The current study evaluated processes underlying two common symptoms (i.e., state regulation problems and deficits in auditory processing) associated with a diagnosis of autism spectrum disorders. Although these symptoms have been treated in the literature as unrelated, when informed by the Polyvagal Theory, these symptoms may be viewed as the predictable consequences of depressed neural regulation of an integrated social engagement system, in which there is down regulation of neural influences to the heart (i.e., via the vagus) and to the middle ear muscles (i.e., via the facial and trigeminal cranial nerves). Respiratory sinus arrhythmia (RSA) and heart period were monitored to evaluate state regulation during a baseline and two auditory processing tasks (i.e., the SCAN tests for Filtered Words and Competing Words), which were used to evaluate auditory processing performance. Children with a diagnosis of autism spectrum disorders (ASD) were contrasted with aged matched typically developing children. The current study identified three features that distinguished the ASD group from a group of typically developing children: 1) baseline RSA, 2) direction of RSA reactivity, and 3) auditory processing performance. In the ASD group, the pattern of change in RSA during the attention demanding SCAN tests moderated the relation between performance on the Competing Words test and IQ. In addition, in a subset of ASD participants, auditory processing performance improved and RSA increased following an intervention designed to improve auditory processing.

Highlights

► Autistic children (ASD) had depressed RSA and auditory processing performance. ► RSA reactivity moderated the relation between dichotic listening and IQ in ASD. ► RSA and auditory processing are theoretically linked to a social engagement system. ► An intervention was tested with ASD that stimulated the social engagement system. ► Auditory processing improved and RSA increased in ASD following intervention.

Introduction

Difficulties in state regulation and deficits in auditory processing are prevalent symptoms in autism spectrum disorders (ASD), although neither are a criterion for diagnosis. Problems in state regulation may be expressed as atypical social and emotional behaviors (e.g., Bachevalier and Loveland, 2006), low thresholds to be reactive, tantrums, difficulties in sustaining attention, and sleep disorders. The auditory processing deficits may be experienced as language and speech delays, difficulties in extracting human voice from background sounds, hyperacusis, or as a general compromise in social communication skills (Dissanayake and Sigman, 2001, Frith and Baron-Cohen, 1987, Hayes and Gordon, 1977, Klin, 1992, Lockyer and Rutter, 1969).

The mechanisms mediating state regulation and auditory processing are assumed to represent disparate response systems. From an empirical perspective state regulation is manifested in observable behaviors, while auditory processing is manifested in expressive and receptive language skills. These problems are not unique to individuals diagnosed with autism, and similar symptoms have been observed in other clinical disorders including fragile X syndrome, attention deficit disorder, post-traumatic stress disorder, and anxiety disorders.

In typically developing children both domains exhibit a developmental trajectory. During the first few years of life language and listening skills improve and are paralleled by improved state regulation. The improved state regulation is often observed as an increased ability to sustain attention, while actively inhibiting responses to distracters. During aging, the reverse is observed and there are increases in problems associated with both domains.

Since deficits in state regulation and auditory processing lack diagnostic specificity, researchers, who study the neurobiological and biobehavioral features of a specific clinical diagnosis such as autism, have not focused on these domains. Rather, research in clinical neuroscience has targeted investigations of potential biomarkers (e.g., genetic, neurochemical) unique to a diagnostic category. This strategy assumes the possibility that a biomarker or set of biomarkers could be identified, which would provide needed information to reconceptualize the diagnosis and treatment of autism. However, research need not be focused on specificity of neurobiological features and can be directed at understanding the neural mechanisms leading to compromised behaviors common to several diagnostic categories. Thus, in spite of this lack of diagnostic specificity, difficulties in state regulation and auditory processing are prevalent, and degrade quality of life by interfering with an ability to participate in social interactions and educational opportunities in the home, clinic, and classroom. This focus on observable behavior and measureable neurobiological processes, independent of clinical diagnosis, is consistent with the NIMH Strategic Plan for Research Domain Criteria.

State regulation and auditory processing are dependent on response systems that are studied by different scientific disciplines, which have little interaction and virtually no common language. For example, the study of psychiatric disorders (i.e., diagnoses), behavioral problems (e.g., state regulation and tantrums), psychological difficulties (e.g., emotional instability), auditory processing disorders (e.g., difficulties understanding verbal instructions), and cognitive deficits (e.g., language delays) represent research domains investigated by separate disciplines. These distinctions contribute to the current models of inquiry applied in clinical neuroscience, which rely on separate disciplines to categorize, investigate, treat, and explain the neurobiological mechanisms of clinical disorders.

Since deficits in state regulation and auditory processing frequently are observed in the same individual, do they share common neural mechanisms? If these deficits have a common neural substrate, will an understanding of this “common” neural mechanism provide insights into the management of symptoms frequently observed in individuals with autism? The above questions may require a new conceptualization of the phenotypic features of autism, especially if features, such as deficits in state regulation and auditory processing, are shared with other clinical disorders.

The Polyvagal Theory (Porges, 1995, Porges, 1998, Porges, 2001, Porges, 2003, Porges, 2007) proposes a strategy that applies evolution as an organizing principle to understand the link between state regulation and auditory processing. According to the Polyvagal Theory, the well-documented phylogenetic shift in neural regulation of the autonomic nervous system provided mammals with a neural circuit that promoted social interactions in safe contexts by supporting calm physiological states and an ability to process relatively soft vocalizations in a frequency band distinct from the lower frequencies associated with predators (see Porges and Lewis, 2009). This “mammalian” circuit functions as the neural substrate for an integrated social engagement system. Many of the behavioral attributes of autism appear to be convergent with a compromise in this hypothetical social engagement system.

The phylogenetic origin of the social engagement system is intertwined with the evolutionary changes in vertebrate autonomic nervous systems. As the muscles of the face and head emerged as social engagement structures, a new component of the autonomic nervous system (i.e., a myelinated vagus) evolved that was regulated by the nucleus ambiguus, a medullary nucleus ventral to the dorsal motor nucleus of the vagus. This convergence of neural mechanisms regulating heart and face provides the neural substrate for an integrated social engagement system with synergistic facial and visceral components. The product of this evolution is a system that co-opted a variety of structures and processes to support social behavior including such disparate processes as ingestion and state regulation, and integrated these processes with social engagement behaviors involving facial expressivity, head gesture, listening, and vocalizations (see Table 1).

Special visceral efferent pathways originating in brainstem nuclei travel through several cranial nerves to regulate the striated muscles of the face and head (Parent and Carpenter, 1996). These "brain-face" circuits, via a synergistic "collaboration" with the meylinated vagus, form the neural substrate of the social engagement system (see Porges, 1998, Porges, 2001, Porges, 2003). The social engagement system is controlled from higher brain circuits and via feedback from the periphery that regulates brainstem nuclei (i.e., lower motor neurons) to control eyelid opening (e.g., looking), facial muscles (e.g., emotional expression), middle ear muscles (e.g., extracting human voice from background noise), muscles of mastication (e.g., ingestion), laryngeal and pharyngeal muscles (e.g., prosody and intonation), and head turning muscles (e.g., social gesture and orientation). Collectively, these muscles function both as determinants of engagement with the social environment and as filters that limit social stimuli. The neural pathways involved in raising the eyelids also tense the stapedius muscle in the middle ear, which functionally dampens the transmission of low frequency background sounds and facilitates the ability to hear the acoustic frequencies associated with human speech. Thus, the neural mechanisms for making eye contact are shared with those needed to listen to human voice. As a cluster, deficits in the features of the social engagement system (see Table 1) such as difficulties in gaze, extraction of human voice from background sounds, facial expression, head gesture, and dampened vocal prosody are common features of ASD.

Based on the Polyvagal Theory, it would be hypothesized that the deficits in behavioral and psychological features of the social engagement system would be paralleled by reduced vagal influences to the heart via the myelinated vagus and measured by the amplitude of respiratory sinus arrhythmia (RSA). According to the Polyvagal Theory, dampened vagal regulation of the heart via the myelinated vagus is an adaptive response strategy to support mobilization (i.e., fight–flight behaviors) in dangerous environments. Since the Polyvagal Theory articulates a hierarchy of neural circuits, the metabolic resources necessary for fight–flight behaviors are not efficiently available unless there is a retraction of the vagal brake (i.e., the calming influence of the myelinated vagus on the sympathetic nervous system enables social engagement behaviors to spontaneously occur). Thus, understanding the neural mechanisms defining the social engagement system provides a plausible model to explain why both auditory processing and state regulation difficulties are prevalent in ASD.

In the current study we focus on documenting the covariation of two processes, vagal regulation of the heart and auditory processing skills, theoretically linked by the Polyvagal Theory. Consistent with a psychophysiological perspective, the experimental design provides an opportunity to evaluate this covariation by contrasting typically developing children and adolescents with ASD participants. Since the prevalence of deficits in state regulation and poor auditory processing skills is high in ASD, the experimental design provides an opportunity to evaluate the covariation of these processes through different analytic strategies. Thus, hypotheses regarding the covariation between RSA and auditory processing are tested via: 1) group contrasts, 2) individual differences, and 3) the response of ASD participants to an intervention designed to improve auditory processing.

Section snippets

Participants

All participants, with and without a diagnosis of autism spectrum disorders (ASD), were recruited from the Chicago area and tested in protocols approved by the University of Illinois at Chicago Institutional Review Board. Potential participants were excluded if they were taking medications or had a medical condition that might influence autonomic function. The participants ranged in age between 6 and 21 years. The control and ASD groups did not differ in age (see Table 2).

Study 1

The ASD (n = 78) participants had significantly lower RSA, F(1, 144) = 48.6, p < .001, and shorter heart period, F(1, 144) = 63.4, p < .001, at baseline than typically developing participants (n = 68). The descriptive data are provided in Table 2. Since the study evaluated individuals across a broad age range, the relation between age in months and the cardiac parameters were evaluated. Consistent with the well-documented relation between the slowing of heart rate and the increase in body size associated

Discussion

The group contrasts identified three features that distinguish the ASD group from a group of typically developing children: 1) baseline RSA, 2) RSA reactivity, and 3) auditory processing performance. The interpretation of the interrelationships among these variables is dependent on the Polyvagal Theory and the functional model of an integrated social engagement system derived from the theory. The neurobiological substrate of the social engagement system provides the basis for a developmentally

Acknowledgments

Support for the research described in this manuscript was provided, in part, by grants from the National Institute of Mental Health (MH060625), Unicorn Children's Foundation, Cure Autism Now Foundation, Nancy Lurie Marks Family Foundation, and Autism Speaks. The contents of this manuscript are solely the responsibility of the authors and do not represent the official views of NIH or other funding agencies. We would like to thank the staff and students at Easter Seals Therapeutic School and

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