Neural Correlates of Cardiac Interoceptive Focus Across Development: Implications for Social Symptoms in Autism Spectrum Disorder

Abstract

Interoception involves the processing of sensory information relevant to physiological functioning and is integral to building self‐awareness, emotional states, and modulating social behaviors. With the role of interoception in emotional processing and social functioning, there is growing interest in characterizing interoception in autism spectrum disorder (ASD), yet, there are mixed results regarding cardiac interoceptive accuracy in ASD. In this study, we explored the neural basis of cardiac interoception using an fMRI heartbeat‐counting task in order to assess neural correlates of primary interoception. We predicted that interoceptive‐specific response in the insula, a “hub” for interoception, would be related to ASD symptomatology. We investigated the relationship of insula responses during cardiac interoceptive focus and a self/caregiver‐reported autism‐related symptom scale (Social Responsiveness Scale‐2 (SRS)). Participants included 46 individuals with autism spectrum disorder (ASD) (age 8–54, mean = 19.43 ± 10.68 years) and 54 individuals with typical development for comparison (TC, age 8–53, mean = 21.43 ± 10.41 years). We found no significant difference in cardiac interoceptive accuracy or neural response to cardiac interoception focus in ASD. Several insula subdivisions had a curvilinear relationship to age, peaking in early adulthood. Interoceptive‐specific insula response was associated with adult self‐report SRS scores; this association differed by diagnostic group and was not present for caregiver‐reported scores. This work suggests that (a) there is no global deficit in cardiac interoception in ASD, but integrating interoceptive cues with social information may distinguish individuals with ASD, and (b) there is a developmental trajectory for interoceptive processing in the insula that may be relevant for socio‐emotional health. Autism Res 2020, 13: 908‐920. © 2020 International Society for Autism Research, Wiley Periodicals, Inc. Lay Summary We use internal sensory information from the body, such as signals from the heart, to understand our emotional response to the external world. We measured how accurately people with autism feel their heartbeat and how the brain responds to this type of information. We found no differences between the autism and comparison groups in how the brain senses heartbeats, or in how accurately people feel their heartbeats. However, for people with autism, brain responses while sensing heartbeats were related to social difficulties. This work suggests people with autism may use internal and external information in a different way.

Role of anatomical insular subdivisions in interoception: Interoceptive attention and accuracy have dissociable substrates

“…Previous fMRI studies have suggested right insular dominance in interoception (Simmons et al., 2013; Zaki et al., 2012), which supports the forebrain asymmetry of sympathetic/parasympathetic processing (Craig, 2005, 2009). Other studies have reported that the bilateral insula is involved in interoceptive attention tasks; however, none of these studies directly compared the activation between the right and left insula (Failla et al., 2020; Haase et al., 2016; Wiebking et al., 2010). Regarding the asymmetry in autonomic input to the insula, the results of the current study imply that a representation of body states is established by the cooperation of sympathetic activities on the right middle‐anterior insula and by parasympathetic activities on the left.…”

“…These studies may support the view of sympathetic bodily re‐representation that occurs exclusively in the right anterior insula, but others implicitly challenge this notion. That is, studies employing the interoceptive attention paradigm have often reported the activation of the bilateral middle insula (Avery et al., 2014; Failla et al., 2020; Haase et al., 2016; Stern et al., 2017; Wiebking et al., 2010). A meta‐analysis on interoceptive attention (especially heart attention) found that the cluster was consistently activated in the bilateral (but somewhat right‐lateralized) dorsal middle insula (Schulz, 2016).…”

Individuals with Autistic Traits Exhibit Heightened Alexithymia But Intact Interoceptive-Exteroceptive Sensory Integration

“…These neuroanatomic finding may implicate the possible overgrowth of interoceptive brain regions in ASD. More recently, however, a functional neuroimaging study recruited 46 ASD patients (aged between 8 and 54 years) and matched controls, and reported that no impairment of interoceptive accuracy was found in both behavioural and functional brain activation patterns (Failla et al, 2020). Further research is needed to clarify whether ASD individuals are impaired in multidimensional interoception.…”

“…Recently, interoceptive deficits in patients with psychiatric disorders have attracted growing research interest. Abnormal interoception is believed to contribute to impairments of social cognitions found in people with anxiety disorders (Palser et al, 2018;Pollatos et al, 2009), depression (Barrett et al, 2016;Paulus & Stein, 2010), anorexia nervosa (Khalsa et al, 2018;McFadden et al, 2014), attention-deficit/hyperactivity disorder (Kutscheidt et al, 2019), schizophrenia (Ebisch et al, 2014;Torregrossa et al, 2019) and autism spectrum disorder (ASD) (Failla et al, 2020;Francis et al, 2019;Garfinkel et al, 2016;Schauder et al, 2015).…”

Atypical interoception as a common risk factor for psychopathology: A review

“…Neither of these studies directly compared neural activation to that in adult participants, however, meaning further work is needed to determine the full developmental trajectory. In a sample of neurotypical and autistic individuals spanning a larger age range (8–54 years), quadratic and linear relationships were observed between age and neural activation while performing the heartbeat counting task in different subdivisions of the insula, and linear relationships between age and activation in a broader interoceptive network, although age was unrelated to behavioural task performance ( Failla et al, 2020 ). Interoceptive accuracy does appear to be associated with heartbeat evoked potentials in adolescence, as in adulthood ( Mai et al, 2018 ), but again work is needed that explicitly follows the developmental trajectory throughout childhood and into adulthood.…”