Sensory processing dysfunction (SPD), manifests as difficulty interpreting the sensory world in an adaptive way, is common across children with neurodevelopmental disorders (NDD), including children who meet the categorical label of autism spectrum disorder (ASD) [1, 2]. Under the umbrella of SPD, there are three suggested primary subtypes: difficulties modulating sensory input, difficulties discriminating sensory information, and difficulties with sensory-based motor control . While these challenges can exist independently, they often co-occur. The Diagnostic and Statistical Manual-5 (DSM-5) now includes hyper- and hypo-reactivity to sensory input (characteristic of sensory modulation) as a core criteria for ASD, which has prompted additional interest and focus on sensory modulation .
Previous research suggests that one aspect of sensory modulation, sensory over-responsivity (SOR), occurs most frequently in the auditory and tactile domains; thus, these sensory domains are the focus of this investigation . We chose to focus on SOR given the distress associated with it . Over-responsivity manifests as extreme adverse or avoidant responses to sensory stimulation, such as covering ears and running from the room in response to a vacuum cleaner, blender, or automatic flushing toilet (auditory over-responsivity (AOR)). In the tactile domain, sensory over-responsivity modulation difficulties may manifest as refusal to wear clothing (particularly underwear), not liking to be touched, and not wanting to touch certain materials, leading to significant household disruption and social challenges (tactile over-responsivity (TOR)).
We seek to investigate the structural underpinnings of SOR to determine if there is a unique, architectural neural signature that can be used as a biomarker for intervention. This study focuses on auditory over-responsivity (AOR) and tactile over-responsivity (TOR) in a broad neurodevelopmental cohort, taking a Research Domain Criteria (RDoC)-inspired “sensory-first” approach . The goal is to compare direct assessment and parent report measures of AOR and TOR in a pediatric cohort and to explore the neural architecture of SOR in children across categorical diagnoses.
Characterizing sensory over-responsivity in children with neurodevelopmental disorders
Sensory responsivity measures include parent reports, expert observation, and psychophysiological testing [8,9,10,11]. Currently, parent report measures often assess sensory modulation but include a combination of modulation phenotypes as well as other aspects of sensory processing [12,13,14,15,16,17,18]. The Sensory Processing-Three Dimensions: Inventory quantifies sensory domains (vision, hearing, touch, and movement) by modulation and discrimination, as well as sensory-based motor challenges [19, 20]. The Sensory Sensitivity Questionnaire and the Sensory Experiences Questionnaire characterize sensory modulation specifically for children with ASD [21, 22]. The Sensory Profile (SP) has been validated cross-culturally and across clinical cohorts using sensory quadrant and section scoring methodology [15, 23,24,25,26,27,28,29]. The Short Sensory Profile (SSP), derived from the SP, has been used to differentiate typically developing children from children with ASD [8, 16, 18, 30, 31]. The SSP and other parent reports have made significant contributions to the research and clinical understanding of sensory dysfunction and have been instrumental for “trait-based” assessment. Although important for describing trait behavior, caregiver reports are subjective by nature and often affected by previous experience and expectation. Consequently, while they are a critical component of a thorough and appropriate clinical formulation, they are less ideal for objective state assessment and in previous work have shown less correlation with brain structure than direct assessment . Furthermore, a recent factor analysis in children with autism spectrum disorder questions the research validity of the SSP’s current factor structure, suggesting that two questions in particular are specific to AOR, which is one of the two sensory domains highlighted in this current project . With a more limited but specific SOR subset of questions from the SSP, we aim to better assess the phenotype between auditory and tactile over-responsivity in this cohort of children with and without neurodevelopmental challenges.
We suggest that often parent report measures, the totals and even some of the current subscales, coalesce a more complex cluster of behavioral observations while direct assessment, such as the one included in this study, aims to assess a single sensory domain at a single point in time, in a controlled environment, on a singular processing ability (sensory over-responsivity). Several sensory observation measures exist for young children such as the Sensory Integration and Praxis Tests (SIPT), the Sensory Processing Assessment for Young Children (SPA), the Tactile Defensiveness and Discrimination Test-Revised (TDDT-R), and the Infant Test of Sensory Functioning [34,35,36,37,38]. A previous study using the Sensory Processing-Three Dimensions: Assessment (SP-3D:A), a direct sensory modulation observation for individuals 3 to 21 years of age, identified the most differentiating items for children, adolescents, and young adults with autism . Moreover, previous work investigated reliability and validity but cut-off scores to enable categorization for clinical utility and direct research group comparison have not yet been developed [39, 40]. Hence, this study seeks to advance the field of sensory assessments by comparing the auditory and tactile over-responsive items for children with neurodevelopmental disorders using parent report (SSP) and direct assessment (SP-3D:A) and by providing cut-off scores. While other observational measures focus on one sensory domain, the SP-3D:A is ideally suited for this task, as it includes characterizations of SOR in both auditory and tactile domains .
Neural architecture of sensory processing to date
The neural architecture, both structural and functional, of sensory processing in individuals with autism has been explored using a variety of techniques and paradigms including EEG, MEG, fMRI, MRS, and DTI [41,42,43,44,45,46]. This study focuses on refining our understanding of the structural differences underlying auditory and tactile over-responsivity using DTI across neurodevelopmental conditions. Prior DTI work has characterized the neural underpinnings of sensory processing differences more broadly in children with ASD and SPD but has not taken a more parsimonious approach [32, 45, 47]. For example, Chang et al. reported robust alterations of posterior white matter microstructure in children with broadly defined SPD relative to typically developing children (TDC) . This investigation found strong correlations between fractional anisotropy (FA), a measure of microstructural integrity, and parent report and direct assessment measures of tactile and auditory discrimination across all children. However, direct assessment of sensory discrimination showed stronger and more continuous mapping to underlying white matter integrity than the parent report measures. Additionally, in children with ASD, Pryweller et al. reported decreased FA in the inferior longitudinal fasciculus (ILF), which correlated directly with measures of TOR (defensiveness), suggesting atypical connectivity between the limbic system and multisensory integration regions . This finding offers a preliminary explanation for the dysregulated emotional valence applied to non-noxious tactile stimuli. While the current literature has provided initial evidence for structural correlates of sensory processing dysregulation, further research is needed to specify the existence of neural tracts associated with specific domains of sensory over-responsivity. This approach will contribute to developing novel, targeted interventions aimed at atypical structural connectivity in children with neurodevelopmental disorders. By assessing connectivity before and after trainings targeting over-responsivity, we hope to be able to determine whether applied interventions are indeed leading to measurable change. But first, we need to know where to look and what to measure. This study is an initial foray in this next step. In this study, we hypothesize that direct assessment of AOR and TOR will show strong inter-test agreement with corresponding parental report behaviors in a NDD cohort and that sensory-first categorization using direct assessment of AOR will identify a more succinct subset of white matter tracts than previously identified using parent report.