Dataset Information

Distinct Patterns of Neural Habituation and Generalization in Children and Adolescents With Autism With Low and High Sensory Overresponsivity.

ABSTRACT: OBJECTIVE:Sensory overresponsivity (SOR), an atypical negative reaction to sensory stimuli, is highly prevalent in autism spectrum disorder (ASD). Previous work has related SOR to increased brain response in sensory-limbic regions. This study investigated where these atypical responses fall in three fundamental stages of sensory processing: arousal (i.e., initial response), habituation (i.e., change in response over time), and generalization of response to novel stimuli. Different areas of atypical response would require distinct intervention approaches. METHODS:Functional MRI was used to examine these patterns of neural habituation to two sets of similar mildly aversive auditory and tactile stimuli in 42 high-functioning children and adolescents with ASD (21 with high levels of SOR and 21 with low levels of SOR) and 27 age-matched typically developing youths (ages 8-17). The relationship between SOR and change in amygdala-prefrontal functional connectivity across the sensory stimulation was also examined. RESULTS:Across repeated sensory stimulation, high-SOR participants with ASD showed reduced ability to maintain habituation in the amygdala and relevant sensory cortices and to maintain inhibition of irrelevant sensory cortices. These results indicate that sensory habituation is a dynamic, time-varying process dependent on sustained regulation across time, which is a particular deficit in high-SOR participants with ASD. However, low-SOR participants with ASD also showed distinct, nontypical neural response patterns, including reduced responsiveness to novel but similar stimuli and increases in prefrontal-amygdala regulation across the sensory exposure. CONCLUSIONS:The results suggest that all children with autism have atypical brain responses to sensory stimuli, but whether they express atypical behavioral responses depends on top-down regulatory mechanisms. Results are discussed in terms of targeted intervention approaches.

SUBMITTER: Green SA

PROVIDER: S-EPMC6889004 | biostudies-literature | 2019 Dec

REPOSITORIES: biostudies-literature

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Distinct Patterns of Neural Habituation and Generalization in Children and Adolescents With Autism With Low and High Sensory Overresponsivity.

Green Shulamite A SA Hernandez Leanna L Lawrence Katherine E KE Liu Janelle J Tsang Tawny T Yeargin Jillian J Cummings Kaitlin K Laugeson Elizabeth E Dapretto Mirella M Bookheimer Susan Y SY

The American journal of psychiatry 20190624 12

<h4>Objective</h4>Sensory overresponsivity (SOR), an atypical negative reaction to sensory stimuli, is highly prevalent in autism spectrum disorder (ASD). Previous work has related SOR to increased brain response in sensory-limbic regions. This study investigated where these atypical responses fall in three fundamental stages of sensory processing: arousal (i.e., initial response), habituation (i.e., change in response over time), and generalization of response to novel stimuli. Different areas ...[more]

PMID: 31230465

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Project description:IMPORTANCE:More than half of youth with autism spectrum disorders (ASDs) have sensory overresponsivity (SOR), an extreme negative reaction to sensory stimuli. However, little is known about the neurobiological basis of SOR, and there are few effective treatments. Understanding whether SOR is due to an initial heightened sensory response or to deficits in regulating emotional reactions to stimuli has important implications for intervention. OBJECTIVE:To determine differences in brain responses, habituation, and connectivity during exposure to mildly aversive sensory stimuli in youth with ASDs and SOR compared with youth with ASDs without SOR and compared with typically developing control subjects. DESIGN, SETTING, AND PARTICIPANTS:Functional magnetic resonance imaging was used to examine brain responses and habituation to mildly aversive auditory and tactile stimuli in 19 high-functioning youths with ASDs and 19 age- and IQ-matched, typically developing youths (age range, 9-17 years). Brain activity was related to parents' ratings of children's SOR symptoms. Functional connectivity between the amygdala and orbitofrontal cortex was compared between ASDs subgroups with and without SOR and typically developing controls without SOR. The study dates were March 2012 through February 2014. MAIN OUTCOMES AND MEASURES:Relative increases in blood oxygen level-dependent signal response across the whole brain and within the amygdala during exposure to sensory stimuli compared with fixation, as well as correlation between blood oxygen level-dependent signal change in the amygdala and orbitofrontal cortex. RESULTS:The mean age in both groups was 14 years and the majority in both groups (16 of 19 each) were male. Compared with neurotypical control participants, participants with ASDs displayed stronger activation in primary sensory cortices and the amygdala (P?<?.05, corrected). This activity was positively correlated with SOR symptoms after controlling for anxiety. The ASDs with SOR subgroup had decreased neural habituation to stimuli in sensory cortices and the amygdala compared with groups without SOR. Youth with ASDs without SOR showed a pattern of amygdala downregulation, with negative connectivity between the amygdala and orbitofrontal cortex (thresholded at z?>?1.70, P?<?.05). CONCLUSIONS AND RELEVANCE:Results demonstrate that youth with ASDs and SOR show sensorilimbic hyperresponsivity to mildly aversive tactile and auditory stimuli, particularly to multiple modalities presented simultaneously, and show that this hyperresponsivity is due to failure to habituate. In addition, findings suggest that a subset of youth with ASDs can regulate their responses through prefrontal downregulation of amygdala activity. Implications for intervention include minimizing exposure to multiple sensory modalities and building coping strategies for regulating emotional response to stimuli.

Project description:BackgroundSensory overresponsivity (SOR) has emerged as a potential endophenotype in obsessive-compulsive disorder (OCD), but few studies have examined SOR in relation to the major symptom dimensions of OCD and to symptoms across the full obsessive-compulsive (OC) symptom spectrum.ObjectiveThis study had 2 main objectives. First, we examined the psychometric properties of the SOR Scales in a community-based sample of Spanish adolescents and adults. Second, we identified how SOR difficulties are related to symptoms across the full OC spectrum (eg, OC, body dysmorphic, hoarding, skin-picking, and hair-pulling symptoms), including the heterogeneity of OC symptoms.MethodsWe translated the SOR Scales into Spanish-a measure that assesses SOR across the 5 sensory modalities-and created a web-based version of the measure. A sample of 1454 adolescents and adults (mean age 23.84, SD 8.46 years) participated in the study, and 388 (26.69%) participants completed the survey twice (approximately 8 months apart). The survey also contained a web-based measure that assesses symptoms across the full OC spectrum: harm and checking, taboo obsessions, contamination or cleaning, symmetry and ordering, body dysmorphic, hoarding, hair-pulling, and skin-picking symptoms.ResultsThe psychometric properties of the SOR Scales were excellent, and the test-retest reliability was adequate. All types of SOR were related to all major symptom dimensions of OCD and to all OC spectrum symptoms.ConclusionsSOR across the sensory modalities can be validly assessed using a web-based measure. SOR emerged as a pure transdiagnostic phenomenon in relation to symptoms across the OC spectrum, with no specific sensory modality being more strongly related to OC symptoms. SOR can shed much needed light on basic mechanisms that are important for the onset and maintenance of OC spectrum symptoms, and this study shows that large-scale web-based studies can aid in this endeavor. Future studies should examine whether SOR precedes or emerges alongside OC symptoms.

Project description:BACKGROUND:Functional magnetic resonance imaging research on autism spectrum disorders (ASDs) has been largely limited to individuals with near-average intelligence. Although cognitive impairment is common in ASDs, functional network connectivity in this population remains poorly understood. Specifically, it remains unknown whether lower-functioning individuals exhibit exacerbated connectivity abnormalities similar to those previously detected in higher-functioning samples or specific divergent patterns of connectivity. METHODS:Resting-state functional magnetic resonance imaging data from 88 children (44 ASD, 44 typically developing; average age: 11 years) were included. Based on IQ, individuals with ASDs were assigned to either a lower-functioning group (mean IQ = 77 ± 6) or a higher-functioning group (mean IQ = 123 ± 8). Two typically developing comparison groups were matched to these groups on head motion, handedness, and age. Seeds in the medial prefrontal cortex, posterior cingulate cortex, posterior superior temporal sulcus, insula, and amygdala were used to contrast whole-brain functional connectivity across groups. RESULTS:Lower-functioning ASD participants (compared with higher-functioning ASD participants) showed significant underconnectivity within the default mode network and the ventral visual stream. Higher-functioning ASD participants (compared with matched typically developing participants) showed significantly decreased anticorrelations among default mode, salience, and task-positive regions. Effect sizes of detected differences were large (Cohen's d > 1.46). CONCLUSIONS:Lower- and higher-functioning individuals with ASDs demonstrated distinct patterns of atypical connectivity. Findings suggest a gross pattern of predominantly reduced network integration in lower-functioning ASDs (affecting default mode and visual networks) and predominantly reduced network segregation in higher-functioning ASDs. Results indicate the need for stratification by general functional level in studies of functional connectivity in ASDs.

Project description:Symptoms of autism spectrum disorder and attention-deficit/hyperactivity disorder often co-occur. Among these, sensory impairment, which is a core diagnostic feature of autism spectrum disorder, is often observed in children with attention-deficit/hyperactivity disorder. However, the underlying mechanisms of symptoms that are shared across disorders remain unknown. To examine the neural correlates of sensory symptoms that are associated with autism spectrum disorder and attention-deficit/hyperactivity disorder, we analysed resting-state functional MRI data obtained from 113 people with either autism spectrum disorder or attention-deficit/hyperactivity disorder (n = 78 autism spectrum disorder, mean age = 29.5; n = 35 attention-deficit/hyperactivity disorder, mean age = 31.2) and 96 neurotypical controls (mean age = 30.6, range: 20-55 years) using a cross-sectional study design. First, we used a multi-dimensional approach to examine intrinsic brain functional connectivity related to sensory symptoms in four domains (i.e. low registration, sensation seeking, sensory sensitivity and sensation avoidance), after controlling for age, handedness and head motion. Then, we used a partial least squares correlation to examine the link between sensory symptoms related to intrinsic brain functional connectivity and neurodevelopmental symptoms measured using the Autism Spectrum Quotient and Conners' Adult Attention-Deficit/Hyperactivity Disorder Rating Scale, regardless of diagnosis. To test whether observed associations were specific to sensory symptoms related to intrinsic brain functional connectivity, we conducted a control analysis using a bootstrap framework. The results indicated that transdiagnostic yet distinct intrinsic brain functional connectivity neural bases varied according to the domain of the examined sensory symptom. Partial least squares correlation analysis revealed two latent components (latent component 1: q < 0.001 and latent component 2: q < 0.001). For latent component 1, a set of intrinsic brain functional connectivity was predominantly associated with neurodevelopmental symptom-related composite score (r = 0.64, P < 0.001), which was significantly correlated with Conners' Adult Attention-Deficit/Hyperactivity Disorder Rating Scale total T scores (r = -0.99, q < 0.001). For latent component 2, another set of intrinsic brain functional connectivity was positively associated with neurodevelopmental symptom-related composite score (r = 0.58, P < 0.001), which was eventually positively associated with Autism Spectrum Quotient total scores (r = 0.92, q < 0.001). The bootstrap analysis showed that the relationship between intrinsic brain functional connectivity and neurodevelopmental symptoms was relative to sensory symptom-related intrinsic brain functional connectivity (latent component 1: P = 0.003 and latent component 2: P < 0.001). The current results suggest that sensory symptoms in individuals with autism spectrum disorder and those with attention-deficit/hyperactivity disorder have shared neural correlates. The neural correlates of the sensory symptoms were associated with the severity of both autism spectrum disorder and attention-deficit/hyperactivity disorder symptoms, regardless of diagnosis.

Dataset Information

Distinct Patterns of Neural Habituation and Generalization in Children and Adolescents With Autism With Low and High Sensory Overresponsivity.

Publications

Distinct Patterns of Neural Habituation and Generalization in Children and Adolescents With Autism With Low and High Sensory Overresponsivity.

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