Anxiety Disorders and Sensory Over-Responsivity in Children with Autism Spectrum Disorders: Is There a Causal Relationship?

“The amygdala has been implicated in anxiety disorders, mainly due to its central role in fear conditioning (e.g., Davis 1992; Garakani et al. 2006; Rauch et al. 2003).”

“However, Mogg and Bradley (1998) describe anxiety as a preattentive bias towards threat, and theorize that the automatic encoding of threat without elaborative processing leads to anxiety.”

“Currently, SOR can be identified in infants later diagnosed with ASD (Zwaigenbaum et al. 2005), which is much earlier than anxiety is usually diagnosed.”

“There is evidence that children with ASD have increased amygdala volumes compared to typically developing children, and that amygdala size is positively correlated with anxiety and severity of social-communication symptoms in these children (Amaral et al. 2008; Juranek et al. 2006).”

“Anxiety disorders are very common in children with autism spectrum disorders (ASD), and can increase the functional impairment of these children (Lainhart 1999; White et al. 2009 ).”

“In particular, MacLeod et al. (2002) demonstrated that training individuals to have an attentional bias towards threat-relevant words subsequently increased their negative response to stress.”

“It is also important to ask whether, theoretically, a preverbal child with low cognitive ability can be anxious, as some theories of anxiety relate anxiety to conscious cognitive processing and anticipation of future events (e.g., Beck and Clark 1997 ).”

“The amount of enhancement in the sensory response is correlated with the amount of amygdala activation, which suggests that children with SOR may have over-active amygdalas (Zald 2003).”

“Reports of SOR rates of 56–70% in children with ASD (Baranek et al. 2006; Ben-Sasson et al. 2007b) indicate elevated levels of SOR relative to rates of 10–17% in the general population (Ben-Sasson et al. 2009; Ben-Sasson et al. 2007b).”

“This may be an indicator of poor modulation of vestibularproprioceptive input, which is often observed in children with SOR ( Miller et al. 2007 ).”

“…have found rates of anxiety disorders and symptoms to be higher in children with ASD than in typically developing (TD) children (Gadow et al. 2004; Kim et al. 2000; Muris et al. 1998; Sukhodolsky et al. 2008; Weisbrot et al. 2005) and children with intellectual disability (Brereton et al. 2006).”

“Animals who have experienced context conditioning become behaviorally avoidant (Bouton and King 1983), and likewise children with SOR often become avoidant of generalized locations such as restaurants, grocery stores, or parties in addition to specific objects (Schoen et al. 2008).”

“Recently, a few studies have shown Cognitive Behavioral Therapy (CBT) to be efficacious in treating anxiety in children with ASD (e.g., Chalfant et al. 2007; Reaven and Hepburn 2003; Sofronoff et al. 2005; Sze and Wood 2007; Wood et al. 2009 ).”

“Exposure therapy could be combined with sensory stimulation intervention, such as body pressure, which would help decrease arousal (Baranek 2002) and make exposure less”

“Physiological studies that include adequate sample sizes and control groups (as suggested by Rogers and Ozonoff 2005), use sensory stimuli that are aversive to children with ASD, and examine subgroups of children with ASD, particularly those with anxiety symptoms.”

“…have found rates of anxiety disorders and symptoms to be higher in children with ASD than in typically developing (TD) children (Gadow et al. 2004; Kim et al. 2000; Muris et al. 1998; Sukhodolsky et al. 2008; Weisbrot et al. 2005) and children with intellectual disability (Brereton et al. 2006).”

“…have found rates of anxiety disorders and symptoms to be higher in children with ASD than in typically developing (TD) children (Gadow et al. 2004; Kim et al. 2000; Muris et al. 1998; Sukhodolsky et al. 2008; Weisbrot et al. 2005) and children with intellectual disability (Brereton et al. 2006).”

“This pairing of a conditioned stimulus (the loud noise) with a physiological reaction (e.g., fight-or-flight response) is known as interoceptive conditioning and is present in many different anxiety disorders (Razran 1961).”

“The amygdala has been implicated in anxiety disorders, mainly due to its central role in fear conditioning (e.g., Davis 1992; Garakani et al. 2006; Rauch et al. 2003 ).”

“Because context conditioning is associated with unpredictability and hippocampus activation (Grillon 2008), it is more characteristic of anxiety than fear.”

“Recently, a few studies have shown Cognitive Behavioral Therapy (CBT) to be efficacious in treating anxiety in children with ASD (e.g., Chalfant et al. 2007; Reaven and Hepburn 2003; Sofronoff et al. 2005; Sze and Wood 2007; Wood et al. 2009).”

“Children with SOR often react negatively to noisy or visually complex environments, are bothered by tags or seams on their clothing, or may dislike being touched unexpectedly (Liss et al. 2006).”

“Recently, a few studies have shown Cognitive Behavioral Therapy (CBT) to be efficacious in treating anxiety in children with ASD (e.g., Chalfant et al. 2007; Reaven and Hepburn 2003; Sofronoff et al. 2005; Sze and Wood 2007; Wood et al. 2009).”

“Reports of SOR rates of 56–70% in children with ASD (Baranek et al. 2006; Ben-Sasson et al. 2007b) indicate elevated levels of SOR relative to rates of 10–17% in the general population (Ben-Sasson et al. 2009; Ben-Sasson et al. 2007b).”

“Markram et al. (2008) examined the role of the amygdala in rats with ASD-like symptoms including repetitive behavior and reduced play and social behavior.”

“Specific phobia is one of the most common anxiety disorders seen in children with ASD (Gadow et al. 2004; Muris et al. 1998; Sukhodolsky et al. 2008), which is consistent with this fear and conditioning model, as it is easy to imagine how children with SOR might develop phobic responses to stimuli…”

“Some of these children also have a reduced range of facial affect and ability to express emotion appropriately (Yirmiya et al. 1989).”

“Specific phobia is one of the most common anxiety disorders seen in children with ASD (Gadow et al. 2004; Muris et al. 1998; Sukhodolsky et al. 2008), which is consistent with this fear and conditioning model, as it is easy to imagine how children with SOR might develop phobic responses to stimuli…”

“…have found rates of anxiety disorders and symptoms to be higher in children with ASD than in typically developing (TD) children (Gadow et al. 2004; Kim et al. 2000; Muris et al. 1998; Sukhodolsky et al. 2008; Weisbrot et al. 2005) and children with intellectual disability (Brereton et al. 2006).”

“Reports of SOR rates of 56–70% in children with ASD (Baranek et al. 2006; Ben-Sasson et al. 2007b) indicate elevated levels of SOR relative to rates of 10–17% in the general population (Ben-Sasson et al. 2009; Ben-Sasson et al. 2007b).”

“Very few toddlers (around 5–6%) with ASD are identified as having high rates of anxiety ( Ben-Sasson et al. 2008 ) but it is unclear whether that is due to actual low rates of anxiety or difficulty in identifying anxiety at this early age.”

“Furthermore, children with anxiety disorders tend to regulate their negative affectivity through avoidance of stimuli that elicit fear (Craske 2003).”

“Keywords Autism spectrum disorders Anxiety Sensory over-responsivity Hyperarousal Sensory defensiveness Anxiety disorders are very common in children with autism spectrum disorders (ASD), and can increase the functional impairment of these children (Lainhart 1999; White et al. 2009).”

“Sensory over-responsivity (SOR) is another common, and impairing feature found in more than half of children with ASD, and SOR has been linked to anxiety in children with ASD (Ben-Sasson et al. 2008; Liss et al. 2006; Pfeiffer et al. 2005).”

“It is still a controversial therapy, and while some studies show that it can improve children’s play and social-communication skills, there is little evidence that it specifically reduces SOR (Ayres and Tickle 1980; Case-Smith and Bryan 1999; Linderman and Stewart 1999).”

“The two conditions can be difficult to distinguish, as they both involve misperception of threat (e.g., Schoen et al. 2008) and overlap in their physiological (e.g., increased heart rate and skin conductance response) and behavioral (e.g., fight-or-flight response, emotional dysregulation,…”

“One way in which the two may be distinguished behaviorally is that SOR should be generalizable to multiple stimuli that elicit the unpleasant sensory response (e.g., several stimuli that create an aversive noise; see Miller et al. 2007) while specific phobia would be to one specific stimulus or situation (e.g. Ollendi…”

“It is still a controversial therapy, and while some studies show that it can improve children’s play and social-communication skills, there is little evidence that it specifically reduces SOR (Ayres and Tickle 1980; Case-Smith and Bryan 1999; Linderman and Stewart 1999).”

“As children with SOR by definition have an intense unconditional response to sensory stimuli, and as these stimuli are often elicited through factors completely outside the children’s control ( Reynolds and Lane 2008 ), one can see how these children are likely at high risk for fear conditioning.”

“The only ASD sensory intervention study that used anxiety as an outcome measure was conducted by Edelson et al. (1999).”

“Furthermore, if a child has a general anxiety disorder, by definition he or she should be generally anxious, not only to specific sensory stimuli (e.g., Masi et al. 2004 ).”

“Recently, a few studies have shown Cognitive Behavioral Therapy (CBT) to be efficacious in treating anxiety in children with ASD (e.g., Chalfant et al. 2007; Reaven and Hepburn 2003; Sofronoff et al. 2005; Sze and Wood 2007; Wood et al. 2009).”

“There is evidence that children with ASD have increased amygdala volumes compared to typically developing children, and that amygdala size is positively correlated with anxiety and severity of social-communication symptoms in these children (Amaral et al. 2008; Juranek et al. 2006 ).”

“Recently, a few studies have shown Cognitive Behavioral Therapy (CBT) to be efficacious in treating anxiety in children with ASD (e.g., Chalfant et al. 2007; Reaven and Hepburn 2003; Sofronoff et al. 2005; Sze and Wood 2007; Wood et al. 2009).”

“SSRIs used to treat anxiety in children may also reduce amygdala volume (Szeszko et al. 2004).”

“It is still a controversial therapy, and while some studies show that it can improve children’s play and social-communication skills, there is little evidence that it specifically reduces SOR (Ayres and Tickle 1980; Case-Smith and Bryan 1999; Linderman and Stewart 1999).”

“For example, weighted vests which provide continuous pressure (Ferterl-Daly et al. 2001) or touch therapy (e.g., massage; Baranek; Field et al. 1997; Silva et al. 2009) have been shown to improve young children with ASD’s responsiveness to sensory input, attention, stereotyped movements, and…”

“This is consistent with work outside the ASD literature showing a decrease in secondary anxiety symptoms in adults with SOR following a sensory-based intervention ( Pfeiffer and Kinnealey 2006 ).”

“…with children, suggesting that relative to healthy controls, children with anxiety disorders show a stronger bias in selectively attending to threat-relevant stimuli, and difficulty disengaging from these stimuli even when they have been asked to attend to other information (Mobini and Grant 2007).”

“Developing parent report and observation measures specific to ASD ( Davis et al. 2008 ) that make such distinctions is needed to analyze sources of stress in the frequent case that children are too young or lack the verbal skills to report their own symptoms.”

“Anxiety disorders are very common in children with autism spectrum disorders (ASD), and can increase the functional impairment of these children ( Lainhart 1999; White et al. 2009).”

“Although there are reports of the association of SOR and anxiety in individuals with other childhood and developmental disorders such as ADHD ( Reynolds et al. 2009 )w e chose to focus on ASD for the following reasons: (a) There are elevated rates of both conditions in individuals with ASD so determining causality bet…”

“For example, Plappert and Pilz (2002) found that mice that were genetically anxiety prone showed a stronger auditory startle reaction to sounds than non-anxious mice.”

“The discipline of the professional evaluating the child is not only likely to impact the child’s diagnosis but also the type of intervention the child is referred to. This problem was demonstrated by Ben-Sasson et al. (2007a) who found that occupational therapists were more likely to recommend a sensory-based interven…”

“Another factor which is thought to play an important role in anxiety in autism is sensory sensitivities (Green and Ben-Sasson 2010).”

“Although these areas of difficulty have been examined separately, studies have yet to examine the relations among these three conditions despite evidence suggesting that they may represent related and overlapping constructs (Campo et al. 2004; Green and Ben-Sasson 2010).”

“Green and Ben-Sasson (2010) proposed a model to explain how hyperreactivity in children with ASD can be characterized as hyper-attention to sensory stimuli and overreaction to those stimuli.”

“One explanation is that abnormal responses to high levels of sensory stimuli may be causative but this needs further exploration (Goldsmith et al. 2006; Green et al. 2010).”

“Based on the observation of increased prevalence of anxiety in more than 40% of ASD children [20], a model has been proposed that links anxiety with the highly prevalent trait of sensory over-responsitivity [21, 22].”

“Understanding sensory issues in adults with ASC is critical to the detection and prescription of appropriate interventions especially in light of studies that propose a theoretical relationship between anxiety and sensory over-responsivity (Green and Ben-Sasson, 2010).”

“Two studies present results supporting Green & BenSasson’s primary SOR theory—namely, (2) above, that SOR precedes anxiety.(98) In a sample including children with ASD, ADHD, and typical development who were presented with a sensory challenge, the intensity of the physical response measured with skin conductance media…”

“…of each condition in young children as well as simultaneously examining whether each one predicts change in the other can help us understand the direction of effect, given that it is as yet unclear what reciprocal patterns (if any) exist between anxiety and SOR (Green and Ben-Sasson 2010).”

“Green and Ben-Sasson (2010) proposed separate causal models for sensory over-responsivity and anxiety in ASD that moves in both directions.”

“There is also evidence of an association between atypical sensory features and anxiety in ASD (Ben-Sasson et al., 2009; Green & Ben-Sasson, 2010; Green, Ben-Sasson, Soto, & Carter, 2012; Pfeiffer, Kinnealey, Reed, & Hertzberg, 2005).”

“…with ASD, and sensory symptoms correlate with anxiety severity in children with ASD (Ben-Sasson et al., 2008), although the potential causal linkages and direction of effects between anxiety and sensory over-responsivity in ASD have not yet been fully determined (Green and Ben-Sasson, 2010).”

“A number of correlational studies have shown that children with ASD and SOR also have high rates of anxiety symptoms.(6,13,16) Because SOR co-occurs frequently with anxiety symptoms, theories related to abnormal amygdala and hippocampus functioning are particularly relevant, given the role of these structures in anxie…”

“In this hypervigilant state, individuals may be more likely to notice and respond to aversive sensory stimuli, and less likely to successfully disengage from potentially threatening sensory stimuli (Green and Ben-Sasson 2010).”

“Whereas SPD, like misophonia, is not delineated as a discrete DSM-5 disorder or ICD-10 condition, and has commonly received attention in the field of occupational therapy, auditory sensory over-responsivity shares some similar phenotypic signs and symptoms to those expressed by individuals with misophonia.”

“…is also emerging of the relationship between anxiety and ASD-specific factors, including impoverished empathy and social skills (Bellini, 2004), theory of mind and central coherence difficulties (Burnette, et al., 2005) and sensory over-sensitivity and responsivity (Green and Ben-Sasson, 2010).”

“Recent work from our laboratories and others has shown a strong link between sensory sensitivity and anxiety (Black et al. in press; Green and Ben-Sasson, 2010; Green et al., 2012; Lidstone et al., 2014), for example.”

“In addition, individuals with ASD have been shown to experience sensory hyper-sensitivity, which in turn may cause them to feel more agitated, hypervigilant, and generally aroused (Green & Ben-Sasson, 2010).”

“It is not known whether sensory features serve as a causal factor for the development of anxiety [Green & Ben-Sasson, 2010], whether both might be a consequence of common underlying pathology such as amygdala dysregulation, and how sensory features relate to cognitive processes and traits such as,…”

“The relationship be-tween anxiety and SOR has rarely been addressed, although recently Green and Ben-Sasson (2010) presented both causal and noncausal models to explain the development and maintenance of these conditions.”

“In terms of neurophysiology, a brain region hypothesised to be involved in sensory over-reactivity and hyperattention in ASC is the amygdala [39].”

“Sensory sensitivities, a type of RRBs, can also lead to specific phobias focused on that sensory stimulus (Green & Ben-Sasson, 2010).”

“Linked with increased levels of anxiety, the rigidity associated with I/S has been theorized to exacerbate and compound distress (Green and Ben-Sasson 2010).”

“Indeed, amygdalar abnormalities typically associated with difficulties with fear extinction (Davis, 1992, 2000), also involve disturbances in social anxiety, hyperarousal, and sensory over-responsivity in ASDs (Amaral et al., 2008; Green and Ben-Sasson, 2010).”

“Green and Ben-Sasson (2010) suggest that responses to particular sensory input may be conditioned through repeated exposure, leading to the expectation of being calmed and a shift in affective state.”

“Green and Ben-Sasson (2010) suggest that sensory over-responsivity is a common feature found in more than one-half of individuals on the autistic spectrum and is also often linked to anxiety and isolation.”

“Green and Ben-Sasson (2010) recently proposed three possible pathways linking anxiety and sensory over-responsivity in children with ASD: (a) anxiety causes sensory over-responsivity, (b) sensory over-responsivity causes anxiety, and (c) anxiety and overresponsivity are causally related by a common…”

“…covariance between SOR and internalizing than externalizing symptoms is perhaps unsurprising in the light of previous studies showing children (typical and atypical) who display elevated symptoms of SOR also tend to be at elevated risk for anxiety (Goldsmith et al., 2006; Green & Ben-Sasson, 2010).”

“Reciprocally, occupational herapists need to be aware of the potential for o-occurring psychopathology among children ith SOR.”

“…et al., 2018), repetitive behaviors (Boyd et al., 2010; Glod et al., 2019; Lidstone et al., 2014; Wigham et al., 2015), increased anxiety (S. A. Green & Ben-Sasson, 2010; S. A. Green et al., 2012; S. J. Lane et al., 2012; Lidstone et al., 2014; Wigham et al., 2015) and sensorimotor coupling…”

“These findings tentatively suggest that sensory sensitivity and aversive sensory experiences in the general population might lead to increased symptoms of worry, possibly through avoidance, hyper-vigilance, hyper-arousal and contextualized conditioning (see Grillon 2008; Green and Ben-Sasson 2010).”

“Given the crosssectional design of these studies, it is difficult to determine whether this relationship is uni- or bi-directional or whether these two variables are simply associated through other common risk factors (see Gotham et al., 2013; Green and Ben-Sasson, 2010; Kerns and Kendall, 2012; Lidstone et al., 2014).”

“…in line with previous findings our results show a significant relationship between sensory hyperreactivity and separation anxiety and phobia/physical injury fears, but not social anxiety [Black et al., 2017; Green & Ben-Sasson, 2010; Kerns et al., 2014; Spain et al., 2018; White et al., 2009].”

“In terms of possible structural mechanisms, Green and Ben-Sasson (2010) cited replicated evidence for amygdala abnormalities among individuals with autism, and suggested that these may play a role in both sensory hyperresponsiveness and anxiety in autism, symptoms associated with autonomic…”

“2009) compared to 3–24% of typically developing children (Green and Ben-Sasson 2010).”

“More work is needed to clarify the relationship between sensory sensitivity and anxiety, but it appears that sensory sensitivity, like anxiety, may be both state- and trait-like (e.g., Green & Ben-Sasson, 2010).”

“Anxiety disorders are more common in individuals with ASD than controls, and are closely related to sensory overresponsivity (Green and Ben-Sasson 2010).”

“Based on studies of the circuit mechanisms underlying auditory hypersensitivity in FXS, we emphasize a “quadruple hit” model to explain auditory hypersensitivity: (1) individual cortical neurons are hyper-responsive to sounds (59, 60); (2) more cortical neurons respond synchronously to the same sound (60); (3) habitua…”

“, 2009), the presence of which is associated with or possibly even caused by sensory hyperreactivity (Green and Ben-Sasson, 2010; Lane et al., 2012).”

“Compared with typically developing youth, anxiety in ASD may be triggered by ASDspecific stressors (i.e., sensory overload, disruption to routines or social interaction difficulties; see Bellini 2004; Ben-Sasson et al. 2008; Green and Ben-Sasson 2010; Ozsivadjian et al. 2012; Pfeiffer et al. 2005; Wood and Gadow 2010)…”

“Given that heightened sensitivity to environmental stimulation and difficulties in sensory modulation are related to anxiety in individuals with ASD (Green & Ben-Sasson, 2010; Pfeiffer Kinnealey, Reed, & Herzberg, 2005), it is not surprising that specific phobias involving adverse sensory…”

“Anxiety symptoms were used as a covariate in these analyses because of their high comorbidity with SOR [Green & Ben-Sasson, 2010; Ben-Sasson et al., 2008], and their correlation with SOR in the ASD sample (r = 0.31, p = .05).”

“31 The primary anxiety model proposes anxiety to be a cause of sensory hyperreactivity, as individuals may be more likely to be conditioned to attend and overreact to sensory input due to characteristics of anxiety (e.g., hypervigilance, hyperarousal, attentional bias, and avoidance).”

“…anxiety, and depression in autism I reviewed studies seeking to assess the relationship between sensory differences in the autistic population and their relationship to stress (Elwin, Schroder, Ek, Wallsten, & Kjellin, 2016; Green & Ben-Sasson, 2010; Horder, Wilson, Mendez, & Murphy, 2014).”

“This experience allows children with ASD to be familiar with the new foods [48,49].”

“Our results echo the established understanding of the relationship between sensory hyper-reactivity and anxiety (Green et al., 2012; Green & Ben-Sasson, 2010; Liss et al., 2005; MacLennan et al., 2020) and our combined data also shows more broadly a relationship of hyper-reactivity and…”

“Another characteristic of studies in this area is a reliance on questionnaires including parent-report surveys (16, 17, 20, 34, 40) or self-report surveys (19, 31, 41).”