Atypical Amygdala Response to Fear Conditioning in Autism Spectrum Disorder

Top, David; Stephenson, Kevin G.; Doxey, Christopher R.; Crowley, Michael J.; Kirwan, C. Brock; South, Mikle

doi:10.1016/j.bpsc.2016.01.008

Cited by 28 publications

(15 citation statements)

References 56 publications

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“…This idea was also suggested by the first ever fMRI study of fear conditioning in autism (43), where we found much stronger amygdala activation to threat vs. safe cues in a neurotypical adult sample, but significantly reduced differentiation between threat and safe in the autistic sample. We wondered whether elevated baseline arousal—either in everyday life and/or as a function of the intense sensory environment of the MRI setting—provided a sort of ceiling effect for amygdala activation so that additional, task-based activation was less likely.…”

Section: Discussionsupporting

confidence: 80%

“…It may be that increased task demands could over-tax sensory integration systems, as suggested by fMRI studies from Green et al (52, 53) who sowed atypical sensory response only for simultaneous stimulation of multiple sensory systems, and not for single sensory modalities presented separately. Possible questions for future research include: Could it be that chronically elevated physiological arousal, and/or an elevated response to lab-based stressors, could modulate findings in habituation studies (43)? Is habituation decreased for unimodal sensory stimulation (i.e., only auditory or only tactile) or do difficulties appear only in the integration of multiple stimuli at once (as is common in real life) (52)?…”

Section: Discussionmentioning

confidence: 99%

“…In that study greater sensory dysfunction was associated with increased stress, and diagnosis was a significant moderator of the relationship between sensory function and stress response. An emerging idea from our lab and the work of others is that everyday psychophysiological arousal may be elevated in autism (35, 42, 43). We do not know of any studies that examine possible links between ambulatory arousal and sensory and/or emotional sensitivity.…”

Section: Introductionmentioning

confidence: 99%

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Psychophysiological Arousal and Auditory Sensitivity in a Cross-Clinical Sample of Autistic and Non-autistic Anxious Adults

et al. 2019

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Many autistic people report overwhelming sensory experiences and also elevated levels of anxiety. Understanding how these experiences are linked to each other can contribute to improved support and intervention for reducing sensory overload and anxiety. This study included 95 young adult participants including autistic adults, non-autistic adults reporting to a psychotherapy clinic with high levels of anxiety, and neurotypical adults with no psychiatric concerns. We measured pupil size using including a baseline task with no auditory stimulus followed by two blocks of simple auditory habituation. In a subset of 80 participants we also measured self-report levels of sensory processing, anxious apprehension, and intolerance of uncertainty. The autism group showed atypical sensory processing on all four measured domains of the Adolescent and Adult Sensory Profile including sensory sensitivity, sensory seeking, sensory avoidance, and low registration subscales. Dimensional analyses across all participants showed significant positive correlations between sensory sensitivity, sensory seeking, and sensory avoidance domains with scores from the Intolerance of Uncertainty Scale-Short Form and Penn State Worry Questionnaire. The autism group showed significantly larger pupil size than other groups at baseline, before any auditory stimulation. There were no group differences in the rate of auditory habituation, nonetheless the overall, absolute larger pupil size remained in the autism group throughout the experiment. We suggest that this and other findings could indicate chronic hyperarousal in many autistic people. Treatment for anxiety in autism should be informed by knowledge of unique aspects of anxiety in autism and consider the role of sensory experience and everyday psychophysiological arousal.

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Section: Discussionsupporting

confidence: 80%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Psychophysiological Arousal and Auditory Sensitivity in a Cross-Clinical Sample of Autistic and Non-autistic Anxious Adults

et al. 2019

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“…This same reasoning applies just as well to explanations for anxiety: reduced modulation of limbic activity via higher cortical systems may result in chronic, unchecked perception of threat and subsequent anxiety (Amaral et al, 2003). Top et al (2016) conducted an fMRI study of fear conditioning and extinction in adults with ASD, concluding that the ASD group failed to recognize safety cues, and thus were delayed in responding to changes between threat to safety contexts.…”

Section: Autism Anxiety and Integration Of Mpfcmentioning

confidence: 99%

Sensory, Emotional and Cognitive Contributions to Anxiety in Autism Spectrum Disorders

South

Rodgers

2017

Front. Hum. Neurosci.

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198

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Severe symptoms of anxiety add substantial additional burden to many individuals diagnosed with Autism Spectrum Disorder (ASD). Improved understanding of specific factors that contribute to anxiety in ASD can aid research regarding the causes of autism and also provide targets for more effective intervention. This mini-review article focuses on emerging evidence for three concepts that appear to be related to each other and which also strongly predict anxiety in ASD samples. Atypical sensory function is included in the diagnostic criteria for ASD and is likely an important contributor to anxiety. Difficulties in understanding and labeling emotions (alexithymia), although a co-morbidity, may arise in part from atypical sensory function and can lead to confusion and uncertainty about how to respond to social and emotional situations. Intolerance of uncertainty (IU) describes people who have a particularly hard time with ambiguity and is known to be a key mechanism underlying some anxiety disorders. While evidence for linking these ideas is to date incomplete, we put forward a model including each concept as a framework for future studies. Specifically, we propose that IU is a critical mediator for anxiety in ASD, and explore the relationships between sensory function, alexithymia and IU. We further explore the role of the medial prefrontal cortex (mPFC) in regulating emotional response, in connection with limbic and insula-based networks, and suggest that disrupted integration in these networks underlies difficulties with habituation to strong emotional stimuli, which results in an enhanced perception of threat in many people with ASD. Behavioral and biologically-based treatments for anxiety in ASD will benefit from attending to these specific mechanisms as adjunct to traditional interventions.

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“…Although no previous studies have examined SFL in individuals with ASD, a small number of studies suggest that autonomic indices of direct fear learning through Pavlovian conditioning are largely intact in this population [ 32 – 34 ], but reduced differentiation between threat and safety cues in amygdala activity has also been reported [ 35 ]. One study reported stronger SFL in neurotypical individuals with high levels of autistic traits [ 36 ].…”

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confidence: 99%

Enhanced social learning of threat in adults with autism

et al. 2020

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Background Recent theories have linked autism to challenges in prediction learning and social cognition. It is unknown, however, how autism affects learning about threats from others “demonstrators” through observation, which contains predictive learning based on social information. The aims of this study are therefore to investigate social fear learning in individual with autism spectrum disorder (ASD) and to examine whether typically developing social cognition is necessary for successful observational learning. Methods Adults with ASD (n = 23) and neurotypical controls (n = 25) completed a social fear learning (SFL) procedure in which participants watched a “demonstrator” receiving electrical shocks in conjunction with a previously neutral conditioned stimulus (CS+), but never with a safe control stimulus (CS−). Skin conductance was used to measure autonomic responses of learned threat responses to the CS+ versus CS−. Visual attention was measured during learning using eye tracking. To establish a non-social learning baseline, each participant also underwent a test of Pavlovian conditioning. Results During learning, individuals with ASD attended less to the demonstrator’s face, and when later tested, displayed stronger observational, but not Pavlovian, autonomic indices of learning (skin conductance) compared to controls. In controls, both higher levels of attention to the demonstrator’s face and trait empathy predicted diminished expressions of learning during test. Limitations The relatively small sample size of this study and the typical IQ range of the ASD group limit the generalizability of our findings to individuals with ASD in the average intellectual ability range. Conclusions The enhanced social threat learning in individuals with ASD may be linked to difficulties using visual attention and mental state attributions to downregulate their emotion.

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Atypical Amygdala Response to Fear Conditioning in Autism Spectrum Disorder

Cited by 28 publications

References 56 publications

Psychophysiological Arousal and Auditory Sensitivity in a Cross-Clinical Sample of Autistic and Non-autistic Anxious Adults

Psychophysiological Arousal and Auditory Sensitivity in a Cross-Clinical Sample of Autistic and Non-autistic Anxious Adults

Sensory, Emotional and Cognitive Contributions to Anxiety in Autism Spectrum Disorders

Enhanced social learning of threat in adults with autism

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