fMRI activation of the fusiform gyrus and amygdala to cartoon characters but not to faces in a boy with autism
Section snippets
Introduction and case history
Autism is a Pervasive Developmental Disorder (PDD) characterized by social impairments, deficits in the development of language, and the presence of stereotypic or repetitive behaviors (American Psychiatric Association, 1994). Individuals with autism also have significant deficits in face perception (reviewed in Grelotti, Gauthier, & Schultz, 2002). These deficits seem to be related to the social impairments at the core of autism (Klin, Sparrow, de Bildt, Cicchetti, Cohen, Volkmar, 1999;
Participants
Three subjects participated in some or all of the experiments described herein. DD watched the Digimon television show daily for 2 years, knew most of the characters’ names, spoke of good, bad, and lucky Digimon, and wished to become a “DigiDestined” like the cartoon children who train Digimon on the television show. He was 11 years old at the time of initial testing, and 12 years old at follow-up. DD's behavioral performance and fMRI activity was compared to two other boys matched to DD in
Neuropsychological and clinical evaluation
DD and CC met criteria for autism using all diagnostic instruments. The consensus of the experienced clinicians (AK, FRV) who evaluated the two patients was that they had a “classical” presentation, similar to those individuals with autism first described by Leo Kanner (1943). Clinicians using standard diagnostic instruments (i.e., the Autism Diagnostic Observation Schedule (ADOS) (Lord, Rutter, DiLavore, & Risi, 1999) and the Autism Diagnostic Interview—Revised (ADI-R) (Lord et al., 1994)
Behavioral testing
Using the forced-choice verification test, we wanted to measure differences in DD's responses to familiar faces, Digimon, and familiar nonface objects to assess his expertise for faces and Digimon. Generally, people can categorize objects faster at the basic level (e.g., “dog” or “car”) than at more specific levels (e.g., “beagle” or “Ford Explorer”). However, experts in a domain, such as dog or bird experts, can categorize objects at the individual level as fast as at the basic level (Tanaka &
Conclusion
Neither expertise effects for objects in the FFA (Gauthier et al., 1999b; Gauthier et al., 2000a) nor a lack of activity for faces in the FFA or amygdala of a person with autism (Critchley et al., 2000; Pierce et al., 2001; Schultz et al., 2000a) are new findings, but the combination of these findings and the amygdala activity to Digimon in the same person has important implications for the study of autism. It suggests that the FG and amygdala of individuals with autism function normally under
Acknowledgments
Donald Cohen, M.D., died in 2001. This article is dedicated to the memory of him: our mentor, collaborator, and colleague, whose legacy embodies the best in clinical services, public advocacy, and clinical science. The authors would like to thank the participants of the study and their families. We are grateful to Tammy Babitz, Jamie Kleinman, Hedy Serofin, Terry Hickey, Cheryl Klaiman, Diana Robbins, Warren Jones, James Tanaka, and the members of the Perceptual Expertise Network for their
References (75)
The contribution of the amygdala to normal and abnormal emotional states
Trends in Neuroscience
(1993)Medial temporal lobe structures and autism: A review of clinical and experimental findings
Neuropsychologia
(1994)- et al.
Response and habituation of the human amygdala during visual processing of facial expression
Neuron
(1996) - et al.
Brain systems mediating aversive conditioning: An event-related fMRI study
Neuron
(1998) - et al.
Functional-anatomic correlates of object priming in humans revealed by rapid presentation event-related fMRI
Neuron
(1998) - et al.
Movement and mind: A functional imaging study of perception and interpretation of complex intentional movement patterns
Neuroimage
(2000) Category-related recognition defects as a clue to the neural substrates of knowledge
Trends in Neurosciences
(1990)- et al.
Face perception and within-category discrimination in prosopagnosia
Neuropsychologia
(1995) - et al.
Levels of categorization in visual recognition studied using functional magnetic resonance imaging
Current Biology
(1997) - et al.
Seen gaze-direction modulates fusiform activity and its coupling with other brain areas during face processing
NeuroImage
(2001)
The effect of face inversion on activity in the human neural systems for face and object perception
Neuron
Neural response suppression, haemodynamic repetition effects, and behavioural priming
Neuropsychologia
Emotional attribution in high-functioning individuals with autistic spectrum disorder: A functional imaging study
Journal of the American Academy of Child & Adolescent Psychiatry
ROC analysis and statistical methods used in functional MRI: Individual subjects
NeuroImage
Object categories and expertise: Is the basic level in the eye of the beholder?
Cognitive Psychology
Neural correlates of facial affect processing in children and adolescents with autism spectrum disorder
Journal of the American Academy of Child & Adolescent Psychiatry
Preferences for visual stimuli following amygdala damage
Journal of Cognitive Neuroscience
Abnormal processing of social information from faces in autism
Journal of Cognitive Neuroscience
Diagnostic and statistical manual of mental disorders
Lesions of the human amygdala impair enhanced perception of emotionally salient events
Nature
Social intelligence in the normal and autistic brain: An fMRI study
European Journal of Neuroscience
Brief report: Neuroanatomic observations of the brain in pervasive developmental disorders
Journal of Autism and Developmental Disorders
Neuroanatomic observations of the brain in autism
Contribution to neuropsychological assessment
Autism, Asperger syndrome and brain mechanisms for the attribution of mental states to animated shapes
Brain
The understanding of the emotional meaning of facial expressions in people with autism
Journal of Autism and Developmental Disorders
Are face-responsive regions selective only for faces?
Neuroreport
Contextually evoked object-specific responses in human visual cortex
Science
The functional neuroanatomy of social behaviour: Changes in cerebral blood flow when people with autistic disorder process facial expressions
Brain
Face Agnosia and the Neural Substrates of Memory
Annual Review of Neuroscience
Developmental prosopagnosia with normal configural processing
Neuroreport
Early commitment of neural substrates for face recognition
Cognitive Neuropsychology
Comprehension of affect in context in children with pervasive developmental disorders
Journal of Child Psychology and Psychiatry
Can face recognition really be dissociated from object recognition?
Journal of Cognitive Neuroscience
Activation of the middle fusiform face area increases with expertise in recognizing novel objects
Nature Neuroscience
Expertise for cars and birds recruits brain areas involved in face recognition
Nature Neuroscience
The fusiform “face area” is part of a network that processes faces at the individual level
Journal of Cognitive Neuroscience
Cited by (183)
Emotion recognition across visual and auditory modalities in autism spectrum disorder: A systematic review and meta-analysis
2022, Developmental ReviewCitation Excerpt :Within the visual modality, difficulty in identifying and understanding emotions through facial expressions is the most common social-cognitive impairment in ASD (Eack, Mazefsky, & Minshew, 2015; Griffiths et al., 2019; Pelphrey et al., 2002; see Harms et al., 2010 for a discussion), despite contradictory evidence suggesting otherwise (Jones et al., 2011; Tracy, Robins, Schriber, & Solomon, 2011). In contrast, the ability to recognise emotions from nonhuman facial stimuli such as cartoons, caricatures, and schematic faces appears intact in ASD (Brosnan et al., 2015; Isomura et al., 2014; Miyahara, Bray, Tsujii, Fujita, & Sugiyama, 2007; Rosset et al., 2008), possibly because of autistic individuals’ greater or restricted interest in these stimuli (Anthony et al., 2013; Grelotti et al., 2005; Kuo, Orsmond, Coster, & Cohn, 2014; Rosset et al., 2008; Spiker, Lin, Van Dyke, & Wood, 2012). Within the auditory modality, studies investigating emotional prosody in ASD have yielded mixed findings, with some reporting clear impairments (e.g., Doi et al., 2013; Schelinski & von Kriegstein, 2019; Taylor, Maybery, Grayndler, & Whitehouse, 2015) and others reporting no impairments (e.g., Baker, Montgomery, & Abramson, 2010; Heikkinen et al., 2010).
Investigating the Influence of Autism Spectrum Traits on Face Processing Mechanisms in Developmental Prosopagnosia
2023, Journal of Autism and Developmental Disorders
- 1
Present address: Johns Hopkins University School of Medicine, 733 North Broadway, Suite 137 MS2006, Baltimore, MD 21205, USA.
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Deceased.