fMRI activation of the fusiform gyrus and amygdala to cartoon characters but not to faces in a boy with autism

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Abstract

Abnormal hypoactivation in the amygdala and fusiform gyrus, brain areas that participate in face processing and social cognition, has consistently been demonstrated in persons with autism. We investigated activity in these areas in a boy with autism, DD, who had a special interest in “Digimon” cartoon characters. DD individuates Digimon faster than familiar faces and objects, but he individuates familiar faces no faster than objects. In contrast, a typically developing boy with an interest in “Pokémon” cartoon characters is equally fast at individuating faces and Pokémon and faster at individuating faces and Pokémon than objects and Digimon. In addition, using functional magnetic resonance imaging (fMRI), we show that DD activates his amygdala and fusiform gyrus for perceptual discriminations involving Digimon but not for those involving familiar or unfamiliar faces. This pattern of activation is not seen in the typically developing control with an interest in Pokémon or in a second comparison case who has autism but no interest in Digimon. These results have important implications for our understanding of autism, cortical face specialization, and the possible role of the amygdala in the development of perceptual expertise.

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

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    1

    Present address: Johns Hopkins University School of Medicine, 733 North Broadway, Suite 137 MS2006, Baltimore, MD 21205, USA.

    2

    Deceased.

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