Skip to main content
Top
Published in: Journal of Neurodevelopmental Disorders 1/2016

Open Access 01-12-2016 | Research

A functional neuroimaging study of fusiform response to restricted interests in children and adolescents with autism spectrum disorder

Authors: Jennifer H. Foss-Feig, Rankin W. McGugin, Isabel Gauthier, Lisa E. Mash, Pamela Ventola, Carissa J. Cascio

Published in: Journal of Neurodevelopmental Disorders | Issue 1/2016

Login to get access

Abstract

Background

While autism spectrum disorder (ASD) is characterized by both social communication deficits and restricted and repetitive patterns of behavior and interest, literature examining possible neural bases of the latter class of symptoms is limited. The fusiform face area (FFA) is a region in the ventral temporal cortex that not only shows preferential responsiveness to faces but also responds to non-face objects of visual expertise. Because restricted interests in ASD are accompanied by high levels of visual expertise, the objective of this study was to determine the extent to which this region responds to images related to restricted interests in individuals with ASD, compared to individuals without ASD who have a strong hobby or interest.

Methods

Children and adolescents with and without ASD with hobbies or interests that consumed a pre-determined minimum amount of time were identified, and the intensity, frequency, and degree of interference of these interests were quantified. Each participant underwent functional magnetic resonance imaging (fMRI) while viewing images related to their personal restricted interests (in the ASD group) or strong interest or hobby (in the comparison group). A generalized linear model was used to compare the intensity and spatial extent of fusiform gyrus response between groups, controlling for the appearance of faces in the stimuli.

Results

Images related to interests and expertise elicited response in FFA in both ASD and typically developing individuals, but this response was more robust in ASD.

Conclusions

These findings add neurobiological support to behavioral observations that restricted interests are associated with enhanced visual expertise in ASD, above and beyond what would be expected for simply a strong interest. Further, the results suggest that brain regions associated with social functioning may not be inherently less responsive in ASD, but rather may be recruited by different environmental stimuli. This study contributes to our understanding of the neural basis of restricted interests in ASD and may provide clues toward developing novel interventions.
Appendix
Available only for authorised users
Literature
1.
go back to reference American Psychiatric Association. Diagnostic and statistical manual of mental disorders (DSM-5®). American Psychiatric Pub, 2013. American Psychiatric Association. Diagnostic and statistical manual of mental disorders (DSM-5®). American Psychiatric Pub, 2013.
2.
go back to reference Bernstein M, Yovel G. Two neural pathways of face processing: a critical evaluation of current models. Neurosci Biobehav Rev. 2015;55:536–46.PubMedCrossRef Bernstein M, Yovel G. Two neural pathways of face processing: a critical evaluation of current models. Neurosci Biobehav Rev. 2015;55:536–46.PubMedCrossRef
3.
go back to reference Brett M, Anton J-L, Valabregue R, Poline J-B. Region of interest analysis using the MarsBar toolbox for SPM 99. Neuroimage. 2002;16(2):S497. Brett M, Anton J-L, Valabregue R, Poline J-B. Region of interest analysis using the MarsBar toolbox for SPM 99. Neuroimage. 2002;16(2):S497.
6.
go back to reference Chawarska K, Macari S, Shic F. Decreased spontaneous attention to social scenes in 6-month-old infants later diagnosed with autism spectrum disorders. Biol Psychiatry. 2013;74(3):195–203. http://dx.doi.org/10.1016/j.biopsych.2012.11.022.PubMedPubMedCentralCrossRef Chawarska K, Macari S, Shic F. Decreased spontaneous attention to social scenes in 6-month-old infants later diagnosed with autism spectrum disorders. Biol Psychiatry. 2013;74(3):195–203. http://​dx.​doi.​org/​10.​1016/​j.​biopsych.​2012.​11.​022.​PubMedPubMedCentralCrossRef
8.
go back to reference Critchley HD, Daly EM, Bullmore ET, Williams SC, Van Amelsvoort T, Robertson DM, Howlin P. The functional neuroanatomy of social behaviour changes in cerebral blood flow when people with autistic disorder process facial expressions. Brain. 2000;123(11):2203–12.PubMedCrossRef Critchley HD, Daly EM, Bullmore ET, Williams SC, Van Amelsvoort T, Robertson DM, Howlin P. The functional neuroanatomy of social behaviour changes in cerebral blood flow when people with autistic disorder process facial expressions. Brain. 2000;123(11):2203–12.PubMedCrossRef
9.
go back to reference Dawson G, Carver L, Meltzoff AN, Panagiotides H, McPartland J, Webb SJ. Neural correlates of face and object recognition in young children with autism spectrum disorder, developmental delay, and typical development. Child Dev. 2002;73(3):700–17.PubMedPubMedCentralCrossRef Dawson G, Carver L, Meltzoff AN, Panagiotides H, McPartland J, Webb SJ. Neural correlates of face and object recognition in young children with autism spectrum disorder, developmental delay, and typical development. Child Dev. 2002;73(3):700–17.PubMedPubMedCentralCrossRef
10.
go back to reference Dawson G, Webb SJ, McPartland J. Understanding the nature of face processing impairment in autism: insights from behavioral and electrophysiological studies. Dev Neuropsychol. 2005;27(3):403–24.PubMedCrossRef Dawson G, Webb SJ, McPartland J. Understanding the nature of face processing impairment in autism: insights from behavioral and electrophysiological studies. Dev Neuropsychol. 2005;27(3):403–24.PubMedCrossRef
11.
go back to reference Dawson G, Webb SJ, Wijsman E, Schellenberg G, Estes A, Munson J, Faja S. Neurocognitive and electrophysiological evidence of altered face processing in parents of children with autism: Implications for a model of abnormal development of social brain circuitry in autism. Dev Psychopathol. 2005;17:679–97.PubMedCrossRef Dawson G, Webb SJ, Wijsman E, Schellenberg G, Estes A, Munson J, Faja S. Neurocognitive and electrophysiological evidence of altered face processing in parents of children with autism: Implications for a model of abnormal development of social brain circuitry in autism. Dev Psychopathol. 2005;17:679–97.PubMedCrossRef
12.
go back to reference Delmonte S, Balsters JH, McGrath J, Fitzgerald J, Brennan S, Fagan AJ, Gallagher L. Social and monetary reward processing in autism spectrum disorders. Molecular autism. 2012;3(7):1–13. Delmonte S, Balsters JH, McGrath J, Fitzgerald J, Brennan S, Fagan AJ, Gallagher L. Social and monetary reward processing in autism spectrum disorders. Molecular autism. 2012;3(7):1–13.
13.
go back to reference Dichter GS. Functional magnetic resonance imaging of autism spectrum disorders. Dialogues Clin Neurosci. 2012;14(3):319.PubMedPubMedCentral Dichter GS. Functional magnetic resonance imaging of autism spectrum disorders. Dialogues Clin Neurosci. 2012;14(3):319.PubMedPubMedCentral
17.
go back to reference Elison JT, Sasson NJ, Turner-Brown LM, Dichter GS, Bodfish JW. Age trends in visual exploration of social and nonsocial information in children with autism. Research in autism spectrum disorders. 2012;6(2):842–51.PubMedPubMedCentralCrossRef Elison JT, Sasson NJ, Turner-Brown LM, Dichter GS, Bodfish JW. Age trends in visual exploration of social and nonsocial information in children with autism. Research in autism spectrum disorders. 2012;6(2):842–51.PubMedPubMedCentralCrossRef
18.
go back to reference Forman SD, Cohen JD, Fitzgerald M, Eddy WF, Mintun MA, Noll DC. Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn Reson Med. 1995;33(5):636–47.PubMedCrossRef Forman SD, Cohen JD, Fitzgerald M, Eddy WF, Mintun MA, Noll DC. Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn Reson Med. 1995;33(5):636–47.PubMedCrossRef
19.
go back to reference Gauthier I, Skudlarski P, Gore JC, Anderson AW. Expertise for cars and birds recruits brain areas involved in face recognition. Nat Neurosci. 2000;3(2):191–7.PubMedCrossRef Gauthier I, Skudlarski P, Gore JC, Anderson AW. Expertise for cars and birds recruits brain areas involved in face recognition. Nat Neurosci. 2000;3(2):191–7.PubMedCrossRef
20.
go back to reference Grelotti DJ, Gauthier I, Schultz RT. Social interest and the development of cortical face specialization: what autism teaches us about face processing. Dev Psychobiol. 2002;40(3):213–25.PubMedCrossRef Grelotti DJ, Gauthier I, Schultz RT. Social interest and the development of cortical face specialization: what autism teaches us about face processing. Dev Psychobiol. 2002;40(3):213–25.PubMedCrossRef
24.
go back to reference Johnson MH, Griffin R, Csibra G, Halit H, Farroni T, De Haan M, Richards J. The emergence of the social brain network: Evidence from typical and atypical development. Dev Psychopathol. 2005;17(03):599–619.PubMedPubMedCentralCrossRef Johnson MH, Griffin R, Csibra G, Halit H, Farroni T, De Haan M, Richards J. The emergence of the social brain network: Evidence from typical and atypical development. Dev Psychopathol. 2005;17(03):599–619.PubMedPubMedCentralCrossRef
25.
go back to reference Kanwisher N, McDermott J, Chun MM. The fusiform face area: a module in human extrastriate cortex specialized for face perception. J Neurosci. 1997;17(11):4302–11.PubMed Kanwisher N, McDermott J, Chun MM. The fusiform face area: a module in human extrastriate cortex specialized for face perception. J Neurosci. 1997;17(11):4302–11.PubMed
26.
go back to reference Kanwisher N, Yovel G. The fusiform face area: a cortical region specialized for the perception of faces. Philosophical Transactions of the Royal Society B: Biological Sciences. 2006;361(1476):2109–28.CrossRef Kanwisher N, Yovel G. The fusiform face area: a cortical region specialized for the perception of faces. Philosophical Transactions of the Royal Society B: Biological Sciences. 2006;361(1476):2109–28.CrossRef
27.
go back to reference Kimko HC, Cross JT, Abernethy DR. Pharmacokinetics and clinical effectiveness of methylphenidate. Clin Pharmacokinet. 1999;37(6):457–70.PubMedCrossRef Kimko HC, Cross JT, Abernethy DR. Pharmacokinetics and clinical effectiveness of methylphenidate. Clin Pharmacokinet. 1999;37(6):457–70.PubMedCrossRef
28.
go back to reference Kirk U, Skov M, Christensen MS, Nygaard N. Brain correlates of aesthetic expertise: a parametric fMRI study. Brain Cogn. 2009;69(2):306–15.PubMedCrossRef Kirk U, Skov M, Christensen MS, Nygaard N. Brain correlates of aesthetic expertise: a parametric fMRI study. Brain Cogn. 2009;69(2):306–15.PubMedCrossRef
30.
go back to reference Klin A, Jones W, Schultz R, Volkmar F, Cohen D. Defining and quantifying the social phenotype in autism. Am J Psychiatry. 2002;159:895–908.PubMedCrossRef Klin A, Jones W, Schultz R, Volkmar F, Cohen D. Defining and quantifying the social phenotype in autism. Am J Psychiatry. 2002;159:895–908.PubMedCrossRef
31.
go back to reference Kuhl PK, Coffey-Corina S, Padden D, Dawson G. Links between social and linguistic processing of speech in preschool children with autism: behavioral and electrophysiological measures. Dev Sci. 2005;8(1):F1–12.PubMedCrossRef Kuhl PK, Coffey-Corina S, Padden D, Dawson G. Links between social and linguistic processing of speech in preschool children with autism: behavioral and electrophysiological measures. Dev Sci. 2005;8(1):F1–12.PubMedCrossRef
33.
go back to reference Lord C, Risi S, Lambrecht L, Cook Jr EH, Leventhal BL, DiLavore PC, Rutter M. The autism diagnostic observation schedule-generic: a standard measure of social and communication deficits associated with the spectrum of autism. J Autism Dev Disord. 2000;30(3):205–23.PubMedCrossRef Lord C, Risi S, Lambrecht L, Cook Jr EH, Leventhal BL, DiLavore PC, Rutter M. The autism diagnostic observation schedule-generic: a standard measure of social and communication deficits associated with the spectrum of autism. J Autism Dev Disord. 2000;30(3):205–23.PubMedCrossRef
34.
go back to reference Lord C, Rutter M, Le Couteur A. Autism Diagnostic Interview-Revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. J Autism Dev Disord. 1994;24(5):659–85.PubMedCrossRef Lord C, Rutter M, Le Couteur A. Autism Diagnostic Interview-Revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. J Autism Dev Disord. 1994;24(5):659–85.PubMedCrossRef
36.
go back to reference Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage. 2003;19(3):1233–9.PubMedCrossRef Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage. 2003;19(3):1233–9.PubMedCrossRef
37.
go back to reference McGugin RW, Gatenby JC, Gore JC, Gauthier I. High-resolution imaging of expertise reveals reliable object selectivity in the fusiform face area related to perceptual performance. Proc Natl Acad Sci. 2012;109(42):17063–8.PubMedPubMedCentralCrossRef McGugin RW, Gatenby JC, Gore JC, Gauthier I. High-resolution imaging of expertise reveals reliable object selectivity in the fusiform face area related to perceptual performance. Proc Natl Acad Sci. 2012;109(42):17063–8.PubMedPubMedCentralCrossRef
39.
go back to reference McPartland JC, Crowley MJ, Perszyk DR, Mukerji CE, Naples AJ, Wu J, Mayes LC. Preserved reward outcome processing in ASD as revealed by event-related potentials. J Neurodevelopmental Disord. 2012;4(16):1–9. McPartland JC, Crowley MJ, Perszyk DR, Mukerji CE, Naples AJ, Wu J, Mayes LC. Preserved reward outcome processing in ASD as revealed by event-related potentials. J Neurodevelopmental Disord. 2012;4(16):1–9.
40.
go back to reference Mundy P, Neal R. Neural plasticity, joint attention and autistic developmental pathology. International review of research in mental retardation. 2001;23:139–68.CrossRef Mundy P, Neal R. Neural plasticity, joint attention and autistic developmental pathology. International review of research in mental retardation. 2001;23:139–68.CrossRef
44.
go back to reference Philip RC, Dauvermann MR, Whalley HC, Baynham K, Lawrie SM, Stanfield AC. A systematic review and meta-analysis of the fMRI investigation of autism spectrum disorders. Neurosci Biobehav Rev. 2012;36(2):901–42.PubMedCrossRef Philip RC, Dauvermann MR, Whalley HC, Baynham K, Lawrie SM, Stanfield AC. A systematic review and meta-analysis of the fMRI investigation of autism spectrum disorders. Neurosci Biobehav Rev. 2012;36(2):901–42.PubMedCrossRef
46.
go back to reference Pinsk MA, Arcaro M, Weiner KS, Kalkus JF, Inati SJ, Gross CG, Kastner S. Neural representations of faces and body parts in macaque and human cortex: a comparative FMRI study. J Neurophysiol. 2009;101(5):2581–600.PubMedPubMedCentralCrossRef Pinsk MA, Arcaro M, Weiner KS, Kalkus JF, Inati SJ, Gross CG, Kastner S. Neural representations of faces and body parts in macaque and human cortex: a comparative FMRI study. J Neurophysiol. 2009;101(5):2581–600.PubMedPubMedCentralCrossRef
47.
go back to reference Rutter M, Bailey A, & Lord C. The social communication questionnaire. Los Angeles: Western Psychological Services. 2003 Rutter M, Bailey A, & Lord C. The social communication questionnaire. Los Angeles: Western Psychological Services. 2003
49.
go back to reference Sasson NJ, Elison JT, Turner-Brown LM, Dichter GS, Bodfish JW. Brief report: circumscribed attention in young children with autism. J Autism Dev Disord. 2011;41(2):242–7.PubMedPubMedCentralCrossRef Sasson NJ, Elison JT, Turner-Brown LM, Dichter GS, Bodfish JW. Brief report: circumscribed attention in young children with autism. J Autism Dev Disord. 2011;41(2):242–7.PubMedPubMedCentralCrossRef
50.
go back to reference Sasson NJ, & Touchstone EW. Visual attention to competing social and object images by preschool children with autism spectrum disorder. Journal of autism and developmental disorders. 2014;44(3):584-592. Sasson NJ, & Touchstone EW. Visual attention to competing social and object images by preschool children with autism spectrum disorder. Journal of autism and developmental disorders. 2014;44(3):584-592.
51.
go back to reference Sasson NJ, Turner-Brown LM, Holtzclaw TN, Lam KS, Bodfish JW. Children with autism demonstrate circumscribed attention during passive viewing of complex social and nonsocial picture arrays. Autism Res. 2008;1(1):31–42.PubMedCrossRef Sasson NJ, Turner-Brown LM, Holtzclaw TN, Lam KS, Bodfish JW. Children with autism demonstrate circumscribed attention during passive viewing of complex social and nonsocial picture arrays. Autism Res. 2008;1(1):31–42.PubMedCrossRef
52.
go back to reference Scherf KS, Elbich D, Minshew N, Behrmann M. Individual differences in symptom severity and behavior predict neural activation during face processing in adolescents with autism. NeuroImage: Clinical. 2015;7:53–67.CrossRef Scherf KS, Elbich D, Minshew N, Behrmann M. Individual differences in symptom severity and behavior predict neural activation during face processing in adolescents with autism. NeuroImage: Clinical. 2015;7:53–67.CrossRef
53.
go back to reference Scherf KS, Luna B, Minshew N, Behrmann M. Location, location, location: alterations in the functional topography of face-but not object-or place-related cortex in adolescents with autism. Front Hum Neurosci. 2010;4:26.PubMedPubMedCentral Scherf KS, Luna B, Minshew N, Behrmann M. Location, location, location: alterations in the functional topography of face-but not object-or place-related cortex in adolescents with autism. Front Hum Neurosci. 2010;4:26.PubMedPubMedCentral
56.
go back to reference Schultz RT, Gauthier I, Klin A, Fulbright RK, Anderson AW, Volkmar F, Gore JC. Abnormal ventral temporal cortical activity during face discrimination among individuals with autism and Asperger syndrome. Arch Gen Psychiatry. 2000;57(4):331–40.PubMedCrossRef Schultz RT, Gauthier I, Klin A, Fulbright RK, Anderson AW, Volkmar F, Gore JC. Abnormal ventral temporal cortical activity during face discrimination among individuals with autism and Asperger syndrome. Arch Gen Psychiatry. 2000;57(4):331–40.PubMedCrossRef
57.
59.
go back to reference South M, Klin A, & Ozonoff S. (1999). The Yale Special Interests Interview. Unpublished Work. South M, Klin A, & Ozonoff S. (1999). The Yale Special Interests Interview. Unpublished Work.
60.
go back to reference South M, Ozonoff S, Suchy Y, Kesner RP, McMahon WM, Lainhart JE. Intact emotion facilitation for nonsocial stimuli in autism: Is amygdala impairment in autism specific for social information? 2008. South M, Ozonoff S, Suchy Y, Kesner RP, McMahon WM, Lainhart JE. Intact emotion facilitation for nonsocial stimuli in autism: Is amygdala impairment in autism specific for social information? 2008.
61.
go back to reference Tarr MJ, Gauthier I. FFA: a flexible fusiform area for subordinate-level visual processing automatized by expertise. Nat Neurosci. 2000;3(8):764–9.PubMedCrossRef Tarr MJ, Gauthier I. FFA: a flexible fusiform area for subordinate-level visual processing automatized by expertise. Nat Neurosci. 2000;3(8):764–9.PubMedCrossRef
63.
go back to reference Ventola P, Friedman HE, Anderson LC, Wolf JM, Oosting D, Foss-Feig J, Pelphrey KA. Improvements in social and adaptive functioning following short-duration PRT program: a clinical replication. J Autism Dev Disord. 2014;44(11):2862–70.PubMedCrossRef Ventola P, Friedman HE, Anderson LC, Wolf JM, Oosting D, Foss-Feig J, Pelphrey KA. Improvements in social and adaptive functioning following short-duration PRT program: a clinical replication. J Autism Dev Disord. 2014;44(11):2862–70.PubMedCrossRef
64.
go back to reference Ventola P, Yang DY, Friedman HE, Oosting D, Wolf J, Sukhodolsky DG, & Pelphrey KA. Heterogeneity of neural mechanisms of response to pivotal response treatment. Brain Imaging and Behavior. 2015;9(1):74-88. Ventola P, Yang DY, Friedman HE, Oosting D, Wolf J, Sukhodolsky DG, & Pelphrey KA. Heterogeneity of neural mechanisms of response to pivotal response treatment. Brain Imaging and Behavior. 2015;9(1):74-88.
65.
go back to reference Watson JD, Myers R, Frackowiak RS, Hajnal JV, Woods RP, Mazziotta JC, Zeki S. Area V5 of the human brain: evidence from a combined study using positron emission tomography and magnetic resonance imaging. Cereb Cortex. 1993;3(2):79–94.PubMedCrossRef Watson JD, Myers R, Frackowiak RS, Hajnal JV, Woods RP, Mazziotta JC, Zeki S. Area V5 of the human brain: evidence from a combined study using positron emission tomography and magnetic resonance imaging. Cereb Cortex. 1993;3(2):79–94.PubMedCrossRef
66.
go back to reference Weiner KS, Grill-Spector K. Sparsely-distributed organization of face and limb activations in human ventral temporal cortex. Neuroimage. 2010;52(4):1559–73.PubMedPubMedCentralCrossRef Weiner KS, Grill-Spector K. Sparsely-distributed organization of face and limb activations in human ventral temporal cortex. Neuroimage. 2010;52(4):1559–73.PubMedPubMedCentralCrossRef
67.
go back to reference Whyte EM, Behrmann M, Minshew NJ, Garcia NV, Scherf KS. Animal, but not human, faces engage the distributed face network in adolescents with autism. Dev Sci. 2015. Whyte EM, Behrmann M, Minshew NJ, Garcia NV, Scherf KS. Animal, but not human, faces engage the distributed face network in adolescents with autism. Dev Sci. 2015.
Metadata
Title
A functional neuroimaging study of fusiform response to restricted interests in children and adolescents with autism spectrum disorder
Authors
Jennifer H. Foss-Feig
Rankin W. McGugin
Isabel Gauthier
Lisa E. Mash
Pamela Ventola
Carissa J. Cascio
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Journal of Neurodevelopmental Disorders / Issue 1/2016
Print ISSN: 1866-1947
Electronic ISSN: 1866-1955
DOI
https://doi.org/10.1186/s11689-016-9149-6

Other articles of this Issue 1/2016

Journal of Neurodevelopmental Disorders 1/2016 Go to the issue