Skip to main content
Top
Gepubliceerd in: Journal of Autism and Developmental Disorders 12/2023

29-09-2022 | Original Paper

Investigating the Influence of Autism Spectrum Traits on Face Processing Mechanisms in Developmental Prosopagnosia

Auteurs: Regan Fry, Xian Li, Travis C. Evans, Michael Esterman, James Tanaka, Joseph DeGutis

Gepubliceerd in: Journal of Autism and Developmental Disorders | Uitgave 12/2023

Log in om toegang te krijgen
share
DELEN

Deel dit onderdeel of sectie (kopieer de link)

  • Optie A:
    Klik op de rechtermuisknop op de link en selecteer de optie “linkadres kopiëren”
  • Optie B:
    Deel de link per e-mail

Abstract

Autism traits are common exclusionary criteria in developmental prosopagnosia (DP) studies. We investigated whether autism traits produce qualitatively different face processing in 43 DPs with high vs. low autism quotient (AQ) scores. Compared to controls (n = 27), face memory and perception were similarly deficient in the high- and low-AQ DPs, with the high-AQ DP group additionally showing deficient face emotion recognition. Task-based fMRI revealed reduced occipito-temporal face selectivity in both groups, with high-AQ DPs additionally demonstrating decreased posterior superior temporal sulcus selectivity. Resting-state fMRI showed similar reduced face-selective network connectivity in both DP groups compared with controls. Together, this demonstrates that high- and low-AQ DP groups have very similar face processing deficits, with additional facial emotion deficits in high-AQ DPs.
Voetnoten
1
Though the term ‘face recognition’ has been used to describe both face memory and face perception (e.g., Benton Face Recognition Test), in the present study we use the term to refer to face memory.
 
2
Although labeled ‘developmental prosopagnosics’, the diagnostic criteria were less strict than typically used in prosopagnosia studies and included individuals who did not self-report face recognition difficulties. Including individuals who had z-scores < -2 on the CFMT and who self-reported face recognition deficits on the PI20 would result in 12% of their sample having DP, which is still far greater than expected in the general population.
 
3
SDD in this study encompasses autism, Asperger’s, and pervasive developmental disorder—not otherwise specified. As of 2013, according to the DSM-5, these disorders are included under the diagnosis of autism spectrum disorder.
 
4
A 102-person age- and gender-matched control group collected after this study was completed had an average RMET score of 28.80 (SD = 3.57). This score was significantly higher than that of the AQ+ DP group (p = .016) but did not differ from the AQ- DP group (p = .606). Details describing this later control group are included in the supplementary materials.
 
5
Because 11 of the DPs in the AQ+ group had AQ scores below the standard clinical cut-off of 32 (Woodbury-Smith et al., 2005) suggestive of mild ASD traits, we also ran exploratory analyses on a smaller group of DPs with AQ scores equal to or above 32 (N = 4), comparing them with the AQ- group measures to evaluate if there were any behavioral differences in the group that fell above the clinical cut-off. These analyses showed very similar results and can be found in the supplementary materials.
 
6
Because our main control group was not given the RMET (see footnote 4) and z-scores were calculated using the main control group as the normative data, the RMET is excluded from this figure.
 
Literatuur
go back to reference Auyeung, B., Lombardo, M. V., Heinrichs, M., Chakrabarti, B., Sule, A., Deakin, J. B., Bethlehem, R. A. I., Dickens, L., Mooney, N., Sipple, J. A. N., Thiemann, P., & Baron-Cohen, S. (2015). Oxytocin increases eye contact during a real-time, naturalistic social interaction in males with and without autism. Translational Psychiatry, 5, e507. https://doi.org/10.1038/tp.2014.146CrossRefPubMedPubMedCentral Auyeung, B., Lombardo, M. V., Heinrichs, M., Chakrabarti, B., Sule, A., Deakin, J. B., Bethlehem, R. A. I., Dickens, L., Mooney, N., Sipple, J. A. N., Thiemann, P., & Baron-Cohen, S. (2015). Oxytocin increases eye contact during a real-time, naturalistic social interaction in males with and without autism. Translational Psychiatry, 5, e507. https://​doi.​org/​10.​1038/​tp.​2014.​146CrossRefPubMedPubMedCentral
go back to reference Baron-Cohen, S., Wheelwright, S., Hill, J., Raste, Y., & Plumb, I. (2001a). The “reading the mind in the eyes” test revised version: A study with normal adults, and adults with Asperger syndrome or high-functioning autism. Psychiatry and Allied Disciplines, 42(2), 241–251. https://doi.org/10.1017/S0021963001006643CrossRef Baron-Cohen, S., Wheelwright, S., Hill, J., Raste, Y., & Plumb, I. (2001a). The “reading the mind in the eyes” test revised version: A study with normal adults, and adults with Asperger syndrome or high-functioning autism. Psychiatry and Allied Disciplines, 42(2), 241–251. https://​doi.​org/​10.​1017/​S002196300100664​3CrossRef
go back to reference Baseler, H. A., Harris, R. J., Young, A. W., & Andrews, T. J. (2014). Neural responses to expression and gaze in the posterior superior temporal sulcus interact with facial identity. Cerebral Cortex, 24(3), 737–744.CrossRefPubMed Baseler, H. A., Harris, R. J., Young, A. W., & Andrews, T. J. (2014). Neural responses to expression and gaze in the posterior superior temporal sulcus interact with facial identity. Cerebral Cortex, 24(3), 737–744.CrossRefPubMed
go back to reference Berger, A., Fry, R., Bobak, A. K., Juliano, A., & DeGutis, J. (2022). Distinct abilities associated with matching same identity faces versus discriminating different faces: Evidence from individual differences in prosopagnosics and controls. Quarterly Journal of Experimental Psychology. https://doi.org/10.1177/17470218221076817CrossRef Berger, A., Fry, R., Bobak, A. K., Juliano, A., & DeGutis, J. (2022). Distinct abilities associated with matching same identity faces versus discriminating different faces: Evidence from individual differences in prosopagnosics and controls. Quarterly Journal of Experimental Psychology. https://​doi.​org/​10.​1177/​1747021822107681​7CrossRef
go back to reference Biotti, F., Wu, E., Yang, H., Jiahui, G., Duchaine, B., & Cook, R. (2017). Normal composite face effects in developmental prosopagnosia. Cortex, 95, 63–76.CrossRefPubMed Biotti, F., Wu, E., Yang, H., Jiahui, G., Duchaine, B., & Cook, R. (2017). Normal composite face effects in developmental prosopagnosia. Cortex, 95, 63–76.CrossRefPubMed
go back to reference Bolte, S., & Poustka, F. (2003). The recognition of facial affect in autistic and schizophrenic subjects and their first-degree relatives. Psychological Medicine, 33, 907–915.CrossRefPubMed Bolte, S., & Poustka, F. (2003). The recognition of facial affect in autistic and schizophrenic subjects and their first-degree relatives. Psychological Medicine, 33, 907–915.CrossRefPubMed
go back to reference Bowles, D. C., McKone, E., Dawel, A., Duchaine, B., Palermo, R., Schmalzl, L., Rivolta, D., Wilson, C. E., & Yovel, G. (2009). Diagnosing prosopagnosia: Effects of ageing, sex, and participant–stimulus ethnic match on the Cambridge face memory test and cambridge face perception test. Cognitive Neuropsychology, 26(5), 423–455. https://doi.org/10.1080/02643290903343149CrossRefPubMed Bowles, D. C., McKone, E., Dawel, A., Duchaine, B., Palermo, R., Schmalzl, L., Rivolta, D., Wilson, C. E., & Yovel, G. (2009). Diagnosing prosopagnosia: Effects of ageing, sex, and participant–stimulus ethnic match on the Cambridge face memory test and cambridge face perception test. Cognitive Neuropsychology, 26(5), 423–455. https://​doi.​org/​10.​1080/​0264329090334314​9CrossRefPubMed
go back to reference Cox, R. W. (1996). AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research, 29(3), 162–173.CrossRefPubMed Cox, R. W. (1996). AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research, 29(3), 162–173.CrossRefPubMed
go back to reference Davis, J. M., McKone, E., Dennett, H., O’Connor, K. B., O’Kearney, R., & Palermo, R. (2011). Individual differences in the ability to recognise facial identity are associated with social anxiety. PLoS ONE, 6(12), e28800.CrossRefPubMedPubMedCentral Davis, J. M., McKone, E., Dennett, H., O’Connor, K. B., O’Kearney, R., & Palermo, R. (2011). Individual differences in the ability to recognise facial identity are associated with social anxiety. PLoS ONE, 6(12), e28800.CrossRefPubMedPubMedCentral
go back to reference DeGutis, J., Cohan, S., Mercado, R. J., Wilmer, J., & Nakayama, K. (2012). Holistic processing of the mouth but not the eyes in developmental prosopagnosia. Cognitive Neuropsychology, 29(5–6), 419–446.CrossRefPubMed DeGutis, J., Cohan, S., Mercado, R. J., Wilmer, J., & Nakayama, K. (2012). Holistic processing of the mouth but not the eyes in developmental prosopagnosia. Cognitive Neuropsychology, 29(5–6), 419–446.CrossRefPubMed
go back to reference DeGutis, J., Wilmer, J., Mercado, R. J., & Cohan, S. (2013). Using regression to measure holistic face processing reveals a strong link with face recognition ability. Cognition, 126(1), 87–100.CrossRefPubMed DeGutis, J., Wilmer, J., Mercado, R. J., & Cohan, S. (2013). Using regression to measure holistic face processing reveals a strong link with face recognition ability. Cognition, 126(1), 87–100.CrossRefPubMed
go back to reference Furl, N., Garrido, L., Dolan, R. J., Driver, J., & Duchaine, B. (2011). Fusiform gyrus face selectivity relates to individual differences in facial recognition ability. Journal of Cognitive Neuroscience, 23(7), 1723–1740.CrossRefPubMed Furl, N., Garrido, L., Dolan, R. J., Driver, J., & Duchaine, B. (2011). Fusiform gyrus face selectivity relates to individual differences in facial recognition ability. Journal of Cognitive Neuroscience, 23(7), 1723–1740.CrossRefPubMed
go back to reference Griffiths, S., Jarrold, C., Penton-Voak, I. S., Woods, A. T., Skinner, A. L., & Munafo, M. R. (2019). Impaired recognition of basic emotions from facial expressions in young people with autism spectrum disorder: Assessing the importance of expression intensity. Journal of Autism and Developmental Disorders, 49, 2768–2778. https://doi.org/10.1007/s10803-017-3091-7CrossRefPubMed Griffiths, S., Jarrold, C., Penton-Voak, I. S., Woods, A. T., Skinner, A. L., & Munafo, M. R. (2019). Impaired recognition of basic emotions from facial expressions in young people with autism spectrum disorder: Assessing the importance of expression intensity. Journal of Autism and Developmental Disorders, 49, 2768–2778. https://​doi.​org/​10.​1007/​s10803-017-3091-7CrossRefPubMed
go back to reference Halliday, D. W. R., MacDonald, S. W. S., Sherf, S. K., & Tanaka, J. W. (2014). A reciprocal model of face recognition and autistic traits: Evidence from an individual differences perspective. PLoS ONE, 9(5), e94013.CrossRefPubMedPubMedCentral Halliday, D. W. R., MacDonald, S. W. S., Sherf, S. K., & Tanaka, J. W. (2014). A reciprocal model of face recognition and autistic traits: Evidence from an individual differences perspective. PLoS ONE, 9(5), e94013.CrossRefPubMedPubMedCentral
go back to reference Haxby, J. V., Hoffman, E. A., & Gobbini, M. I. (2002). Human neural systems for face recognition and social communication. Biological Psychiatry, 51(1), 59–67.CrossRefPubMed Haxby, J. V., Hoffman, E. A., & Gobbini, M. I. (2002). Human neural systems for face recognition and social communication. Biological Psychiatry, 51(1), 59–67.CrossRefPubMed
go back to reference Jiang, X., Bollich, A., Cox, P., Hyder, E., James, H., Gowani, S. A., Hadjikhani, N., Blanz, V., Manoach, D. S., Barton, J. J. S., Gaillard, W. D., & Riesenhuber, M. (2013). A quantitative link between face discrimination deficits and neuronal selectivity for faces in autism. NeuroImage: Clinical, 2, 320–331.CrossRefPubMed Jiang, X., Bollich, A., Cox, P., Hyder, E., James, H., Gowani, S. A., Hadjikhani, N., Blanz, V., Manoach, D. S., Barton, J. J. S., Gaillard, W. D., & Riesenhuber, M. (2013). A quantitative link between face discrimination deficits and neuronal selectivity for faces in autism. NeuroImage: Clinical, 2, 320–331.CrossRefPubMed
go back to reference Li, X., Arizpe, J., Rothlein, D., Esterman, M., & DeGutis, J. (2020). Deficient functional MRI selectivity and connectivity in developmental prosopagnosia is specific to face regions. Journal of Vision, 20(11), 827–827. Li, X., Arizpe, J., Rothlein, D., Esterman, M., & DeGutis, J. (2020). Deficient functional MRI selectivity and connectivity in developmental prosopagnosia is specific to face regions. Journal of Vision, 20(11), 827–827.
go back to reference Marriage, S., Wolverton, A., & Marriage, K. (2009). Autism Spectrum disorder grown up: A chart review of adult functioning. Journal of Canadian Academy of Child and Adolescent Psychiatry, 18(4), 322–328. Marriage, S., Wolverton, A., & Marriage, K. (2009). Autism Spectrum disorder grown up: A chart review of adult functioning. Journal of Canadian Academy of Child and Adolescent Psychiatry, 18(4), 322–328.
go back to reference Mishra, M. V., Fry, R. M., Saad, E., Arizpe, J. M., Ohashi, Y. G. B., & DeGutis, J. M. (2021). Comparing the sensitivity of face matching assessments to detect face perception impairments. Neuropsychologia, 163, 108067.CrossRefPubMedPubMedCentral Mishra, M. V., Fry, R. M., Saad, E., Arizpe, J. M., Ohashi, Y. G. B., & DeGutis, J. M. (2021). Comparing the sensitivity of face matching assessments to detect face perception impairments. Neuropsychologia, 163, 108067.CrossRefPubMedPubMedCentral
go back to reference Mishra, M. V., Likitlersuang, J., Wilmer, J. B., Cohan, S., Germine, L., & DeGutis, J. M. (2019). Gender differences in familiar face recognition and the influence of sociocultural gender inequality. Scientific Reports, 9(1), 1–12.CrossRef Mishra, M. V., Likitlersuang, J., Wilmer, J. B., Cohan, S., Germine, L., & DeGutis, J. M. (2019). Gender differences in familiar face recognition and the influence of sociocultural gender inequality. Scientific Reports, 9(1), 1–12.CrossRef
go back to reference Pierce, K., Muller, R. A., Ambrose, J., Allen, G., & Couchesne, E. (2001). Face processing occurs outside the fusiform ‘face area’ in autism: Evidence from functional MRI. Brain, 124, 2059–2073.CrossRefPubMed Pierce, K., Muller, R. A., Ambrose, J., Allen, G., & Couchesne, E. (2001). Face processing occurs outside the fusiform ‘face area’ in autism: Evidence from functional MRI. Brain, 124, 2059–2073.CrossRefPubMed
go back to reference Pitcher, D., Dilks, D. D., Saxe, R. R., Triantafyllou, C., & Kanwisher, N. (2011). Differential selectivity for dynamic versus static information in face-selective cortical regions. NeuroImage, 56(4), 2356–2363.CrossRefPubMed Pitcher, D., Dilks, D. D., Saxe, R. R., Triantafyllou, C., & Kanwisher, N. (2011). Differential selectivity for dynamic versus static information in face-selective cortical regions. NeuroImage, 56(4), 2356–2363.CrossRefPubMed
go back to reference Riggio, R. E. (1992). The Social Skills Inventory (SSI): Measuring nonverbal and social skills. In V. Manusov (Ed.), The sourcebook of nonverbal measures: Going beyond words (pp. 25–33). Routledge. Riggio, R. E. (1992). The Social Skills Inventory (SSI): Measuring nonverbal and social skills. In V. Manusov (Ed.), The sourcebook of nonverbal measures: Going beyond words (pp. 25–33). Routledge.
go back to reference Spain, D., Sin, J., Linder, K. B., McMahon, J., & Happe, F. (2018). Social anxiety in autism spectrum disorder: A systematic review. Research in Autism Spectrum Disorders, 52, 51–68.CrossRef Spain, D., Sin, J., Linder, K. B., McMahon, J., & Happe, F. (2018). Social anxiety in autism spectrum disorder: A systematic review. Research in Autism Spectrum Disorders, 52, 51–68.CrossRef
go back to reference Spreen, O., & Strauss, E. (2006). A compendium of neuropsychological tests: Administration, norms, and commentary. Oxford University Press. Spreen, O., & Strauss, E. (2006). A compendium of neuropsychological tests: Administration, norms, and commentary. Oxford University Press.
go back to reference Tanaka, J. W., & Sung, A. (2016). The “eye avoidance” hypothesis of autism face processing. Journal of Autism and Developmental Disorders, 46(5), 1538–1552.CrossRefPubMedPubMedCentral Tanaka, J. W., & Sung, A. (2016). The “eye avoidance” hypothesis of autism face processing. Journal of Autism and Developmental Disorders, 46(5), 1538–1552.CrossRefPubMedPubMedCentral
go back to reference Wechsler, D. (2001). Wechsler test of adult reading: WTAR. The Psychological Corporation. Wechsler, D. (2001). Wechsler test of adult reading: WTAR. The Psychological Corporation.
go back to reference Wechsler, D. (2008). Wechsler adult intelligence scale–Fourth Edition (WAIS–IV). San Antonio, TX: NCS Pearson, 22(498), 1. Wechsler, D. (2008). Wechsler adult intelligence scale–Fourth Edition (WAIS–IV). San Antonio, TX: NCS Pearson, 22(498), 1.
go back to reference West, R. L., Crook, T. H., & Barron, K. L. (1992). Everyday memory performance across the life span: Effects of age and noncognitive individual differences. Psychology and Aging, 7(1), 72–82.CrossRefPubMed West, R. L., Crook, T. H., & Barron, K. L. (1992). Everyday memory performance across the life span: Effects of age and noncognitive individual differences. Psychology and Aging, 7(1), 72–82.CrossRefPubMed
Metagegevens
Titel
Investigating the Influence of Autism Spectrum Traits on Face Processing Mechanisms in Developmental Prosopagnosia
Auteurs
Regan Fry
Xian Li
Travis C. Evans
Michael Esterman
James Tanaka
Joseph DeGutis
Publicatiedatum
29-09-2022
Uitgeverij
Springer US
Gepubliceerd in
Journal of Autism and Developmental Disorders / Uitgave 12/2023
Print ISSN: 0162-3257
Elektronisch ISSN: 1573-3432
DOI
https://doi.org/10.1007/s10803-022-05705-w

Andere artikelen Uitgave 12/2023

Journal of Autism and Developmental Disorders 12/2023 Naar de uitgave