Brief report: Visual processing of faces in individuals with fragile X syndrome: an eye tracking study

Faraz Farzin, Susan M Rivera, David Hessl, Faraz Farzin, Susan M Rivera, David Hessl

Abstract

Gaze avoidance is a hallmark behavioral feature of fragile X syndrome (FXS), but little is known about whether abnormalities in the visual processing of faces, including disrupted autonomic reactivity, may underlie this behavior. Eye tracking was used to record fixations and pupil diameter while adolescents and young adults with FXS and sex- and age-matched typically developing controls passively viewed photographs of faces containing either a calm, happy, or fearful expression, preceded by a scrambled face matched on luminance. Results provide quantitative evidence for significant differences in gaze patterns and increased pupillary reactivity when individuals with FXS passively view static faces. Such abnormalities have significant implications in terms of understanding causes of gaze avoidance observed in individuals with FXS.

Figures

Figure 1
Figure 1
Mean number of fixations to each AOI region by group for (a) calm, (b) happy, and (c) fearful faces. Double asterisk (**) indicates significant difference between pairwise comparisons at the p < .01 level. Error bars represent SEM.
Figure 2
Figure 2
Example fixation plots from one subject in each group (TD on left, FXS on right) for a single (a) calm, (b) happy, (c) fearful, and (d) scrambled face trial. The plot displays a static frame of fixation data for each image. Each fixation is illustrated with a blue circle where the radius represents the length of the fixation.
Figure 3
Figure 3
Mean proportion gaze duration to each AOI region by group for (a) calm, (b) happy, and (c) fearful faces. Gaze durations are reported as percentages and error bars represent SEM. Asterisk (*) and double asterisk (**) indicate significant difference between pairwise comparisons at the p < .05 and p < .01 level, respectively.
Figure 4
Figure 4
Relative change in pupil diameter (mm) between scrambled face slide to (a) calm, (b) happy, and (c) fearful faces, across 250 ms intervals, by group. Curves are time-locked to the onset of the face stimulus. Gray shaded region with asterisk (*) or double asterisk (**) indicates significant pairwise difference at the p < .05 and p < .01 level, respectively.

References

    1. Bailey DB, Roberts JE, Hooper SR, Hatton DD, Mirrett PL, Roberts JE, et al. Research on fragile X syndrome and autism: implications for the study of genes, environments, and developmental language disorders. In: Rice ML, Warren SF, editors. Developmental Language Disorders: From Phenotypes to Etiologies. Mahwah, NJ: Lawrence Erlbaum Associates; 2004. pp. 121–150.
    1. Bailey DBJ, Hatton DD, Skinner M, Mesibov GB. Autistic behavior, FMR1 protein, and developmental trajectories in young males with fragile X syndrome. Journal of Autism and Developmental Disorder. 2001;31:165–174.
    1. Belmonte MK, Bourgeron T. Fragile X syndrome and autism at the intersection of genetic and neural networks. Nature Neuroscience. 2006;9(10):121–1225.
    1. Belser RC, Sudhalter V. Arousal difficulties in males with fragile X syndrome: A preliminary report. Developmental Brain Dysfunction. 1995;8:270–279.
    1. Binstock TC. Fragile X and the amygdala: Cognitive, interpersonal, emotional and neuroendrocrine consideration. Developmental Brain Dysfunction. 1995;8:199–217.
    1. Bradley MM, Miccoli L, Escrig MA, Lang PJ. The pupil as a measure of emotional arousal and autonomic activation. Psychophysiology. 2008;45(4):602–607.
    1. Bregman JD, Leckman JF, Ort SI. Fragile X syndrome: Genetic predisposition to psychology. Journal of Autism and Developmental Disorders. 1988;18(3):343–354.
    1. Cohen D, Pichard N, Tordjman S, Baumann C, Burglen L, Excoffier E, et al. Specific genetic disorders and autism: Clinical contribution towards their identification. Journal of Autism and Developmental Disorders. 2005;35:103–116.
    1. Cohen IL, Vietze PM, Sudhalter V, Jenkins EC, Brown WT. Effects of age and communication level on eye contact in fragile X males and non-fragile X autistic males. American Journal of Medical Genetics. 1991;38(23):498–502.
    1. Crawford D, Acuna JM, Sherman SL. FMR1 and the fragile X syndrome: human genome epidemiology review. Genetics in Medicine. 2001;3(5):359–371.
    1. Dalton KM, Nacewicz BM, Alexander AL, Davidson RJ. Gaze-fixation, brain activation, and amygdala volume in unaffected siblings of individuals with autism. Biological Psychiatry. 2007;61(4):512–520.
    1. Dalton KM, Nacewicz BM, Johnstone T, Schaefer HS, Gernsbacher MA, Goldsmith HH, et al. Gaze fixation and the neural circuitry of face processing in autism. Nature Neuroscience. 2005;8:519–526.
    1. Demos KE, Kelley WM, Ryan SL, Davis FC, Whalen PJ. Human amygdala sensitivity to the pupil size of others. Cerebral Cortex. 2008:bhn034.
    1. Ekman P, Levenson RW, Friesen WV. Autonomic nervous system activity distinguishes among emotions. Science. 1983;221:1208–1210.
    1. Garrett AS, Menon V, MacKenzie K, Reiss AL. Here’s looking at you, kid: neural systems underlying face and gaze processing in fragile X syndrome. Archives of General Psychiatry. 2004;61(3):281–288.
    1. Gloor P. The Temporal Lobe and Limbic System. New York: Oxford University Press; 1997.
    1. Guastella AJ, Mitchell PB, Dadds MR. Oxytocin increases gaze to the eye region of human faces. Biological Psychiatry. 2008;63(1):3–5.
    1. Hall S, DeBernardis M, Reiss A. Social escape behaviors in children with fragile X syndrome. Journal of Autism and Developmental Disorders. 2006;36:935–947.
    1. Harris SW, Goodlin-Jones B, Nowicki ST, Hessl D, Tassone F, Barabato I, et al. Autism Profiles of Young Males with Fragile X Syndrome. American Journal of Medical Genetics Part A in press.
    1. Harrison NA, Singer T, Rotshtein P, Dolan RJ, Critchley HD. Pupillary contagion: central mechanisms engaged in sadness processing. Social Cognition and Affective Neuroscience. 2006;1:5–17.
    1. Hess EH, Polt JM. Pupil size as related to interest value of visual stimuli. Science. 1960;132:349–350.
    1. Hessl D, Glaser B, Dyer-Friedman J, Blasey C, Hastie T, Gunnar M, et al. Cortisol and behavior in fragile X syndrome. Psychoneuroendocrinology. 2002;27(7):855–872.
    1. Hessl D, Glaser B, Dyer-Friedman J, Reiss AL. Social behavior and cortisol reactivity in children with fragile X syndrome. Journal of Child Psychology and Psychiatry. 2006;47(6):602–610.
    1. Hessl D, Rivera SM, Reiss AL. The neuroanatomy and neuroendocrinology of fragile X syndrome. Mental Retardation and Developmental Disabilities Research Review. 2004;10:17–24.
    1. Kaufmann WE, Cortell R, Kau AS, Bukelis I, Tierney E, Gray RM, et al. Autism spectrum disorder in fragile X syndrome: Communication, social interaction, and specific behaviors. American Journal of Medical Genetics Part A. 2004;129A:225–234.
    1. Klin A, Jones W, Schultz R, Volkmar F, Cohen D. Visual fixation patterns during viewing of naturalistic social situations as predictors of social competence in individuals with autism. Archives of General Psychiatry. 2002;59(9):809–816.
    1. Lewis P, Abbeduto L, Murphy M, Richmond E, Giles N, Bruno L, et al. Cognitive, language, and social-cognitive skills of individuals with fragile X syndrome with and without autism. Journal of Intellectual Disability Research. 2006;50(7):532–545.
    1. Lord C, Rutter M, DiLavore PC, Risi S. Autism Diagnostic Observation Schedule- Manua. Los Angeles: Western Psychological Services; 2002.
    1. Merin N, Young GS, Ozonoff S, Rogers SJ. Visual Fixation Patterns during Reciprocal Social Interaction Distinguish a Subgroup of 6-Month-Old Infants At-Risk for Autism from Comparison Infants. Journal of Autism and Developmental Disorder. 2007;37(1):108–121.
    1. Paradee W, Melikian HE, Rasmussen DL, Kenneson A, Conn PJ, Warren ST. Fragile X mouse: strain effects of knockout phenotype and evidence suggesting deficient amygdala function. Neuroscience. 1999;94(1):185–192.
    1. Pelphrey KA, Sasson NJ, Reznick JS, Paul G, Goldman BD, Piven J. Neural basis of eye gaze processing deficits in autism. Brain. 2002;128:1038–1048.
    1. Pierce K, Haist F, Sedaghat F, Courchesne E. The brain response to personally familiar faces in autism: Findings of fusiform activity and beyond. Brain. 2004;127:2703–2716.
    1. Reddy KS. Cytogenetic abnormalities and fragile-X syndrome in Autism Spectrum Disorder. BMC Medical Genetics. 2005;6:3.
    1. Rogers SJ, Wehner EA, Hagerman RJ. The behavioral phenotype in Fragile X: Symptoms of autism in very young children with Fragile X syndrome, idiopathic autism, and other developmental disorders. Journal of Developmental and Behavioral Pediatrics. 2001;22:409–417.
    1. Rutter M, Bailey A, Lord C. Social Communication Questionnaire (SCQ) Los Angeles: Western Psychological Services; 2003.
    1. Saluto A, Brussino A, Tassone F, Arduino C, Cagnoli C, Pappi P, et al. An enhanced polymerase chain reaction assay to detect pre- and full mutation alleles of the fragile X mental retardation 1 gene. Journal of Molecular Diagnostics. 2005;7(5):605–612.
    1. Schultz RT, Gauthier I, Klin A, Fulbright RK, Anderson AW, Volkmar F, et al. Abnormal ventral temporal cortical activity during face discrimination among individuals with autism and Asperger syndrome. Archives of General Psychiatry. 2000;57:331–340.
    1. Speer LL, Cook AE, McMahon WM, Clark E. Face processing in children with autism:effects of stimulus contents and type. Autism. 2007;11(3):265–277.
    1. Spezio ML, Adolphs R, Hurley RS, Piven J. Abnormal use of facial information in high-functioning autism. Journal of Autism and Developmental Disorder. 2007;37(5):929–939.
    1. Steinhauer SR, Siegle GJ, Condray R, Pless M. Sympathetic and parasympathetic innervation of pupillary dilation during sustained processing. International Journal of Psychophysiology. 2004;52:77–86.
    1. Tassone F, Hagerman RJ, Garcia AD, Khandijian EW, Greco CM, Hagerman PJ. Intranuclear inclusions in neural cells with premutation alleles in fragile X associated tremor/ataxia syndrome. Journal of Medical Genetics. 2004;41:1–3.
    1. Tottenham N. MacArthur Foundation Research Network 2002
    1. van Kooten IAJ, Palmen SJMC, von Cappeln P, Steinbusch HWM, Korr H, Heinsen H, et al. Neurons in the fusiform gyrus are fewer and smaller in autism. Brain. 2008;131:987–999.
    1. Wassink TH, Piven J, Patil SR. Chromosomal abnormalities in a clinic sample of individuals with autistic disorder. Psychiatric Genetics. 2001;11:57–63.
    1. Wechsler D. Wechsler Intelligence Scale for Children. Fourth Edition. San Antonio: Harcourt Assessment, Inc.; 2003.
    1. Wisbeck JM, Huffman LC, Freund L, Gunnar MR, Davis EP, Reiss AL. Cortisol and social stressors in children with fragile X: A pilot study. Journal of Developmental and Behavioral Pediatrics. 2000;21:278–282.

Source: PubMed

Спонсоры и соавторы

Заболевания

Медикаментозные вмешательства

Подписаться