Preferencje help
Widoczny [Schowaj] Abstrakt
Liczba wyników
2018 | 78 | 2 |
Tytuł artykułu

Face processing in a case of high functioning autism with developmental prosopagnosia

Warianty tytułu
Języki publikacji
The ability to “read” the information about facial identity, expressed emotions, and intentions is crucial for non-verbal social interaction. Neuroimaging and clinical studies consequently link face perception with fusiform gyrus (FG) and occipital face area (OFA) activity. Here we investigated face processing in an adult, patient PK, diagnosed with both high functioning autism spectrum disorder (ASD) and developmental prosopagnosia (DP). Both disorders have a significant impact on face perception and recognition, thus creating a unique neurodevelopmental condition. We used eye-tracking and functional magnetic resonance imaging (fMRI) method. Eye-tracking and fMRI results of PK were compared to results of control subjects. Patient PK showed atypical gaze-fixation strategy during face perception and typical patterns of brain activations in the FG and OFA. However, a significant difference between PK and control subjects was found in the left anterior superior temporal sulcus/middle temporal gyrus (aSTS/MTG). In PK the left aSTS/MTG was hypo-activated in comparison to the control subjects. Additionally, functional connectivity analysis revealed decreased inter-hemispheric connectivity between right and left aSTS/MTG in ‘ASD and DP’ patient during face recognition performance as compared to the control subjects. The lack of activity in the left aSTS/MTG observed in the case of the clinical subject, combined with the behavioral, eye-tracking, and neuropsychological results, suggests that impairment of the cognitive mechanism of face recognition involves higher level of processing. It seems to be related to insufficient access to semantic knowledge about the person when prompted by face stimuli.
Słowa kluczowe
Opis fizyczny
  • Laboratory of Social Psychology, Department of Ergonomics, Central Institute for Labour Protection, National Research Institute, Warsaw, Poland
  • Laboratory of Psychophysiology, Department of Neurophysiology, Nencki Institute of Experimental Biology, Polish Academy of Science, Warsaw, Poland
  • Faculty of Psychology, University of Warsaw, Warsaw, Poland
  • Laboratory of Psychophysiology, Department of Neurophysiology, Nencki Institute of Experimental Biology, Polish Academy of Science, Warsaw, Poland
  • Laboratory of Brain Imaging, Neurobiology Center, Nencki Institute of Experimental Biology, Polish Academy of Science, Warsaw, Poland
  • Laboratory of Brain Imaging, Neurobiology Center, Nencki Institute of Experimental Biology, Polish Academy of Science, Warsaw, Poland
  • Laboratory of Psychophysiology, Department of Neurophysiology, Nencki Institute of Experimental Biology, Polish Academy of Science, Warsaw, Poland
  • Ashburner J (2007) A fast diffeomorphic image registration algorithm. Neuroimage 38: 95–113.
  • Avidan G, Hasson U, Malach R, Behrmann M (2005) Detailed exploration of face-related processing in congenital prosopagnosia: 2. Functional neuroimaging findings. J Cogn Neurosci 17: 1150–1167.
  • Avidan G, Behrmann M (2008) Implicit familiarity processing in congenital prosopagnosia. J Neuropsychol 2: 141–164.
  • Avidan G, Tanzer M, Behrmann M (2011) Impaired holistic processing in congenital prosopagnosia. Neuropsychologia 49: 2541–2552.
  • Avidan G, Tanzer M, Hadj-Bouziane F, Liu N, Ungerleider LG, Behrmann M (2013) Selective dissociation between core and extended regions of the face processing network in congenital prosopagnosia. Cereb Cortex 24: 1565–1578.
  • Baron-Cohen S, Wheelwright S, Skinner R, Martin J, Clubley E (2001) The autism-spectrum quotient (AQ): evidence from Asperger syndrome/high-functioning autism, males and females, scientists and mathematicians. J Autism Dev Disord 31: 5–17.
  • Barton JJS, Cherkasova M, O’Connor M (2001) Covert recognition in acquired and developmental prosopagnosia. Neurology 57: 1161–1168.
  • Barton JJS, Cherkasova M, Press D, Intriligato J, O’Connor M (2003) Developmental prosopagnosia: a study of three patients. Brain Cogn 51: 12–30.
  • Barton JJS, Cherkasova M, Hefter R, Cox TA, O’Connor M, Manoach DS (2004) Are patients with social developmental disorders prosopagnosic? Perceptual heterogeneity in the Asperger and socio-emotional processing disorders. Brain 127: 1706–1716.
  • Bate S, Haslam C, Tree JJ, Hodgson TL (2008) Evidence of an eye movement-based memory effect in congenital prosopagnosia. Cortex 44: 806–819.
  • Bentin S, DeGutis JM, D’Esposito M, Robertson LC (2007) Too many trees to see the forest: Performance, event-related potential, functional magnetic resonance imaging manifestations of integrative congenital prosopagnosia. J Cogn Neurosci 19: 132–146.
  • Brambati SM, Benoit S, Monetta L, Belleville S, Joubert S (2010) The role of the left anterior temporal lobe in the semantic processing of famous faces. Neuroimage 53: 674–681.
  • Brzeziński J, Gaul M, Hornowska E, Jaworowska A, Machowski A, Zakrzewska M (2004) WAIS-R(PL). Wechsler Adult Intelligence Scale – Revised. Pracownia Testów Psychologicznych Polskiego Towarzystwa Psychologicznego, Warsaw, Poland.
  • Chatterjee G, Nakayama K (2012) Normal facial age and gender perception in developmental prosopagnosia. Cogn Neuropsychol 29: 482–502.
  • Ciechanowicz A, Jaworowska A, Matczak A (2000) INTE – Kwestionariusz Inteligencji Emocjonalnej. Pracownia Testów Psychologicznych Polskiego Towarzystwa Psychologicznego, Warsaw, Poland.
  • Cook R, Shah P, Gaule A, Brewer R, Bird G (2015) Autism and Developmental Prosopagnosia: A Cross-Disorder Study. J Vis 15: 1211.
  • Corbett BA, Carmean V, Ravizza S, Wendelken C, Henry ML, Carter C, Rivera SM (2009) A functional and structural study of emotion and face processing in children with autism. Psychiatry Res 173: 196–205.
  • Critchley HC, Daly EM, Bullmore ET, Steven CR, Williams SCR, Van Amelsvoort T, Robertson DM, Rowe A, Phillips M, McAlonan G, Howlin P, Murphy DG (2000) The functional neuroanatomy of social behavior. Changes in cerebral blood flow when people with autistic disorder process facial expressions. Brain 123: 2203–2212.
  • Dalton KM, Nacewicz BM, Johnstone T, Schaefer HS, Gernsbacher MA, Goldsmith HH, Alexander AL, Davidson RJ (2005) Gaze fixation and the neural circuitry of face processing in autism. Nat Neurosci 8: 519–526.
  • Dawson G, Webb SJ, McPartland J (2005) Understanding the nature of face processing impairment in autism: insights from behavioral and electrophysiological studies. Dev Neuropsychol 27: 403–424.
  • DeGutis J, Bentin S, Roberton LC, D’Esposito M (2007) Functional plasticity in ventral temporal cortex following cognitive rehabilitation of a congenital prosopagnosic. J Cogn Neurosci 19: 1790–1802.
  • De Haan EHF, Bauer RM, Greve KW (1992) Behavioural and physiological evidence for covert face recognition in a prosopagnosic patient. Cortex 28: 77–95.
  • Duchaine BC, Parker H, Nakayama K (2003) Normal recognition of emotion in a prosopagnosic. Perception 32: 827–838.
  • Ellis HD, Leafhead KM (1996) Raymond: A study of an adult with Asperger syndrome. In: Methods in madness: Case studies in cognitive neuropsychiatry (Halligan PW and Marshall JC, Eds.), Psychology Press, Oxford, p. 79–92.
  • Farah MJ, Wilson KD, Drain HM, Tanaka JR (1995) The inverted face inversion effect in prosopagnosia: Evidence for mandatory, face-specific perceptual mechanisms. Vision Res 35: 2089–2093.
  • Furl N, Garrido L, Dolan RJ, Driver J, Duchaine B (2011) Fusiform gyrus face selectivity relates to individual differences in facial recognition ability. J Cogn Neurosci 23: 1723–1740.
  • Fusar-Poli P, Placentino A, Carlett F, Landi P, Allen P, Surguladze S, Benedetti F, Abbamonte M, Gasparotti R, Barale F, Perez J, McGuire P, Politi P (2009) Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. J Psychiatry Neurosci 34: 418–432.
  • Garrido L, Furl N, Draganski B, Weiskopf N, Stevens J, Tan GC, Driver J, Dolan RJ, Duchaine B (2009) Voxel-based morphometry reveals reduced grey matter volume in the temporal cortex of developmental prosopagnosics. Brain 132: 3443–3455.
  • Gobbini MI, Haxby JV (2007) Neural systems for recognition of familiar faces. Neuropsychologia 45: 32–41.
  • Gorno-Tempini ML, Price CJ, Josephs O, Vandenberghe R, Cappa SF,Kapur N, Frackowiak RSJ (1998) The neural systems sustaining face and proper-name processing. Brain 121: 2103–2118.
  • Gorno-Tempini ML, Price CJ (2001) Identification of famous faces and buildings. A functional neuroimaging study of semantically unique items. Brain 124: 2087–2097.
  • Grelotti DJ, Klin AJ, Gauthier I, Skudlarski P, Cohen DJ, Gore JC, Volkmar FR, Schultz RT (2005) fMRI activation of the fusiform gyrus and amygdala to cartoon characters but not to faces in a boy with autism. Neuropsychologia 43: 373–385.
  • Hadjikhani N, de Gelder B (2002) Neural basis of prosopagnosia: an fMRI study. Hum Brain Mapp 16: 176–182.
  • Hadjikhani N, Joseph RM, Snyder J, Chabris CF, Clark J, Steele S, McGrath L, Vangel M, Aharon I, Feczko E, Harris GJ, Tager-Flusberg H (2004) Activation of the fusiform gyrus when individuals with autism spectrum disorder view faces. Neuroimage 22: 1141–1150.
  • Hadjikhani N, Joseph RM, Snyder J, Tager-Flusberg H (2007) Abnormal activation of the social brain during face perception in autism. Hum Brain Mapp 28: 441–449.
  • Haist F, Adamo M, Han Wazny J, Lee K, Stiles J (2013) The functional architecture for face-processing expertise: fMRI evidence of the developmental trajectory of the core and the extended face systems. Neuropsychologia 51: 2893–2908.
  • Hasson U, Avidan G, Deouell LY, Bentin S, Malach R (2003) Face-selective activation in a congenital prosopagnosic subject. J Cogn Neurosci 15: 419–431.
  • Haxby JV, Hoffman EA, Gobbini MI (2002) Human neural systems for face recognition and social communication. Biol Psychiatry 51: 59–67.
  • Hernandez N, Metzger A, Magné R, Bonnet-Brilhault F, Roux S, Barthelemy C, Martineau J (2009) Exploration of core features of a human face by healthy and autistic adults analyzed by visual scanning. Neuropsychologia 47: 1004–1012.
  • Huis in ’t Veld E, Van den Stock J, de Gelder B (2012) Configuration perception and face memory, face context effects in developmental prosopagnosia. Cogn Neuropsychol 29: 464–481.
  • Humphreys K, Hasson U, Avidan G, Minshew N, Behrmann M (2008) Cortical patterns of category-selective activation for faces, places and objects in adults with autism. Autism Res 1: 52–63.
  • Iidaka T (2014) Role of the fusiform gyrus and superior temporal sulcus in face perception and recognition: An empirical review. Jpn Psychol Res 56: 33–45.
  • Jaworowska A, Szustrowa T (1991) TMZ – Test Matryc Ravena w wersji dla Zaawansowanych. Pracownia Testów Psychologicznych Polskiego Towarzystwa Psychologicznego, Warsaw, Poland.
  • Jaworowska A, Matczak A, Rotter JB (2003) Test Niedokończonych Zdań Rottera RISB: podręcznik. Pracownia Testów Psychologicznych Polskiego Towarzystwa Psychologicznego, Warsaw, Poland.Jaworowska A (2017) BENTON – Test Pamięci Wzrokowej Bentona. Pracownia Testów Psychologicznych Polskiego Towarzystwa Psychologicznego, Warsaw, Poland.
  • Kanwisher N, Yovel G (2006) The fusiform face area: A cortical region specialized for the perception of faces. Philos Trans R Soc Lond B Biol Sci 361: 2109–2128.
  • Kennerknecht I, Grueter T, Welling B, Wentzek S, Horst J, Edwards S, Grueter M (2006) First report on the prevalence of non-syndromic hereditary prosopagnosia (HPA) Am J Med Genet A 140: 1617–1622.
  • Kleinhans NM, Johnson LC, Richards T, Mahurin R, Greenson J, Dawson G, Aylward E (2009) Reduced neural habituation in the amygdala and social impairments in autism spectrum disorders. Am J Psychiatry 166: 467–475.
  • Klin A, Jones W, Schultz R, Volkmar F, Cohen D (2002a) Defining and quantifying the social phenotype in autism. Am J Psychiatry 159: 895–908.
  • Klin A, Jones W, Schultz R, Volkmar F, Cohen D (2002b) Visual fixation patterns during viewing of naturalistic social situations as predictors of social competence in individuals with autism. Arch Gen Psychiatry 59: 809–816.
  • Klin A, Jones W (2008) Altered face scanning and impaired recognition of biological motion in a 15-month-old infant with autism. Dev Sci 11: 40–46.
  • Kracke I (1994) Developmental prosopagnosia in Asperger syndrome: presentation and discussion of an individual case. Dev Med Child Neurol 36: 873–886.
  • Lancaster JL, Woldorff MG, Parsons LM, Liotti M, Freitas CS, Rainey L, Kochunov PV, Nickerson D, Mikiten SA, Fox PT (2000) Automated Talairach Atlas labels for functional brain mapping. Hum Brain Mapp 10: 120–131.
  • Lê S, Raufaste E, Démonet JF (2003) Processing of normal, inverted, scrambled faces in a patient with prosopagnosia: behavioural and eye tracking data. Brain Res Cogn Brain Res 17: 26–35.
  • Le Grand R, Cooper PA, Mondloch CJ, Lewis TL, Sagiv N, de Gelder B, Maurer D (2006) What aspects of face processing are impaired in developmental prosopagnosia? Brain Cogn 61: 139–158.
  • Leveroni CL, Seidenberg M, Mayer AR, Mead LA, Binder JR, Rao SM (2000) Neural systems underlying the recognition of familiar and newly learned faces. J Neurosci 20: 878–886.
  • Levine DN, Calvanio R (1989) Prosopagnosia: a defect in visual configural processing. Brain Cogn 10: 149–170.
  • Lord C, Risi S, Lambrecht L, Cook EH, Leventhal BL, DiLavore PC, Pickles A, Rutter M (2000) The autism diagnostic observation schedule-generic: A standard measure of social and communication deficits associated with the spectrum of autism. J Autism Dev Disord 30: 205–223.
  • Łojek E (2007) RHLB-PL – Bateria Testów do Badania Funkcji Językowych i Komunikacyjnych Prawej Półkuli Mózgu. Pracownia Testów Psychologicznych Polskiego Towarzystwa Psychologicznego, Warsaw, Poland.
  • Matczak A, Piekarska J, Studniarek E (2005) Skala Inteligencji Emocjonalnej. Pracownia Testów Psychologicznych Polskiego Towarzystwa Psychologicznego, Warsaw, Poland.
  • McConachie H (1976) Developmental prosopagnosia. A single case report. Cortex 12: 76–82.
  • Monzalvo K, Fluss J, Billard C, Dehaene S, Dehaene-Lambertz G (2012) Cortical networks for vision and language in dyslexic and normal children of variable socio-economic status. Neuroimage 61: 258–274.
  • Myles BS, Bock SJ, Simpson RL (2001) Asperger Syndrome Diagnostic Scale. Western Psychological Services, Los Angeles, California, USA.
  • Nakahachi T, Yamashita K, Iwase M, Ishigami W, Tanaka C, Toyonaga K, Maeda S, Hirotsune H, Tei Y, Yokoi K, Okajima S, Shimizu A, Takeda M (2008) Disturbed holistic processing in autism spectrum disorders verified by two cognitive tasks requiring perception of complex visual stimuli. Psychiatry Res 159: 330–338.
  • Nasr S, Tootell RB (2012) Role of fusiform and anterior temporal cortical areas in facial recognition. Neuroimage 63: 1743–1753.
  • Natu V, O’Toole AJ (2011) The neural processing of familiar and unfamiliar faces: A review and synopsis. Br J Psychol 102: 726–747.
  • Njiokiktjien C, Verschoor A, de Sonneville L, Huyser C, Op het Veld V, Toorenaar N (2001) Disordered recognition of facial identity and emotions in three Asperger type autists. Eur Child Adolesc Psychiatry 10: 79–90.
  • Nomi JS, Uddin LQ (2015) Face processing in autism spectrum disorders: From brain regions to brain networks. Neuropsychologia 71: 201–216.
  • Oldfield RC (1971) The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia 9: 97–113.
  • Pelphrey KA, Sasson NJ, Reznick JS, Paul G, Goldman BD, Piven J (2002) Visual scanning of faces in autism. J Autism Dev Disord 32: 249–261.
  • Pelphrey KA, Morris JP, McCarthy G, LaBar KS (2007) Perception of dynamic changes in facial affect and identity in autism. Soc Cogn Affect Neurosci 2: 140–149.
  • Philip RC, Dauvermann MR, Whalley HC, Baynham K, Lawrie SM, Stanfield AC (2012) A systematic review and meta-analysis of the fMRI investigation of autism spectrum disorders. Neurosci Biobehav Rev 36: 901–942.
  • Pierce K, Haist F, Sedaghat F, Courchesne E (2004) The brain response to personally familiar faces in autism: findings of fusiform activity and beyond. Brain 127: 2703–2716.
  • Pierce K, Müller RA, Ambrose J, Allen G, Courchesne E (2001) Face processing occurs outside the fusiform ‘face area’ in autism: evidence from functional MRI. Brain 124: 2059–2073.
  • Pietz J, Ebinge F, Rating D (2003) Prosopagnosia in a preschool child with Asperger syndrome. Dev Med Child Neurol 45: 55–57.
  • Redcay E (2008) The superior temporal sulcus performs a common function for social and speech perception: Implications for the emergence of autism. Neurosci Biobehav Rev 32: 123–142.
  • Rivolta D, Schmalz L, Coltheart M, Palermo R (2010) Semantic information can facilitate covert face recognition in congenital prosopagnosia. J Clin Exp Neuropsychol 32: 1002–1016.
  • Saitovitch A, Bargiacchi A, Chabane N, Brunelle F, Samson Y, Boddaert N, Zilbovicius M (2012) Social cognition and the superior temporal sulcus: Implications in autism. Rev Neurol 168: 762–770.
  • Schultz RT, Gauthier I, Klin A, Fulbright RK, Anderson AW, Volkmar F, Skudlarski P, Lacadie C, Cohen DJ, Gore JC (2000) Abnormal ventral temporal cortical activity during face discrimination among individuals with autism and Asperger syndrome. Arch Gen Psychiatry 57: 331–340.
  • Schutte NS, Malouff JM, Hall LE, Haggerty DJ, Cooper JT, Golden CJ, Dornheim L (1998) Development and validation of a measure of emotional intelligence. Pers Individ Dif 25: 167–177.
  • Sergent J, Ohta S, MacDonald B (1992) Functional neuroanatomy of face and object processing. A positron emission tomography study. Brain 115: 15–36.
  • Schweinberger SR, Burton AM (2003) Covert recognition and the neural system for face processing. Cortex 39: 9–30.
  • Soulières I, Zeffiro TA, Girard ML, Mottron L (2011) Enhanced mental image mapping in autism. Neuropsychologia 49: 848–857.
  • Susilo T, Duchaine B (2013) Advances in developmental prosopagnosia research. Curr Opin Neurobiol 23: 423–429.
  • Swettenham J, Baron-Cohen S, Charman T, Cox A, Baird G, Drew A, Rees L, Wheelwright S (1998) The frequency and distribution of spontaneous attention shifts between social and nonsocial stimuli in autistic, typically developing, nonautistic developmentally delayed infants. J Child Psychol Psychiatry 39: 747–753.
  • Tranel D, Damasio AR (1985) Knowledge without awareness: an autonomic index of facial recognition by prosopagnosics. Science 228: 1453–1454.
  • Wagner J, Hirsch S, Vogel-Farley V, Redcay E, Nelson C (2013) Eye-tracking, autonomic, electrophysiological correlates of emotional face processing in adolescents with Autism Spectrum Disorder. J Autism Dev Disord 43: 188–199.
  • Wechsler D (1997) Wechsler Memory Scale – Third Edition manual. The Psychological Corporation, San Antonio, TX., USA.
  • Weigelt S, Koldewyn K, Kanwisher N (2013) Face recognition deficits in Autism Spectrum Disorders are both domain specific and process specific. PLoS One 8: e74541.
  • Weisberg J, Milleville SC, Kenworthy L, Wallace GL, Gotts SJ, Beauchamp MS, Martin A (2014) Social perception in autism spectrum disorders: impaired category selectivity for dynamic but not static images in ventral temporal cortex. Cereb Cortex 24: 37–48.
  • Whitfield-Gabrieli S, Nieto-Castanon A (2012) Conn: a functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connect 2: 125–141.
  • Wicker B, Fonlupt P, Hubert B, Tardif C, Gepner B, Deruelle C (2008) Abnormal cerebral effective connectivity during explicit emotional processing in adults with autism spectrum disorder. Soc Cogn Affect Neurosci 3: 135–143.
  • Yovel G, Kanwisher N (2005) The neural basis of the behavioral face-inversion effect. Curr Biol 15: 2256–2262.
  • Zilbovicius M, Saitovitch A, Popa T, Rechtman E, Diamandis L, Chabane N, Brunelle F, Samson Y, Boddaert N (2013) Autism, social cognition and superior temporal sulcus. Open J Psychiatr 3: 46–55.
Typ dokumentu
Identyfikator YADDA
JavaScript jest wyłączony w Twojej przeglądarce internetowej. Włącz go, a następnie odśwież stronę, aby móc w pełni z niej korzystać.