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Journal of Neurodevelopmental Disorders

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Open Access 01-12-2015 | Research

Face scanning and spontaneous emotion preference in Cornelia de Lange syndrome and Rubinstein-Taybi syndrome

Authors: Hayley Crawford, Joanna Moss, Joseph P. McCleery, Giles M. Anderson, Chris Oliver

Published in: Journal of Neurodevelopmental Disorders | Issue 1/2015

Abstract

Background

Existing literature suggests differences in face scanning in individuals with different socio-behavioural characteristics. Cornelia de Lange syndrome (CdLS) and Rubinstein-Taybi syndrome (RTS) are two genetically defined neurodevelopmental disorders with unique profiles of social behaviour.

Methods

Here, we examine eye gaze to the eye and mouth regions of neutrally expressive faces, as well as the spontaneous visual preference for happy and disgusted facial expressions compared to neutral faces, in individuals with CdLS versus RTS.

Results

Results indicate that the amount of time spent looking at the eye and mouth regions of faces was similar in 15 individuals with CdLS and 17 individuals with RTS. Both participant groups also showed a similar pattern of spontaneous visual preference for emotions.

Conclusions

These results provide insight into two rare, genetically defined neurodevelopmental disorders that have been reported to exhibit contrasting socio-behavioural characteristics and suggest that differences in social behaviour may not be sufficient to predict attention to the eye region of faces. These results also suggest that differences in the social behaviours of these two groups may be cognitively mediated rather than subcortically mediated.

The methods used here are identical to those used and described in a previous study conducted by the authors to investigate face processing in Fragile X Syndrome and Autism Spectrum Disorder [41].

Development of the MacBrain Face Stimulus Set was overseen by Nim Tottenham and supported by the John D. and Catherine T. MacArthur Foundation Research Network on Early Experience and Brain Development. Please contact Nim Tottenham at tott0006@tc.umn.edu for more information concerning the stimulus set.

Where results from non-parametric tests, used when data were not normally distributed, did not differ from results from the equivalent parametric tests, the results from the parametric tests are reported.

Baron-Cohen S, Joliffe T, Mortimore C, Robertson M. Another advanced test of theory of mind: evidence from very high functioning adults with autism or asperger syndrome. J Child Psychol Psychiatry. 1997;38:813–22.PubMedCrossRef

Baron-Cohen S, Wheelwright S, Hill J, Raste Y, Plumb I. The “reading the mind in the eyes” test revised version: a study with normal adults, and adults with asperger syndrome or high-functioning autism. J Child Psychol Psychiatry. 2001;42:241–51.PubMedCrossRef

Riby DM, Hancock PJB. Viewing it differently: social scene perception in Williams syndrome and autism. Neuropsychologia. 2008;46:2855–60.PubMedCrossRef

Riby DM, Doherty-Sneddon G, Bruce V. Exploring face perception in disorders of development: evidence from Williams syndrome and autism. J Neuropsychol. 2008;2:47–64.PubMedCrossRef

Riby DM, Hancock PJB. Do faces capture the attention of individuals with Williams syndrome or autism? evidence from tracking eye movements. J Autism Dev Disord. 2009;39:421–31.PubMedCrossRef

Kennedy DP, Adolphs R. Impaired fixation to eyes following amygdala damage arises from abnormal bottom-up attention. Neuropsychologia. 2010;48:3392–8.PubMedCentralPubMedCrossRef

Spezio ML, Huang PY, Castelli F, Adolphs R. Amygdala damage impairs eye contact during conversations with real people. J Neurosci. 2007;27:3994–7.PubMedCrossRef

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. Nat Neurosci. 2005;8:519–26.PubMedCentralPubMed

Sweeten TL, Posey DJ, Shekhar A, McDougle CJ. The amygdala and related structures in the pathophysiology of autism. Pharmacol Biochem Behav. 2002;71:449–55.PubMedCrossRef

10.

Cody Hazlett H, Pelphrey KA, Piven J. Structural and functional magnetic resonance imaging of autism. Int J Dev Neurosci. 2002;20:421–38.CrossRef

11.

Kirchner JC, Hatri A, Heekeren HR, Dziobeck I. Autistic symptomatology, face processing abilities, and eye fixation patterns. J Autism Dev Disord. 2011;41:158–67.PubMedCrossRef

12.

Speer LL, Cook AE, McMahon WM, Clark E. Face processing in children with autism effects of stimulus contents and type. Autism. 2007;11:265–77.PubMedCrossRef

13.

Guillon Q, Hadjikhani N, Badual S, Rogé B. Visual social attention in autism spectrum disorder: insights from eye-tracking studies. Neurosci Biobehav Rev. 2014;42:279–97.PubMedCrossRef

14.

Kliemann D, Dziobeck I, Hatri A, Steimke R, Heekeren HR. Atypical reflexive gaze patterns on emotional faces in autism spectrum disorders. J Neurosci. 2010;30:12281–7.PubMedCrossRef

15.

Bal E, Harden E, Lamb D, Van Hecke AV, Denver JW, Porges SW. Emotion recognition in children with autism spectrum disorders: relations to eye gaze and autonomic state. J Autism Dev Disord. 2010;40:358–70.PubMedCrossRef

16.

Adolphs R, Tranel D, Damasio H, Damasio A. Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature. 1994;372:669–72.PubMedCrossRef

17.

Izard C, Fine S, Schultz D, Mostow A, Ackerman B, Youngstrom E. Emotion knowledge as a predictor of social behaviour and academic competence in children at risk. Psychol Sci. 2001;12:18–23.PubMedCrossRef

18.

Sawyer AA, Williamson P, Young RL. Can gaze avoidance explain why individuals with Asperger’s syndrome can’t recognise emotions from facial expressions? J Autism Dev Disord. 2012;42:606–18.PubMedCrossRef

19.

Harms MB, Martin A, Wallace GL. Facial emotion recognition in autism spectrum disorders: a review of behavioral and neuroimaging studies. Neuropsychol Rev. 2010;20:290–322.PubMedCrossRef

20.

Tager-Flusberg H, Skwerer DP, Joseph RM. Model syndromes for investigating social cognitive and affective neuroscience: a comparison of autism and Williams syndrome. Soc Cogn Affect Neurosci. 2006;1:175–82.PubMedCentralPubMedCrossRef

21.

Beck B. Epidemiology of Cornelia de Lange’s syndrome. Acta Paediatr. 1976;65:631–8.CrossRef

22.

Berney TP, Ireland M, Burn J. Behavioural phenotype of Cornelia de Lange syndrome. Arch Dis Child. 1999;81:333–6.PubMedCentralPubMedCrossRef

23.

Moss J, Oliver C, Berg K, Kaur G, Jephcott L, Cornish K. Prevalence of autism spectrum phenomenology in Cornelia de Lange and Cri du Chat syndromes. Am J Ment Retard. 2008;113:278–91.PubMedCrossRef

24.

Moss J, Howlin P, Magiati I, Oliver C. Characteristics of autism spectrum disorder in Cornelia de Lange syndrome. J Child Psychol Psychiatry. 2012;53:883–91.PubMedCrossRef

25.

Gillis LA, McCallum J, Kaur M, DeScipio C, Yaeger D, Mariani A, et al. NIPBL mutational analysis in 120 individuals with Cornelia de Lange syndrome and evaluation of genotype-phenotype correlations. Am J Hum Genet. 2004;75:610–23.PubMedCentralPubMedCrossRef

26.

Krantz ID, McCallum J, DeScipio C, Kaur M, Gillis LA, Yaeger D, et al. Cornelia de Lange syndrome is caused by mutations in NIPBL, the human homolog of Drosophila melanogaster Nipped-B. Nat Gen. 2004;36:631–5.CrossRef

27.

Miyake N, Visser R, Kinoshita A, Yoshiura K-I, Niikawa N, Kondoh T, et al. Four novel NIPBL mutations in Japanese patients with Cornelia de Lange syndrome. Am J Med Genet A. 2005;135:103–5.PubMedCrossRef

28.

Deardorff MA, Kaur M, Yaeger D, Rampuria A, Korolev S, Pie J, et al. Mutations in cohesin complex members SMC3 and SMC1A cause a mild variant of Cornelia de Lange syndrome with predominant mental retardation. Am J Hum Genet. 2007;80:485–94.PubMedCentralPubMedCrossRef

29.

Musio A, Selicorni A, Focarelli ML, Gervasini C, Milani D, Russo S, et al. X-linked Cornelia de Lange syndrome owing to SMC1L1 mutations. Nat Gen. 2006;38:528–30.CrossRef

30.

Deardorff MA, Bando M, Nakato R, Watrin E, Itoh T, Minamino M, et al. HDAC8 mutations in Cornelia de Lange syndrome affect the cohesin acetylation cycle. Nature. 2012;489:313–7.PubMedCentralPubMedCrossRef

31.

Minor A, Shinawi M, Hogue JS, Vineyard M, Hamlin DR, Tan C, et al. Two novel RAD21 mutations in patients with mild Cornelia de Lange syndrome-like presentation and report of the first familial case. Genet Med. 2014;537:279–84.

32.

Richards C, Moss J, O’Farrell L, Kaur G, Oliver C. Social anxiety in Cornelia de Lange syndrome. J Autism Dev Disord. 2009;39:1155–62.PubMedCrossRef

33.

Wieser M, Pauli P, Alpers GW, Muhlberger A. Is eye to eye contact really threatening and avoided in social anxiety? An eye-tracking and psychophysiology study. J Anxiety Disord. 2009;23.

34.

Evans KC, Wright CI, Wedig MM, Gold AL, Pollack MH, Rauch SL. A functional MRI study of amygdala response to angry schematic faces in social anxiety disorder. Depress Anxiety. 2008;25:495–505.CrossRef

35.

Amarel DG. The primate amygdala and the neurobiology of social behaviour: implications for understanding social anxiety. Biol Psychiatry. 2002;51:11–7.CrossRef

36.

Cornish K, Turk J, Levitas A. Fragile X syndrome and autism: common developmental pathways? Curr Pediatr Rev. 2007;3:61–8.CrossRef

37.

Dalton KM, Holsen L, Abbeduto L, Davidson RJ. Brain function and gaze fixation during facial-emotion processing in fragile X and autism. Autism Res. 2008;1:231–9.PubMedCentralPubMedCrossRef

38.

Holsen LM, Dalton KM, Johnstone T, Davidson RJ. Prefrontal social cognition network dysfunction underlying face encoding and social anxiety in fragile X syndrome. Neuroimage. 2008;43:592–604.PubMedCentralPubMedCrossRef

39.

Farzin F, Rivera SM, Hessl D. Brief report: visual processing of faces in individuals with fragile X syndrome: an eye tracking study. J Autism Dev Disord. 2009;39:946–52.PubMedCentralPubMedCrossRef

40.

Farzin F, Scaggs F, Hervey C, Berry-Kravis E, Hessl D. Reliability of eye tracking and pupillometry measures in individuals with fragile X syndrome. J Autism Dev Disord. 2011;41:1515–22.PubMedCentralPubMedCrossRef

41.

Crawford H, Moss J, Anderson GM, Oliver C, McCleery JP. Implicit discrimination of basic facial expressions of positive/negative emotion in fragile X syndrome and autism spectrum disorder, American journal on intellectual and developmental disabilities. 2015.

42.

Hessl D, Rivera S, Koldewyn K, Cordeiro L, Adamns J, Tassone F, et al. Amygdala dysfunction in men with the fragile x premutation. Brain. 2007;130:404–16.PubMedCrossRef

43.

Hennekam RC, Van Den Boogaard M-J, Sibbles BJ, Van Spijker HG. Rubinstein-taybi syndrome in the Netherlands. Am J Med Genet. 1990;37:17–29.CrossRef

44.

Petrif F, Giles RH, Dauwerse HG, Saris JJ, Hennekam RC, Masuno M, et al. Rubinstein-Taybi syndrome caused by mutations in the transcriptional co-activator CBP. Nature. 1995;376:348–51.CrossRef

45.

Coupry I, Roudaut C, Stef M, Delrue MA, Marche M, Burgelin I, et al. Molecular analysis of the CBP gene in 60 patients with Rubinstein-Taybi syndrome. J Med Genet. 2002;39:415–21.PubMedCentralPubMedCrossRef

46.

Kalkhoven E, Roelfsema JH, Teunissen H, den Boer A, Ariyurek Y, Zantema A, et al. Loss of CBP acetyltransferase activity by PHD finger mutations in Rubinstein-Taybi syndrome. Hum Mol Genet. 2003;12:441–50.PubMedCrossRef

47.

Hennekam RC. Rubinstein-Taybi syndrome. Eur J Hum Genet. 2006;14:981–5.PubMedCrossRef

48.

Roelfsema JH, White SJ, Ariyürek Y, Bartholdi D, Niedrist D, Papadia F, et al. Genetic heterogeneity in Rubinstein-Taybi syndrome: mutations in both the CBP and EP300 genes cause disease. Am J Hum Genet. 2005;76:572–80.PubMedCentralPubMedCrossRef

49.

Hennekam RC, Baselier AC, Beyaert E, Bos A. Psychological and speech studies in Rubinstein-Taybi syndrome. Am J Ment Retard. 1992;96:645–60.PubMed

50.

Gotts EE, Liemohn WP. Behavioural characteristics of three children with the broad-thumb-hallux (Rubinstein-Taybi) syndrome. Biol Psychiatry. 1977;12:413–23.PubMed

51.

Baxter G, Beer J. Rubinstein-Taybi syndrome. Phys Rep. 1992;70:451–6.

52.

Stevens CA, Carey JC, Blackburn BL. Rubinstein-Taybi syndrome: a natural history study. Am J Med Genet. 1990;37:30–7.CrossRef

53.

Galéra C, Taupiac E, Fraisse S, Naudion S, Toussaint E, Rooryck-Thambo C, et al. Socio-behavioral characteristics of children with Rubinstein-Taybi syndrome. J Autism Dev Disord. 2009;39:1252–60.PubMedCrossRef

54.

Yagihashi T, Kenjiro K, Nobuhiko O, Mizuno S, Kenji K, Takao T, et al. Age-dependent change in behavioural feature in Rubinstein-Taybi syndrome. Congenit Anom. 2012;52:82–6.CrossRef

55.

Rutter M, Bailey A, Lord C. The social communication questionnaire. Los Angeles, CA: Western Psychological Services; 2003.

56.

Sparrow SS, Cicchetti DV, Balla DA. Vineland-II adaptive behavior scales: survey forms manual. Circle Pines, MN: AGS Publishing; 2005.

57.

Tottenham N, Tanaka JW, Leon AC, McCarry T, Nurse M, Hare TA, et al. The NimStim set of facial expressions: judgments from untrained research participants. Psychiatry Res. 2009;168:242–9.PubMedCentralPubMedCrossRef

58.

Jones W, Carr K, Klin A. Absence of preferential looking to the eyes of approaching adults predicts level of social disability in 2-year-olds with autism. Arch Gen Psychiatry. 2008;65.

59.

Campbell DJ, Shic F, Macari S, Chawarska K. Gaze response to dyadic bids at 2 years related to outcomes at 3 years in autism spectrum disorders: a subtyping analysis. J Autism Dev Disord. 2014;44:431–42.PubMedCentralPubMedCrossRef

60.

Rice K, Moriuchi JM, Jones W, Klin A. Parsing heterogeneity in autism spectrum disorders: visual scanning of dynamic social scenes in school-aged children. J Am Acad Child Adolesc Psychiatry. 2012;51:238–43.PubMedCentralPubMedCrossRef

61.

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. Arch Gen Psychiatry. 2002;59:809–16.PubMedCrossRef

62.

Perry A, Flanagan HE, HGeiser JD, Freeman NL. Brief report: the Vineland adaptive behavior scales in young children with autism spectrum disorders at different cognitive levels. J Autism Dev Disord. 2009;39:1066–78.PubMedCrossRef

63.

Bölte S, Poustka F. The relation between general cognitive level and adaptive behaviour domains in individuals with autism with and without comorbid mental retardation. Child Psychiatry Hum Dev. 2002;33:165–72.PubMedCrossRef

64.

Desimone R, Duncan J. Neural mechanisms of selective visual attention. Annu Rev Neurosci. 1995;18:193–222.PubMedCrossRef

65.

Peeters G, Czapinski J. Positive-negative asymmetry in evaluations: the distinction between affective and informational negativity effects. Eur Rev Soc Psychol. 1990;1:33–60.CrossRef

66.

Öhman A, Mineka S. Fears, phobias, and preparedness: toward an evolved module of fear and fear learning. Psychol Rev. 2001;108:483.PubMedCrossRef

Title: Face scanning and spontaneous emotion preference in Cornelia de Lange syndrome and Rubinstein-Taybi syndrome
Authors: Hayley Crawford
Joanna Moss
Joseph P. McCleery
Giles M. Anderson
Chris Oliver
Publication date: 01-12-2015
Publisher: BioMed Central
Published in: Journal of Neurodevelopmental Disorders / Issue 1/2015
Print ISSN: 1866-1947
Electronic ISSN: 1866-1955
DOI: https://doi.org/10.1186/s11689-015-9119-4

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Springer Medicine

Face scanning and spontaneous emotion preference in Cornelia de Lange syndrome and Rubinstein-Taybi syndrome

Abstract

Background

Methods

Results

Conclusions

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

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