The regulatory function of social referencing in preschoolers with Down syndrome or Williams syndrome

Journal of Neurodevelopmental Disorders

Carolyn B Mervis²  Angela John Thurman¹ 

[1] MIND Institute, Department of Psychiatry and Behavioral Sciences, University of California, UC Davis, 2825 50th Street, Room 2101, Sacramento, CA, 95817, USA;Department of Psychological and Brain Sciences, University of Louisville, Louisville, KY, 40292, USA

关键词: Williams-Beuren syndrome;    Social referencing;    Joint attention;    Intellectual disability;    Gaze following;    Emotional responsivity;    Eye contact;    Down syndrome;   

Others  :  811577
DOI  :  10.1186/1866-1955-5-2

 received in 2012-05-19, accepted in 2013-01-25,  发布年份 2013

【 摘 要 】

Background

An important developmental task is to learn to recognize another person as a source of information and to utilize this information as a method of learning about the surrounding world. This socially guided form of learning, referred to as social referencing, is critical for the development of children’s understanding of other people, themselves and their surrounding world. In the present project, the regulatory function of social referencing was examined in two genetic disorders that are characterized by differing patterns of socio-cognitive development: Down syndrome (DS) and Williams syndrome (WS).

Methods

Participants were 20 children with DS and 20 children with WS aged 42 to 71 months, matched on chronological age and gender. Each child participated in four studies: one study in which we examined performance in a social referencing paradigm and three studies in which we considered performance on tasks designed to tap each of three component abilities (initiating eye contact, gaze following and emotional responsivity) important for success in social referencing.

Results

The majority of children in both groups demonstrated positive behavioral responses regarding the stimulus in the Social Referencing task when the adult communicated a joyful message but did not regulate their own behavior in accordance with the adult’s expression of fear. Between-group differences were observed in both conditions, with most differences indicating more advanced socio-communicative competence for children with DS than for children with WS even though the overall intellectual abilities and receptive language abilities of the children with WS were significantly higher than were those of the children with DS. The results of follow-up studies indicated that children with DS were more likely to initiate eye contact (unsolicited) and to follow another person’s gaze in triadic situations than were children with WS. Neither group regulated their behavior in response to expressions of fear.

Conclusions

These findings provide new insight into the development of the social cognitive phenotypes associated with DS and WS. These social cognitive differences found during the preschool years likely contribute to the differing phenotypes observed later in life between individuals with DS and individuals with WS.

【 授权许可】

   
2013 Thurman and Mervis; licensee BioMed Central Ltd.

【 参考文献 】

• [1]Feinman S: Social referencing in infancy. Merrill-Palmer Quart 1982, 28:445-470.
• [2]Campos JJ, Stenberg C: Perception, appraisal, and emotion: The onset of social referencing. In Infant Social Cognition: Empirical and Theoretical Considerations. Edited by Lamb ME, Sherrod LR. Hillsdale, NJ: Lawrence Erlbaum Associates; 1981:273-314.
• [3]Klinnert MD, Emde RN, Butterfield P, Campos JJ: Social referencing: The infant's use of emotional signals from a friendly adult with mother present. Dev Psychol 1986, 22:427-432.
• [4]Hala S (Ed): The Development of Social Cognition. Hove, England: Psychology Press/Erlbaum (UK) Taylor & Francis; 1997.
• [5]Feinman S, Lewis M: Social referencing at ten months: A second-order effect on infants' responses to strangers. Child Dev 1983, 54:878-887.
• [6]Centers for Disease Control and Prevention: Improved national prevalence estimates for 18 selected major birth defects - United States, 1999–2001. Morb Mortal Wkly Rep 2006, 54:1301-1305.
• [7]Korenberg JR, Chen XN, Schipper R, Sun Z, Gonsky R, Gerwehr S, Disteche C: Down syndrome phenotypes: The consequences of chromosomal imbalances. Proc Natl Acad Sci 1994, 91:4997-5001.
• [8]Fidler DJ: The emerging Down syndrome behavioral phenotype in early childhood: Implications for practice. Infants Young Child 2005, 18:86-103.
• [9]Klein BP, Mervis CB: Contrasting patterns of cognitive abilities of 9- and 10-year-olds with Williams syndrome or Down syndrome. Dev Neuropsychol 1999, 16:177-196.
• [10]Wishart J, Johnston FH: The effects of experience on attribution of a stereotyped personality to children with Down's syndrome. J Ment Defic Res 1990, 34:409-420.
• [11]Carr J: Down's Syndrome: Children Growing Up. Cambridge: Cambridge University Press; 1995.
• [12]Jahromi LB, Gulsrud A, Kasari C: Emotional competence in children with Down syndrome: Negativity and regulation. Am J Ment Retard 2008, 113:32-43.
• [13]Porter MA: Cognitive and Social Skills in Neurodevelopmental Disorders: An Examination of Williams Syndrome, Down syndrome, and Autism. Saarbrücken, Germany: VDM Verlag Dr. Müller Aktiengesellschaft & Co; 2008.
• [14]Strømme P, Bjørnstad PG, Ramstad K: Prevalence estimation of Williams syndrome. J Child Neuropsychol 2002, 17:269-271.
• [15]Morris CA: The dysmorphology, genetics, and natural history of Williams-Beuren syndrome. In Williams-Beuren syndrome: Research, Evaluation and Treatment. Edited by Morris CA, Lenhoff HM, Wang PP. Baltimore: Johns Hopkins University Press; 2006:3-17.
• [16]Mervis CB, Klein-Tasman BP: Williams syndrome: Cognition, personality, and adaptive behavior. Ment Retard Dev Disabil Res Rev 2000, 6:148-158.
• [17]Udwin O, Yule W: A cognitive and behavioural phenotype in Williams syndrome. J Clin Exp Neuropsychol 1991, 13:232-244.
• [18]Gosch A, Pankau R: Personality characteristics and behaviour problems in individuals of different ages with Williams syndrome. Dev Med Child Neurol 1997, 39:527-533.
• [19]Jones W, Bellugi U, Lai Z, Chiles M, Reilly J, Lincoln A: Adolphs R: II. Hypersociability in Williams syndrome. J Cog Neurosci 2000, 12:30-46.
• [20]Davies M, Udwin O, Howlin P: Adults with Williams syndrome. Preliminary study of social, emotional and behavioural difficulties. Br J Psychiatry 1998, 172:273-276.
• [21]Sullivan K, Winner E, Tager-Flusberg H: Can adolescents with Williams syndrome tell the difference between lies and jokes? Dev Neuropsychol 2003, 23:85-104.
• [22]Leyfer OT, Woodruff-Borden J, Klein-Tasman B, Fricke JS, Mervis CB: Prevalence of psychiatric disorders in 4 to 16-year-olds with Williams syndrome. Am J Med Gen 2006, 141B:615-622.
• [23]Woodruff-Borden J, Kistler DJ, Henderson DR, Crawford NA, Mervis CB: Longitudinal course of anxiety in children and adolescents with Williams syndrome. Am J Med Gen 2010, 154C:277-290.
• [24]Mervis CB, John AE: Cognitive and behavioral characteristics of Williams syndrome. Am J Med Gen 2010, 154C:266-276.
• [25]Tager-Flusberg H, Plesa Skwerer D: Social engagement in Williams syndrome. In The Development of Social Engagement: Neurobiological Perspectives. Edited by Marshall PJ, Fox N. Oxford: Oxford University Press; 2006:331-354.
• [26]Rowe ML, Peregrine E, Mervis CB: Communicative development in toddlers with Williams syndrome. Atlanta, GA: Poster presented at the Society for Research in Child Development; 2005.
• [27]John AE, Mervis CB: Comprehension of the communicative intent behind pointing and gazing gestures by young children with Down syndrome and Williams syndrome. J Speech Hear Res 2010, 53:950-960.
• [28]Mervis CB, Morris CA, Klein-Tasman BP, Bertrand J, Kwitny S, Appelbaum LG, Rice CE: Attentional characteristics of infants and toddlers with Williams syndrome during triadic interactions. Dev Neuropsychol 2003, 23:243-268.
• [29]Fidler DJ, Hepburn S, Most D, Philofsky A: Emotional responsivity in young children with Williams syndrome. Am J Ment Retard 2007, 112:194-206.
• [30]Elliott CD: Differential Ability Scales. 2nd edition. San Antonio, TX: Psychological Corporation; 2007.
• [31]Dunn LM, Dunn DM: The Peabody Picture Vocabulary Test. 4th edition. Minneapolis, MN: Pearson; 2007.
• [32]Izard CE: The Face of Emotion. New York: Appleton-Century-Crofts; 1971.
• [33]Ekman P, Friesen WV: Unmasking the Face. Cambridge, MA: Malor Books; 2003.
• [34]Hiatt SW, Campos JJ, Emde RN: Facial patterning and infant emotional expression: Happiness, surprise and fear. Child Dev 1979, 50:1020-1035.
• [35]Bretherton I (Ed): Intentional Communication and the Development of an Understanding of Mind. Hillsdale, NJ: Lawrence Erlbaum Associates, Inc; 1991.
• [36]Tomasello M (Ed): Joint Attention as Social Cognition. Hillsdale, NJ: Lawrence Erlbaum Associates, Inc; 1995.
• [37]Saxon TF, Frick JE, Colombo J: A longitudinal study of maternal interactional styles and infant visual attention. Merrill-Palmer Quart 1997, 43:48-66.
• [38]Trevarthen C, Hubley P: Secondary intersubjectivity: Confidence, confiding and acts of meaning in the first year. In Action, Gesture and Symbol: The Emergence of Language. Edited by Lock A. New York: Academic Press; 1978:183-229.
• [39]Bakeman R, Adamson LB: Coordinating attention to people and objects in mother-infant and peer-infant interaction. Child Dev 1984, 55:1278-1289.
• [40]Berger J, Cunningham C: The development of eye contact between mothers and normals versus Down's syndrome infants. Dev Psychol 1981, 17:678-689.
• [41]Berger J, Cunningham C: Development of early vocal behaviors and interactions in Down's syndrome and nonhandicapped infant-mother pairs. Dev Psychol 1983, 19:322-331.
• [42]Kasari C, Sigman M, Mundy P, Yirmiya N: Affective sharing in the context of joint attention interactions of normal, autistic, and mentally retarded children. J Autism Dev Disord 1990, 20:87-100.
• [43]Lewy AL, Dawson G: Social stimulation and joint attention in young autistic children. J Abnorm Child Psychol 1992, 20:555-566.
• [44]Mundy P, Sigman M, Kasari C, Yirmiya N: Nonverbal communication skills in Down syndrome. Child Dev 1988, 59:235-249.
• [45]Laing E, Butterworth G, Ansari D, Gsodl M, Longhi E, Panagiotaki G, Karmiloff-Smith A: Atypical development of language and social communication in toddlers with Williams syndrome. Dev Sci 2002, 5:233-246.
• [46]Phillips W, Baron-Cohen S, Rutter M: The role of eye contact in goal detection: Evidence from normal infants and children with and without autism or mental handicap. Dev Psychopathol 1992, 4:375-383.
• [47]John AE: The regulatory function of social referencing in preschoolers with Down syndrome or Williams syndrome: PhD thesis. University of Louisville, Dept. of Psychological and Brain Sciences; 2011.
• [48]Noldus: The Observer XT. Wageningen, The Netherlands: Noldus Information Technology BV; 2010.
• [49]Adamson LB: (Ed): Communication Development During Infancy. Madison, WI: Brown and Benchmark; 1995.
• [50]D'Entremont B, Hains SMJ, Muir D: A demonstration of gaze following in 3- to 6-month-olds. Infant Behav Dev 1997, 20:569-572.
• [51]Moor C: Gaze following and the control of attention. In Early Social Cognition: Understanding Others in the First Months of Life. Edited by Rochat P. Mahwah, NJ: Erlbaum; 1999.
• [52]Baron-Cohen S: Mindblindness: An Essay on Autism and Theory of Mind. Mit Pr; 1995.
• [53]Brooks R, Meltzoff A: The importance of eyes: How infants interpret adult looking behavior. Dev Psychol 2002, 38:958-966.
• [54]Corkum V, Moore C: Development of joint visual attention in infants. In Joint Attention: Its Origins and Role in Development. Edited by Moore C, Dunham PJ. Hillsdale, NJ: Erlbaum; 1995.
• [55]Leekam S, Baron-Cohen S, Perrett D, Milders M, Brown S: Eye-direction detection: A dissociation between geometric and joint attention skills in autism. Br J Dev Psychol 1997, 15:77-95.
• [56]Sigman M, Ruskin E: Continuity and change in the social competence of children with autism, Down syndrome, and developmental delays. Monogr Soc Res Child Dev 1999, 64:1-114.
• [57]Klein-Tasman BP, Mervis CB, Lord C, Phillips K: Socio-communicative deficits in young children with Williams syndrome: Performance on the Autism Diagnostic Observation Schedule. Child Neuropsychol 2007, 13:444-467.
• [58]Lincoln AJ, Searcy YM, Jones W, Lord C: Social interaction behaviors discriminate young children with autism and Williams syndrome. J Am Acad Child Adolesc Psychiatry 2007, 46:323-331.
• [59]Behne T, Carpenter M, Tomasello M: One-year-olds comprehend the communicative intentions behind gestures in a hiding game. Dev Sci 2005, 8:492-499.
• [60]Carpenter M, Nagell K, Tomasello M: Social cognition, joint attention, and communicative competence from 9 to 15 months of age. Monogr Res Child Dev 1998, 63:1-143. i-v
• [61]Holodynski M, Friedlmeier W: The internalization model of emotional development. In Development of Emotion and Emotion Regulation. Edited by Holodynski M, Friedlmeier W. New York: Springer; 2005:43-88.
• [62]Cohn JF, Campbell SB, Matias R, Hopkins J: Face-to-face interactions of postpartem depressed mother-infant pairs at 2 months. Dev Psychol 1990, 26:15-23.
• [63]Termine NT, Izard CE: Infants' responses to their mothers' expressions of joy and sadness. Dev Psychol 1988, 24:223-229.
• [64]Kasari C, Freeman SF, Hughes MA: Emotion recognition by children with Down syndrome. Am J Ment Retard 2001, 106:59-72.
• [65]Williams KR, Wishart JG, Pitcairn TK, Willis DS: Emotion recognition by children with Down syndrome: Investigation of specific impairments and error patterns. Am J Ment Retard 2005, 110:378-392.
• [66]Tager-Flusberg H, Sullivan K: A componential view of theory of mind: Evidence from Williams syndrome. Cognition 2000, 76:59-89.
• [67]Gagliardi C, Frigerio E, Burt D, Cazzaniga I, Perrett D, Borgatti R: Facial expression recognition in Williams syndrome. Neuropsychologia 2003, 41:733-738.
• [68]Scambler DJ, Hepburn S, Rutherford MD, Wehner EA, Rogers SJ: Emotional responsivity in children with autism, children with other developmental disabilities, and children with typical development. J Aut Dev Disord 2007, 37:553-563.
• [69]Plesa-Skwerer D, Tager-Flusberg H: Social cognition in Williams-Beuren syndrome. In Williams-Beuren Syndrome: Research, Evaluation and Treatment. Edited by Morris CA, Lenhoff HM, Wang PP. Baltimore: Johns Hopkins University Press; 2007:237-253.
• [70]Baldwin DA: Understanding the Link between Joint Attention and Language. Hillsdale, NJ: Lawrence Erlbaum Accociates; 1995.
• [71]Mundy P, Neal R: Neural plasticity, joint attention and transactional social-orienting model of autism. Intern Rev Ment Retard 2001, 23:139-168.
• [72]Tomasello M: Joint Attention as Social Cognition. Hillsdale, NJ, England: Lawrence Erlbaum Associates; 1995.
• [73]Charman T, Baron-Cohen S, Swettenham J, Baird G, Cox A, Drew A: Testing joint attention, imitation, and play as infancy precursors to language and theory of mind. Cogn Dev 2000, 15:481-498.
• [74]Yirmiya N, Solomonica-Levi D, Shulman C, Pilowsky T: Theory of mind abilities in individuals with autism, Down syndrome, and retardation of unknown etiology: The role of age and intelligence. J Child Psychol Psychiatry 1996, 37:1003-1014.
• [75]Abbeduto L, Pavetto M, Kesin E, Weissman M, Karadottir S, O’Brien A, Cawthon S: The linguistic and cognitive profile of Down syndrome: Evidence from a comparison with fragile X syndrome. Down Syndr Res Pract 2001, 7:9-15.
• [76]Tager-Flusberg H, Sullivan K, Boshart J: Executive functions and performance on false belief tasks. Dev Neuropsychol 1997, 13:487-493.
• [77]Mundy P, Block J, Vaughn Van Hecke A, Delgado C, Parlade M, Pomeras Y: Individual differences in the development of joint attention in infancy. Child Dev 2007, 78:938-954.
• [78]Mundy P, Gomes A: Individual differences in joint attention skill development in the second year. Infant Behav Dev 1998, 21:469-482.
• [79]Watson O’Reilly A, Painter KM, Bornstein MH: Relations between language and symbolic gesture development in early childhood. Cogn Dev 1997, 12:185-197.
• [80]Mervis CB, Becerra AM: Language and communicative development in Williams syndrome. Ment Retard Dev Disabil 2007, 13:3-15.
• [81]Edgin JO, Pennington BF, Mervis CB: Neuropsychological components of intellectual disability: The contributions of immediate, working, and associated memory. J Intellect Disabil Res 2010, 54:406-417.
• [82]Vicari S, Caselli MC, Gagliardi C, Tonucci F, Volterra V: Language acquisition in special populations: A comparison between Down syndrome and Williams syndrome. Neuropsychologia 2002, 40:2461-2470.
• [83]Wang PP, Bellugi U: Evidence from two genetic syndromes for dissociation between verbal and visual-spatial short-term memory. J Clin Exper Neuropsychol 1994, 16:317-322.
• [84]Gathercole SE, Willis CS, Emslie H, Baddeley AD: Phonological memory and vocabulary development during the early school years: A longitudinal study. Dev Psychol 1992, 28:887-898.
• [85]Robinson BF, Mervis CB, Robinson BW: The roles of verbal short-term memory and working memory in the acquisition of grammar by children with Williams syndrome. Dev Neuropsychol 2003, 23:13-31.
• [86]Edgin JO: A neuropsychological model for the development of the cognitive profiles in mental retardation syndromes: Evidence from Down syndrome and Williams syndrome. PhD thesis, University of Denver, Department of Psychology; 2003.
• [87]Vicari S, Bates E, Caselli M, Pasqualetti P, Gagliardi C, Tonucci F, Volterra V: Neuropsychological profile of Italians with Williams syndrome: An example of dissociation between language and cognition. J Intern Neuropsychol Soc 2004, 10:862-876.
• [88]Meltzoff AN: Understanding the intentions of others: Re-enactment of intended acts by 18-month-old children. Dev Psychol 1995, 31:838-850.
• [89]Davies M, Howlin P, Udwin O: Independence and adaptive behavior in adults with Williams syndrome. Am J Med Gen 1997, 70:188-195.
• [90]Howlin P, Udwin O: Outcome in adult life for people with Williams syndrome: Results from a survey of 239 families. J Intellecy Dis Res 2006, 50:151-160.
• [91]Williams JHG, Waiter GD, Perra O, Perrett DI, Whiten A: An fMRI study of joint attention experience. Neuroimage 2005, 25:113-140.
• [92]Carr L, Iacoboni M, Dubeau M-C, Mazziotta JC, Lenzi GL: Neural mechanisms of empathy in humans: A relay from neural systems for imitation to limbic areas. Proc Natl Acad Sci 2003, 100:5497-5502.
• [93]Singer T, Seymour B, O’Doherty J, Kaube H, Dolan RJ, Frith D: Empathy for pain involves the affective but not sensory components of pain. Science 2004, 303:1157-1162.
• [94]Pinter JD, Brown WE, Eliez S, Schmitt JE, Capone GT, Reiss AL: Amygdala and hippocampal volumes in children with Down syndrome: A high-resolution MRI study. Neurol 2001, 10:972-974.
• [95]Aylward EH, Li Q, Honeycutt NA, Warren AC, Pulsifer MB, Barta PE, Chan MD, Perlson GD: MRI volumes of the hippocampus and amygdala in adults with Down’s syndrome with and without dementia. Am J Psychiatry 1999, 156:564-568.
• [96]Menghini D, Costanzo F, Vicari S: Relationship between brain and cognitive processes in Down syndrome. Behav Gen 2011, 41:381-393.
• [97]Martens MA, Wilson S, Dudgeon P, Reutens DC: Approachabiltiy and the amygdala: Insights from Williams syndrome. Neuropsychologia 2009, 47:2446-2453.
• [98]Reiss AL, Eckert MA, Rose F, Karchemsky A, Kesler S, Chang M, Reynolds MF, Kwon H, Galaburda A: An experiment of nature: Brain anatomy parallels cognition and behavior in Williams syndrome. J Neurosci 2004, 24:5009-5015.
• [99]Capitão L, Sampaio A, Sampaio C, Vasconcelos C, Férnandez M, Garayzábal E, Gonçalves OF: MRI amygdala volume in Williams syndrome. Res Dev Disabil 2011, 6:2767-2772.
• [100]Meyer-Lindenberg A, Hariri AR, Munoz KE, Mervis CB, Mattay VS, Morris CA, Berman KF: Neural correlates of genetically abnormal social cognition in Williams syndrome. Nat Neurosci 2005, 8:991-993.
• [101]Menghini D, Di Paola M, Federico F, Vicari S, Petrosini L, Caltagirone C, Bozzali M: Relationship between brain abnormalities and cognitive profile in Williams syndrome. Behav Gen 2011, 41:394-402.
• [102]Cohen JD, Mock JR, Nichols T, Zadina J, Corey DM, Lemen L, Foundas AL: Morphometry of human insular cortex and insular volume reduction in Williams syndrome. J Psychiatr Res 2010, 44:81-89.
• [103]Jabbi M, Kippenhan JS, Kohn P, Marenco S, Mervis CB, Morris CA, Berman KF: The Williams syndrome chromosome 7q11.23 hemideletion confers hypersocial, anxious personality coupled with altered insula structure and function. Proc Natl Acad Sci 2012, 109:5164-5165.
• [104]Haas BW, Mills D, Yam A, Hoeft F, Bellugi U, Reiss A: Genetic influences on sociability: Heightened amygdala reactivity and event-related responses to positive social stimuli in Williams syndrome. J Neurosci 2009, 29:1132-1139.