Theory of Mind and Executive Control Deficits in Typically Developing Adults and Adolescents with High Levels of Autism Traits

Elif Gökçen, Norah Frederickson, K V Petrides, Elif Gökçen, Norah Frederickson, K V Petrides

Abstract

Autism spectrum disorder (ASD) is characterised by profound difficulties in empathic processing and executive control. Whilst the links between these processes have been frequently investigated in populations with autism, few studies have examined them at the subclinical level. In addition, the contribution of alexithymia, a trait characterised by impaired interoceptive awareness and empathy, and elevated in those with ASD, is currently unclear. The present two-part study employed a comprehensive battery of tasks to examine these processes. Findings support the notion that executive function and theory of mind are related abilities. They also suggest that individuals with elevated levels of autism-like traits experience a partially similar pattern of social and executive function difficulties to those diagnosed with ASD, and that these impairments are not explained by co-occurring alexithymia.

Keywords: Alexithymia; Autism spectrum disorder; Executive control; Subclinical autism traits; Theory of mind.

References

    1. American Psychiatric Association . Diagnostic and statistical manual of mental disorders. 5. Arlington, VA: American Psychiatric Publishing; 2013.
    1. Apperly IA, Carroll DJ, Samson D, Qureshi A, Humphreys GW, Moffatt G. Why are there limits on theory of mind use? Evidence from adults’ ability to follow instructions from an ignorant speaker. Quarterly Journal of Experimental Psychology. 2010;63:1201–1217. doi: 10.1080/17470210903281582.
    1. Austin G, Groppe K, Elsner B. The reciprocal relationship between executive function and theory of mind in middle childhood: a 1-year longitudinal perspective. Frontiers in Psychology. 2014;5:655. doi: 10.3389/fpsyg.2014.00655.
    1. Bagby RM, Parker JDA, Taylor GJ. The twenty-item Toronto Alexithymia Scale-I. Item selection and cross-validation of the factor structure. Journal of Psychosomatic Research. 1994;38:23–32. doi: 10.1016/0022-3999(94)90005-1.
    1. Bagby RM, Taylor GJ, Quilty LC, Parker JD. Reexamining the factor structure of the 20-item Toronto alexithymia scale: commentary on Gignac, Palmer, and Stough. Journal of Personality Assessment. 2007;89:258–264. doi: 10.1080/00223890701629771.
    1. Baron-Cohen S, Jolliffe T, Mortimore C, Robertson M. Another advanced test of theory of mind: Evidence from very high-functioning adults with autism or Asperger Syndrome. Journal of Child Psychology and Psychiatry. 1997;38:813–822. doi: 10.1111/j.1469-7610.1997.tb01599.x.
    1. Baron-Cohen S, Wheelwright S. The empathy quotient (EQ). An investigation of adults with Asperger syndrome or high functioning autism, and normal sex differences. Journal of Autism and Developmental Disorders. 2004;34:163–175. doi: 10.1023/B:JADD.0000022607.19833.00.
    1. 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. Journal of Child Psychology and Psychiatry. 2001;42:241–251. doi: 10.1111/1469-7610.00715.
    1. Baron-Cohen S, Wheelwright S, Skinner R, Martin J, Clubley E. The autism-spectrum quotient (AQ): evidence from Asperger syndrome/high-functioning autism, males and females, scientists and mathematicians. Journal of Autism and Developmental Disorders. 2001;31:5–17. doi: 10.1023/A:1005653411471.
    1. Baron-Cohen S, Wheelwright S, Spong A, Scahill V, Lawson J. Are intuitive physics and intuitive psychology independent? A test with children with Asperger syndrome. Journal of Developmental and Learning Disorders. 2001;5:47–78.
    1. Bauminger N, Kasari C. Loneliness and friendship in high-functioning children with autism. Child Development. 2000;71:447–456. doi: 10.1111/1467-8624.00156.
    1. Bird G, Cook R. Mixed emotions: The contribution of alexithymia to the emotional symptoms of autism. Translational Psychiatry. 2013;3:e285. doi: 10.1038/tp.2013.61.
    1. Bird G, Silani G, Brindley R, White S, Frith U, Singer T. Empathic brain responses in insula are modulated by levels of alexithymia but not autism. Brain. 2010;133:1515–1525. doi: 10.1093/brain/awq060.
    1. Blair RJR. Psychophysiological responsiveness to the distress of others in children with autism. Personality and Individual Differences. 1999;26:477–485. doi: 10.1016/S0191-8869(98)00154-8.
    1. Bölte S, Duketis E, Poustka F, Holtmann M. Sex differences in cognitive domains and their clinical correlates in higher-functioning autism spectrum disorders. The International Journal of Research and Practice. 2011;15:497–511. doi: 10.1177/1362361310391116.
    1. Brainard DH. The psychophysics toolbox. Spatial Vision. 1997;10:433–436. doi: 10.1163/156856897X00357.
    1. Bull R, Phillips LH, Conway C. The role of control functions in mentalizing: Dual task studies of theory of mind and executive functioning. Cognition. 2008;107:663–672. doi: 10.1016/j.cognition.2007.07.015.
    1. Capps L, Kasari C, Yirmiya N, Sigman M. Parental perception of emotional expressiveness in children with autism. Journal of Consulting Clinical Psychology. 1993;61:475–484. doi: 10.1037/0022-006X.61.3.475.
    1. Carlson SM, Claxton LJ, Moses LJ. The relation between executive function and theory of mind is more than skin deep. Journal of Cognition and Development. 2013;16:186–197. doi: 10.1080/15248372.2013.824883.
    1. Carlson SM, Moses LJ. Individual differences in inhibitory control and children’s theory of mind. Child Development. 2001;72:1032–1053. doi: 10.1111/1467-8624.00333.
    1. Carlson SM, Moses LJ, Breton C. How specific is the relation between executive function and theory of mind? Contributions of inhibitory control and working memory. Infant and Child Development. 2002;11:73–92. doi: 10.1002/icd.298.
    1. Chamberlain B, Kasari C, Rotheram-Fuller E. Involvement or isolation? The social networks of children with autism in regular classrooms. Journal of Autism and Developmental Disorders. 2007;37:230–242. doi: 10.1007/s10803-006-0164-4.
    1. Christ SE, Kanne SM, Reiersen AM. Executive function in individuals with subthreshold autism traits. Neuropsychology. 2010;24:590–598. doi: 10.1037/a0019176.
    1. Cianchetti C, Corona S, Foscoliano M, Scalas F, Sannio-Fancello G. Modified Wisconsin Card Sorting Test: Proposal of a supplementary sorting method. Archives of Clinical Neuropsychology. 2005;20:555–558. doi: 10.1016/j.acn.2004.12.002.
    1. Cook R, Brewer R, Shah P, Bird G. Alexithymia, not autism, predicts poor recognition of emotional facial expressions. Psychological Science. 2013;24:723–732. doi: 10.1177/0956797612463582.
    1. Corbett BA, Constantine LJ, Hendren R, Rocke D, Ozonoff S. Examining executive functioning in children with autism spectrum disorder, attention deficit hyperactivity disorder and typical development. Psychiatry Research. 2009;166:210–222. doi: 10.1016/j.psychres.2008.02.005.
    1. Davis MH. A multidimensional approach to individual differences in empathy. JSAS Catalog of Selected Documents in Psychology. 1980;10:85.
    1. Dawson G, Meltzoff A, Osterling J, Rinaldi J. Neuropsychological correlates of early autistic symptoms. Child Development. 1998;69:1247–1482. doi: 10.2307/1132265.
    1. Decety J. The neurodevelopment of empathy in humans. Developmental Neuroscience. 2010;32:257–267. doi: 10.1159/000317771.
    1. Decety J, Jackson PL. A social-neuroscience perspective on empathy. Current Directions in Psychological Science. 2006;15:54–58. doi: 10.1111/j.0963-7214.2006.00406.x.
    1. Decety J, Lamm C. Human empathy through the lens of social neuroscience. Scientific World Journal. 2006;6:1146–1163. doi: 10.1100/tsw.2006.221.
    1. Dumontheil I, Apperly IA, Blakemore SJ. Online usage of theory of mind continues to develop in late adolescence. Developmental Science. 2010;13:331–338. doi: 10.1111/j.1467-7687.2009.00888.x.
    1. Dziobek I, Fleck S, Kalbe E, Rogers K, Hassenstab J, Brand M, et al. Introducing MASC: A movie for the assessment of social cognition. Journal of Autism and Developmental Disorders. 2006;36:623–636. doi: 10.1007/s10803-006-0107-0.
    1. Dziobek I, Rogers K, Fleck S, Bahnemann M, Heekeren HR, Wolf OT, Convit A. Dissociation of cognitive and emotional empathy in adults with Asperger syndrome using the Multifaceted Empathy Test (MET) Journal of Autism and Developmental Disorders. 2008;38:464–473. doi: 10.1007/s10803-007-0486-x.
    1. Eslinger PJ, Moore P, Anderson C, Grossman M. Social cognition, executive functioning, and neuroimaging correlates of empathic deficits in frontotemporal dementia. Journal of Neuropsychiatry and Clinical Neurosciences. 2011;23:74–82. doi: 10.1176/appi.neuropsych.23.1.74.
    1. Fan YT, Chen C, Chen SC, Decety J, Cheng Y. Empathic arousal and social understanding in individuals with autism: evidence from fMRI and ERP measurements. Social Cognitive Affective Neuroscience. 2014;9:1203–1213. doi: 10.1093/scan/nst101.
    1. Frith U, Frith CD. Development and neurophysiology of mentalizing. Philosophical Transactions of the Royal Society of London Series B—Biological Sciences. 2003;358:459–473. doi: 10.1098/rstb.2002.1218.
    1. Gökçen E, Petrides KV, Hudry K, Frederickson N, Smillie LD. Sub-threshold autism traits: The role of trait emotional intelligence and cognitive flexibility. British Journal of Psychology. 2014;105:187–199. doi: 10.1111/bjop.12033.
    1. Grant A, Berg EA. Behavioural analysis of degree of reinforcement and ease of shifting to new responses in a Weigl-type card-sorting problem. Journal of Experimental Psychology. 1948;38:404–411. doi: 10.1037/h0059831.
    1. Hadjikhani N, Zurcher NR, Rogier O, Hippolyte L, Lemonnier E, et al. Emotional contagion for pain is intact in autism spectrum disorders. Translational Psychiatry. 2014;4:e343. doi: 10.1038/tp.2013.113.
    1. Heavey L, Phillips W, Baron-Cohen S, Rutter M. The Awkward Moments Test: A naturalistic measure of social understanding in autism. Journal of Autism and Developmental Disorders. 2000;30:225–236. doi: 10.1023/A:1005544518785.
    1. Hill EL. Evaluating the theory of executive dysfunction in autism. Developmental Review. 2004;24:189–233. doi: 10.1016/j.dr.2004.01.001.
    1. Hill EL. Executive dysfunction in autism. Trends in Cognitive Sciences. 2004;8:26–32. doi: 10.1016/j.tics.2003.11.003.
    1. Horn W. Leistungsprufsystem: LPS. Göttingen: Hogrefe; 1962.
    1. Hughes C. Executive function in preschoolers: Links with theory of mind and verbal ability. British Journal of Developmental Psychology. 1998;16:233–253. doi: 10.1111/j.2044-835X.1998.tb00921.x.
    1. Hughes C. Finding your marbles: Does preschoolers’ strategic behavior predict later understanding of mind? Developmental Psychology. 1998;34:1326–1339. doi: 10.1037/0012-1649.34.6.1326.
    1. Hughes C, Ensor R. Executive function and theory of mind: Predictive relations from ages 2 to 4. Developmental Psychology. 2007;43:1447–1459. doi: 10.1037/0012-1649.43.6.1447.
    1. Jones AP, Happé FG, Gilbert F, Burnett S, Viding E. Feeling, caring, knowing: different types of empathy deficit in boys with psychopathic tendencies and autism spectrum disorder. Journal of Child Psychology and Psychiatry. 2010;51:1188–1197. doi: 10.1111/j.1469-7610.2010.02280.x.
    1. Joseph RM, Tager-Flusberg H. The relationship of theory of mind and executive functions to symptom type and severity in children with autism. Development and Psychopathology. 2004;16:137–155. doi: 10.1017/S095457940404444X.
    1. Jurado MB, Rosselli M. The elusive nature of executive functions: A review of our current understanding. Neuropsychological Review. 2007;17:213–233. doi: 10.1007/s11065-007-9040-z.
    1. Kaiser S, Aschenbrenner S, Pfüller U, Roesch-Ely D, Weisbrod M. INHIB –Test battery for response inhibition. Mödling: Schuhfried; 2010.
    1. Kaller CP, Unterrainer JM, Kaiser S, Weisbrod M, Aschenbrenner S. Tower of London-Freiburg Version. Mödling: Schuhfried; 2012.
    1. Koven NS, Thomas W. Mapping facets of alexithymia to executive dysfunction in daily life. Personality and Individual Differences. 2010;49:24–28. doi: 10.1016/j.paid.2010.02.034.
    1. Lahera G, Boada L, Pousa E, Mirapeix I, Morón-Nozaleda G, Marinas L, Parellada M. Movie for the Assessment of Social Cognition (MASC): Spanish validation. Journal of Autism and Developmental Disorders. 2014;44:1886–1896. doi: 10.1007/s10803-014-2061-6.
    1. Lehnhardt FG, Falter CM, Gawronski A, Pfeiffer K, Tepest R, Franklin J, Vogeley K. Sex-related cognitive profile in autism spectrum disorders diagnosed late in life: Implications for the female autistic phenotype. Journal of Autism and Developmental Disorders. 2016;46:139–154. doi: 10.1007/s10803-015-2558-7.
    1. Lezak MD. Neuropsychological assessment. 3. New York: Oxford University Press; 1995.
    1. Lockwood PL, Bird G, Bridge M, Viding E. Dissecting empathy: high levels of psychopathic and autistic traits are characterized by difficulties in different social information processing domains. Frontiers in Human Neuroscience. 2013;7:760. doi: 10.3389/fnhum.2013.00760.
    1. McEvoy RE, Rogers SJ, Pennington BF. Executive function and social communication deficits in young autistic children. Journal of Child Psychology and Psychiatry. 1993;34:563–578. doi: 10.1111/j.1469-7610.1993.tb01036.x.
    1. Minio-Paluello I, Baron-Cohen S, Avenanti A, Walsh V, Aglioti SM. Absence of embodied empathy during pain observation in Asperger syndrome. Biological Psychiatry. 2009;65:55–62. doi: 10.1016/j.biopsych.2008.08.006.
    1. Montag C, Dziobek I, Richter IS, Neuhaus K, Lehmann A, Sylla R, et al. Different aspects of theory of mind in paranoid schizophrenia: evidence from a video-based assessment. Psychiatry Research. 2011;186:203–209. doi: 10.1016/j.psychres.2010.09.006.
    1. Moriguchi Y, Ohnishi T, Lane RD, Maeda M, Mori T, Nemoto K, et al. Impaired self-awareness and theory of mind: An fMRI study of mentalizing in alexithymia. Neuroimage. 2006;32:1472–1482. doi: 10.1016/j.neuroimage.2006.04.186.
    1. Nemiah JC, Freyberger H, Sifneos PE. Alexithymia: A view of the psychosomatic process. In: Hill OW, editor. Modern trends in psychosomatic medicine. London: Butterworths; 1976. pp. 430–439.
    1. Ozonoff S, Pennington BF, Rogers SJ. Executive function deficits in high-functioning autistic individuals: Relationship to theory of mind. Journal of Child Psychology and Psychiatry. 1991;32:1081–1105. doi: 10.1111/j.1469-7610.1991.tb00351.x.
    1. Parker JDA, Taylor GJ, Bagby RM. The 20-item Toronto Alexithymia Scale: III. Reliability and factorial validity in a community population. Journal of Psychosomatic Research. 2003;55:269–275. doi: 10.1016/S0022-3999(02)00578-0.
    1. Pelli DG. The VideoToolbox software for visual psychophysics: Transforming numbers into movies. Spatial Vision. 1997;10:437–442. doi: 10.1163/156856897X00366.
    1. Pellicano E. Links between theory of mind and executive function in young children: Clues to developmental primacy. Developmental Psychology. 2007;43:974–990. doi: 10.1037/0012-1649.43.4.974.
    1. Perner J. The meta-intentional nature of executive functions and theory of mind. In: Carruthers P, Boucher J, editors. Language and thought: Interdisciplinary themes. Cambridge: Cambridge University Press; 1998. pp. 270–283.
    1. Perner J. About + belief + counterfactual. In: Mitchell P, Riggs K, editors. Children’s reasoning and the mind. Hove: Psychology Press; 2000. pp. 367–401.
    1. Perner J, Lang B. Theory of mind and executive function: Is there a developmental relationship. In: Baron-Cohen S, Tager-Flusberg T, Cohen D, editors. Understanding other minds: Perspectives from developmental cognitive neuroscience. 2. Oxford: Oxford University Press; 2000. pp. 150–181.
    1. Perner J, Lang B, Kloo D. Theory of mind and self-control: More than a common problem of inhibition. Child Development. 2002;73:752–767. doi: 10.1111/1467-8624.00436.
    1. Ponnet K, Buysse A, Roeyers H, De Clercq A. Mind reading in young adults with ASD: Does structure matter? Journal of Autism and Developmental Disorders. 2008;38:905–918. doi: 10.1007/s10803-007-0462-5.
    1. Preißler S, Dziobek I, Ritter K, Heekeren HR, Roepke S. Social cognition in borderline personality disorder: Evidence for disturbed recognition of the emotions, thoughts, and intentions of others. Frontiers in Behavioural Neuroscience. 2010;4:182. doi: 10.3389/fnbeh.2010.00182.
    1. Premack D, Woodruff G. Does the chimpanzee have a theory of mind? Behavioral and Brain Sciences. 1978;1:515–526. doi: 10.1017/S0140525X00076512.
    1. Purdon SE. The screen for cognitive impairment in psychiatry (SCIP): administration manual and normative data. Edmonton: PNL Inc; 2005.
    1. Rameson LT, Morelli SA, Lieberman MD. The neural correlates of empathy: Experience, automaticity, and prosocial behavior. Journal of Cognitive Neuroscience. 2012;24:235–245. doi: 10.1162/jocn_a_00130.
    1. Reitan RM, Wolfson D. The Halstead Reitan Neuropsychological test battery: Theory and clinical interpretation. Tuscon, AZ: Neuropsychology Press; 1993.
    1. Robinson S, Goddard L, Dritschel B, Wisley M, Howlin P. Executive functions in children with autism spectrum disorders. Brain and Cognition. 2009;71:362–368. doi: 10.1016/j.bandc.2009.06.007.
    1. Rogers K, Dziobek I, Hassenstab J, Wolf OT, Convit A. Who cares? Revisiting empathy in Asperger syndrome. Journal of Autism and Developmental Disorders. 2007;37:709–715. doi: 10.1007/s10803-006-0197-8.
    1. Russell J. How executive disorders can bring about an adequate theory of mind. In: Russell J, editor. Autism as an executive disorder. Oxford, England: Oxford University Press; 1997. pp. 256–304.
    1. Russell J. Cognitive theories of autism. In: Harrison JE, Owen AM, editors. Cognitive deficits in brain disorders. London: Martin Dunitz; 2002. pp. 295–323.
    1. Russo N, Flanagan T, Iarocci G, Berringer D, Zelazo PD, Burack JA. Deconstructing executive deficits among persons with autism: Implications for cognitive neuroscience. Brain and Cognition. 2007;65:77–86. doi: 10.1016/j.bandc.2006.04.007.
    1. Sabbagh MA, Xu F, Carlson SM, Moses LJ, Lee K. The development of executive functioning and theory of mind: A comparison of Chinese and US preschoolers. Psychological Science. 2006;17:74–81. doi: 10.1111/j.1467-9280.2005.01667.x.
    1. Schwenck C, Mergenthaler J, Keller K, Zech J, Salehi S, Taurines R, et al. Empathy in children with autism and conduct disorder: Group-specific profiles and developmental aspects. Journal of Child Psychology and Psychiatry. 2012;53:651–659. doi: 10.1111/j.1469-7610.2011.02499.x.
    1. Seara-Cardoso A, Craig N, Roiser J, McCrory E, Viding E. Investigating associations between empathy, morality and psychopathic personality traits in the general population. Personality and Individual Differences. 2012;52:67–71. doi: 10.1016/j.paid.2011.08.029.
    1. Shamay-Tsoory SG. The neural bases for empathy. Neuroscientist. 2011;17:18–24. doi: 10.1177/1073858410379268.
    1. Shamay-Tsoory SG, Aharon-Peretz J, Perry D. Two systems for empathy: A double dissociation between emotional and cognitive empathy in inferior frontal gyrus versus ventromedial prefrontal lesions. Brain. 2009;132:617–627. doi: 10.1093/brain/awn279.
    1. Silani G, Bird G, Brindley R, Singer T, Frith C, Frith U. Levels of emotional awareness and autism: An fMRI study. Social Neuroscience. 2008;3:97–112. doi: 10.1080/17470910701577020.
    1. Singer T. The neuronal basis and ontogeny of empathy and mind reading: Review of literature and implications for future research. Neuroscience and Biobehavioral Reviews. 2006;30:855–863. doi: 10.1016/j.neubiorev.2006.06.011.
    1. Singer T, Lamm C. The social neuroscience of empathy. Year in cognitive neuroscience 2009. Annals of the New York Academy of Science. 2009;1156:81–96. doi: 10.1111/j.1749-6632.2009.04418.x.
    1. Smillie LD, Cooper AJ, Tharp IJ, Pelling EL. Individual differences in cognitive control: The role of psychoticism and working memory in set-shifting. British Journal of Psychology. 2009;100:629–643. doi: 10.1348/000712608X382094.
    1. Smith A. The empathy imbalance hypothesis of autism: A theoretical approach to cognitive and emotional empathy in autistic development. Psychological Record. 2009;59:489–510.
    1. Stroop JR. Studies of interference in serial verbal reactions. Journal of Experimental Psychology. Learning, Memory, and Cognition. 1935;18:643–662.
    1. Stuss DT, Knight RT. Principles of frontal lobe function. Oxford: Oxford University Press; 2002.
    1. Tantam D. The challenge of adolescents and adults with asperger syndrome. Child Adolescence and Psychiatric Clinics of North America. 2003;12:143–163. doi: 10.1016/S1056-4993(02)00053-6.
    1. Vetter NC, Altgassen M, Phillips L, Mahy CEV, Kliegel M. Development of affective theory of mind across adolescence: disentangling the role of executive functions. Developmental Neuropsychology. 2013;38:114–125. doi: 10.1080/87565641.2012.733786.
    1. von dem Hagen EA, Nummenmaa L, Yu R, Engell AD, Ewbank MP, Calder AJ. Autism spectrum traits in the typical population predict structure and function in the superior temporal sulcus. Cerebral Cortex. 2011;21:493–500. doi: 10.1093/cercor/bhq062.
    1. Wechsler D. Wechsler Abbreviated Scale of intelligence. San Antonio, TX: The Psychological Corporation; 1999.
    1. Woodbury-Smith MR, Robinson J, Wheelwright S, Baron-Cohen S. Screening adults for Asperger syndrome using the AQ: A preliminary study of its diagnostic validity in clinical practice. Journal of Autism and Developmental Disorders. 2005;35:331–335. doi: 10.1007/s10803-005-3300-7.

Source: PubMed

3
Prenumerera