Structural and Functional Neuroimaging of Restricted and Repetitive Behavior in Autism Spectrum Disorder
DOI:
https://doi.org/10.6000/2292-2598.2015.03.01.4Keywords:
Autism spectrum disorder, neuroimaging, repetitive behaviour, repetitive motor behaviour, insistence on sameness, circumscribed interests.Abstract
A prominent symptom of Autism Spectrum Disorder includes restricted and repetitive behaviours. This symptom has been divided into three subtypes: repetitive motor behaviour, insistence on sameness and circumscribed interests. In the past, the neural correlates of these behaviours have been largely understudied. More recently, neuroimaging studies have pointed to a number of neural networks that may underlay these behaviours. However, results from this work have been varied and remain difficult to integrate. The purpose of this review is to summarize recent neuroimaging studies on restricted and repetitive behaviours in autism, and to provide an organized framework that will permit a clearer understanding of the neural correlates of these behaviours. Using a developmental perspective, this review will identify that there are distinct and overlapping neural networks that are associated with repetitive motor behaviour, insistence on sameness and circumscribed interests. In addition, this review will identify a series of executive and affective function tasks that have proven efficacious in the study of repetitive behaviour.
References
American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders (5th ed.). Washington, DC: Author 2013. http://dx.doi.org/10.1176/appi.books.9780890425596 DOI: https://doi.org/10.1176/appi.books.9780890425596
Langen M, Kas M, Staal W, van Engeland H, Durston S. The neurobiology of repetitive behavior: of mice. Neurosci Biobehav Rev 2010; 35(Pt 3): 345-355. http://dx.doi.org/10.1016/j.neubiorev.2010.02.004 DOI: https://doi.org/10.1016/j.neubiorev.2010.02.004
Lewis M, Kim S. The pathophysiology of restricted and repetitive behavior. J Neurodev Disord 2009; 1: 114-132. http://dx.doi.org/10.1007/s11689-009-9019-6 DOI: https://doi.org/10.1007/s11689-009-9019-6
Lam KSL, Bodfish JW, Piven J. Evidence for three subtypes of repetitive behavior in autism that differ in familiality and association with other symptoms. The J Child Psychol Psychiatry 2008; 49(Pt 11): 1193-1200. http://dx.doi.org/10.1111/j.1469-7610.2008.01944.x DOI: https://doi.org/10.1111/j.1469-7610.2008.01944.x
Cuccaro ML, Shao Y, Grubber J, Slifer M, Wolpert CM, Donnelly SL, et al. Factor analysis of restricted and repetitive behaviors in autism using the Autism Diagnostic Interview-R. Child Psychiatry Hum Dev 2003; 34: 3-17. DOI: https://doi.org/10.1023/A:1025321707947
Szatmari P, Georgiades S, Bryson S, Zwaigenbaum L, Roberts W, Mahoney W, et al. Investigating the structure of the restricted and repetitive behaviors and interests domain of autism. J Child Psychol Psychiatry 2006; 47(Pt 6): 582-590. http://dx.doi.org/10.1111/j.1469-7610.2005.01537.x DOI: https://doi.org/10.1111/j.1469-7610.2005.01537.x
Lewis MH, Tanimura Y, Lee LW, Bodfish J. Animal models of restricted repetitive behavior in autism. Behav Brain Res 2007; 176: 66-74. http://dx.doi.org/10.1016/j.bbr.2006.08.023 DOI: https://doi.org/10.1016/j.bbr.2006.08.023
Turner MA. Annotation: repetitive behavior in autism: A review of psychological research. J Child Psychol Psychiatry 1999; 40(Pt 6): 839-849. DOI: https://doi.org/10.1017/S0021963099004278
Langen M, Bos D, Noordermeer SD, Nederveen H, van Engeland H, Durston S. Changes in the development of the striatum are involved in repetitive behaviors in autism. Biol Psychiatry 2013; 75(Pt 5): 405-411. http://dx.doi.org/10.1016/j.biopsych.2013.08.013 DOI: https://doi.org/10.1016/j.biopsych.2013.08.013
Duerden EG, Card D, Roberts W, Mak-Fan KM, Chakravarty M, Lerch JP, et al. Self-injurious behaviors are associated with alterations in the somatosensory system in children with autism spectrum disorder. Brain Struct Funct 2013; 219(Pt 4), 1251-1261. http://dx.doi.org/10.1007/s00429-013-0562-2 DOI: https://doi.org/10.1007/s00429-013-0562-2
Hollander E, Anagnostou E, Chaplin W, Esposito K, Haznedar M, Licalzi E, et al. Striatal volumes on magnetic resonance imaging and repetitive behaviors in autism. Biol Psychiatry 2005; 58(Pt 3): 226-232. http://dx.doi.org/10.1016/j.biopsych.2005.03.040 DOI: https://doi.org/10.1016/j.biopsych.2005.03.040
Sears LL, Vest C, Mohammed S, Bailey J, Rason BJ, Piven J. An MRI study of the basal ganglia in autism. Prog Neuropsychopharmacol Biol Psychiatry 1999; 23(Pt 4): 613-624. http://dx.doi.org/10.1016/S0278-5846(99)00020-2 DOI: https://doi.org/10.1016/S0278-5846(99)00020-2
Goldberg MC, Spinellia S, Joela S, Pekara JJ, Dencklaa MB, Mostofskya SH. Children with high functioning autism show increased prefrontal and temporal cortex activity during error monitoring. Dev Cogn Neuroscience 2011; 1(Pt 1): 47-56. http://dx.doi.org/10.1016/j.dcn.2010.07.00 DOI: https://doi.org/10.1016/j.dcn.2010.07.002
Anagnostou E, Taylor M. Review of neuroimaging in autism spectrum disorders: what have we learned and where do we go from here. Mol Autism 2011; 2(Pt 1): 4. http://dx.doi.org/10.1186/2040-2392-2-4 DOI: https://doi.org/10.1186/2040-2392-2-4
Just MA, Cherkassky VL, Keller TA, Kana RK, Minshew NJ. Functional and anatomical cortical underconnectivity in autism: Evidence from an FMRI study of an executive function task and corpus callosum morphometry. Cereb Cortex 2007; 17(Pt 4): 951-961. DOI: https://doi.org/10.1093/cercor/bhl006
Lopez BR, Lincoln AJ, Ozonoff S, Lai Z. Examining the relationship between executive functions and restricted, repetitive symptoms of autistic disorder. J Autism Dev Disord 2005; 35: 445-460. DOI: https://doi.org/10.1007/s10803-005-5035-x
Mosconi MW, Kay M, D’Cruz AM, Seidenfeld A, Guter S, Standford LD, et al. Impaired inhibitory control is associated with higher-order repetitive behaviors in autism spectrum disorders. Psychol Med 2009; 39(Pt 9): 1559-1566. http://dx.doi.org/10.1017/S0033291708004984 DOI: https://doi.org/10.1017/S0033291708004984
South M, Ozonoff S, McMahon WM. The relationship between executive functioning, central coherence and repetitive behaviors in the high-functioning autism spectrum. Autism 2007; 11: 437. http://dx.doi.org/10.1177/1362361307079606 DOI: https://doi.org/10.1177/1362361307079606
Pierce K, Courchesne E. Evidence for a cerebellar role in reduced exploration and stereotyped behavior in autism. Biol Psychiatry 2001; 49: 655-664. http://dx.doi.org/10.1016/S0006-3223(00)01008-8 DOI: https://doi.org/10.1016/S0006-3223(00)01008-8
Hardan AY, Girgis RR, Lacerda ALT, Yorbik O, Kilpatrick M, Keshavan M, et al. Magnetic resonance imaging study of the orbitofrontal cortex in autism. J Child Neurol 2005; 21: 866-871. http://dx.doi.org/10.1177/08830738060210100701 DOI: https://doi.org/10.1177/08830738060210100701
Arnott B, McConachie H, Meins E, Fernyhough C, Couteur AL, Turner M, et al. The frequency of restricted and repetitive behaviors in a community sample of 15-month-old-infants. J Dev Behav Pediatr 2010; 3: 223-229. http://dx.doi.org/10.1097/DBP.0b013e3181d5a2ad DOI: https://doi.org/10.1097/DBP.0b013e3181d5a2ad
Esposito G, Pasca SP. Motor abnormalities as a putative endophenotype for autism spectrum disorders. Front Integr Neurosci 2013; 7(Pt 43): 1-5. http://dx.doi.org/10.3389/fnint.2013.00043 DOI: https://doi.org/10.3389/fnint.2013.00043
Nordahl CW, Dierker D, Mostafavi I, Schumann CM, Rivera SM, Amaral DG, et al. Cortical folding abnormalities in autism revealed by surface-based morphometry. J Neurosci 2007; 27(Pt 43): 11725-11735. http://dx.doi.org/10.1523/JNEUROSCI.0777-07.2007 DOI: https://doi.org/10.1523/JNEUROSCI.0777-07.2007
Goldman S, O’Briende LM, Filipekf PA, Rapina I, Herbertgh MR. Motor stereotypies and volumetric brain alterations in children with autistic disorder. Res Autism Spect Disor 2013; 7(Pt 1): 82-92. http://dx.doi.org/10.1016/j.rasd.2012.07.005 DOI: https://doi.org/10.1016/j.rasd.2012.07.005
Boyd BA, Conroy MA, Richmond Mancil G, Nakao T, Alter P. Effects of circumscribed interests on the social behaviors of children with autism spectrum disorders. J Autism Dev Disord 2007; 37: 1555-1561. DOI: https://doi.org/10.1007/s10803-006-0286-8
Richler J, Bishop SL, Kleinke J, Lord C. Restricted and repetitive behaviors in young children with autism spectrum disorders. J Autism Dev Disord 2007; 37: 73-85. DOI: https://doi.org/10.1007/s10803-006-0332-6
Estes A, Shaw DWW, Sparks BF, Friedman S, Giedd JN, Dawson G, et al. Basal ganglia morphometry and repetitive behavior in young children with autism spectrum disorder. Autism Res 2011; 4(Pt 3): 212-220. http://dx.doi.org/10.1002/aur.193 DOI: https://doi.org/10.1002/aur.193
Langen M, Schnack HG, Nederveen H, Bos D, Lahuis BE, de Jonge MV, et al. Changes in the developmental trajectories of striatum in autism. Biol Psychiatry 2009; 66: 327-333. http://dx.doi.org/10.1016/j.biopsych.2009.03.017 DOI: https://doi.org/10.1016/j.biopsych.2009.03.017
Langen M, Durston S, Staal WG, Palmen SJMC, vanEngeland H. Caudate nucleus is enlarged in high-functioning medication-naïve subjects with autism. Biol Psychiatry 2007; 62(Pt 3): 262-266. http://dx.doi.org/10.1016/j.biopsych.2006.09.040 DOI: https://doi.org/10.1016/j.biopsych.2006.09.040
Herbert MR, Ziegler DA, Deutsch CK, O’Brien LM, Lange N, Bakardjiev A, et al. Dissociations of cerebral cortex, subcortical and white matter volumes in autistic boys. Brain 2003; 126(Pt 5): 1182-1192. http://dx.doi.org/10.1093/brain/awg110 DOI: https://doi.org/10.1093/brain/awg110
Voelbel G, Bates M, Buckman J, Pandina G, Hendren R. Caudate nucleus volume and cognitive performance: Are they related in childhood psychopathology? Biol Psychiatry 2006; 60(Pt 9): 942-950. http://dx.doi.org/10.1016/j.biopsych.2006.03.071 DOI: https://doi.org/10.1016/j.biopsych.2006.03.071
South M, Ozonof S, McMahon WM. Repetitive behavior profiles in Asperger syndrome and high functioning autism. J Autism Dev Disord 2005; 35(Pt 2): 145-158. DOI: https://doi.org/10.1007/s10803-004-1992-8
Kringelbach ML, Rolls ET. The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology. Prog Neurobiol 2004; 72(Pt 5): 341-372. http://dx.doi.org/10.1016/j.pneurobio.2004.03.006 DOI: https://doi.org/10.1016/j.pneurobio.2004.03.006
Evans DW, Lewis MD, Lobust E. The role of the orbitofrontal cortex in normally developing compulsive-like behaviors and obsessive compulsive disorder. Brain Cogn 2004; 55(Pt 1): 220-234. http://dx.doi.org/10.1016/S0278-2626(03)00274-4 DOI: https://doi.org/10.1016/S0278-2626(03)00274-4
Vink M, Kahn RS, Raemaekers M, van den Heuvel M, Boersma M, Ramsey NF. Function of striatum beyond inhibition and execution of motor responses. Hum Brain Mapp 2005; 25: 336-344. http://dx.doi.org/10.1002/hbm.20111 DOI: https://doi.org/10.1002/hbm.20111
Zanbelt BB, Vink M. On the role of the striatum in response inhibition. PLoS ONE 2010; 5(Pt 11): 1384. http://dx.doi.org/10.1371/journal.pone.0013848 DOI: https://doi.org/10.1371/journal.pone.0013848
Balleine BW, Delgado MR, Hikosaka, O. The role of the dorsal striatum in reward and decision-making. J Neurosci 2007; 27(Pt 31): 8161-8165. http://dx.doi.org/10.1523/JNEUROSCI.1554-07.2007 DOI: https://doi.org/10.1523/JNEUROSCI.1554-07.2007
Villablanca JR. Why do we have a caudate nucleus? Acta Neurobiol Exp (WARS) 2010; 70: 95-105. DOI: https://doi.org/10.55782/ane-2010-1778
Hagmann P, Cammoun L, Gigandet X, Meuli R, Honey CJ, Wedeen Van J, et al. Mapping the structural core of human cerebral cortex. PLoS Biol 2008; 6(Pt 7): e159. http://dx.doi.org/10.1371/journal.pbio.0060159 DOI: https://doi.org/10.1371/journal.pbio.0060159
Di X, Rao H. Progress in functional connectivity analysis. Progress in Biochemistry and Biophysics 2007; 1: 34-35.
Agam Y, Joseph RM, Barton JJS, Manoach DS. Reduced cognitive control of response inhibition by the anterior cingulate cortex in autism spectrum disorders. NeuroImage 2010; 52: 336-347. http://dx.doi.org/10.1016/j.neuroimage.2010.04.010 DOI: https://doi.org/10.1016/j.neuroimage.2010.04.010
Kana RK, Keller TA, Minsher NJ, Just MA. Inhibitory control in high-functioning autism: Decreased activation and underconnectivity in inhibition networks. Biol Psychiatry 2007; 62(Pt 3): 198-206. http://dx.doi.org/10.1016/j.biopsych.2006.08.004 DOI: https://doi.org/10.1016/j.biopsych.2006.08.004
Schmitz N, Rubia K, Daly E, Smith A, Williams S, Murphy DGM. Neural correlates of executive function in autistic spectrum disorders. Biol Psychiatry 2006; 59: 7-16. http://dx.doi.org/10.1016/j.biopsych.2005.06.007 DOI: https://doi.org/10.1016/j.biopsych.2005.06.007
Mizuno A, Villalobosa ME, Daviesa MM, Dahla BC, Muller R. Partially enhanced thalamocortical functional connectivity in autism. Brain Res 2006; 1104: 160-174. http://dx.doi.org/10.1016/j.brainres.2006.05.064 DOI: https://doi.org/10.1016/j.brainres.2006.05.064
Turner KC, Frost L, Linsencardt D, McIlroy JR, Muller R. Atypical diffuse functional connectivity between caudate nuclei and cerebral cortex in autism. Behav Brain Funct 2006; 2(Pt 1): 34. http://dx.doi.org/10.1186/1744-9081-2-34 DOI: https://doi.org/10.1186/1744-9081-2-34
Boyd BA, McBee M, Holtzclaw T, Baranek GT, Bodfish JW. Relationships among repetitive behaviors, sensory features, and executive functions in high functioning autism. Res Autism Spect Disord 2009; 3(Pt 4): 959-966. http://dx.doi.org/10.1016/j.rasd.2009.05.003 DOI: https://doi.org/10.1016/j.rasd.2009.05.003
Bolling DZ, Pitskel NB, Deen B, Crowley MJ, McPartland JC, Kaiser MD, et al. Enhanced neural responses to rule violation in children with autism: A comparison to social exclusion. Dev Cogn Neurosci 2011; 1(Pt 3): 280-294. http://dx.doi.org/10.1016/j.dcn.2011.02.002 DOI: https://doi.org/10.1016/j.dcn.2011.02.002
Solomon M, Ozonoff SJ, Ursu S, Ravizza S, Cummings N, Ly S, Carter CS. The neural substrates of cognitive control deficits in autism spectrum disorder. Neuropsychologia 2009; 47: 2515-2526. http://dx.doi.org/10.1016/j.neuropsychologia.2009.04.019 DOI: https://doi.org/10.1016/j.neuropsychologia.2009.04.019
Uddin LQ, Supekar K, Lynch CJ, Khouzam A, Phillips J, Feinstein C, et al. Salience network-based classification and prediction of symptom severity in children with autism. JAMA Psychiatry 2013; 1-11. http://dx.doi.org/10.1001/jamapsychiatry.2013.104 DOI: https://doi.org/10.1001/jamapsychiatry.2013.104
Paulus MP, Stein MB. An insular view of anxiety. Biol Psychiatry 2006; 60: 383-387. http://dx.doi.org/10.1016/j.biopsych.2006.03.042 DOI: https://doi.org/10.1016/j.biopsych.2006.03.042
Ptak R. The frontoparietal attention network of the human brain: action, saliency, and a priority map of the environment. Neuroscientist 2012; 18(Pt 5): 502-515. http://dx.doi.org/10.1177/1073858411409051 DOI: https://doi.org/10.1177/1073858411409051
Fan J. Attentional network deficits in autism spectrum disorders. In: Buxbaum, JD and Hof PR, editors. The Neuroscience of Autism Spectrum Disorders. Elsevier Inc 2013, p. 281-288. DOI: https://doi.org/10.1016/B978-0-12-391924-3.00019-3
Clery H, Andersson F, Bonnet-Brilhault F, Philippe A, Wicker B, Gornot M. fMRI investigation of visual change detection in adults with autism. Neuroimage Clin 2013; 2: 303-312. http://dx.doi.org/10.1016/j.nicl.2013.01.010 DOI: https://doi.org/10.1016/j.nicl.2013.01.010
Shafritz KM, Dichter GS, Baranek GT, Belger A. The neural circuitry mediating shifts in behavioral response and cognitive set in autism. Biol Psychiatry 2008; 63(Pt 10): 974-980. http://dx.doi.org/10.1016/j.biopsych.2007.06.028 DOI: https://doi.org/10.1016/j.biopsych.2007.06.028
Casico JC, Foss-Feig JH, Heacock J, Schauder KB, Loring WA, Rogers BP, et al. Affective neural response to restricted interests in autism spectrum disorders. J Child Psychol Psychiatry 2013; 55(Pt 2): 162-171.
http://doi.org/10.1111/jcpp.12147 DOI: https://doi.org/10.1111/jcpp.12147
Dichter GS, Felder JN, Green SR, Rittenberg AM, Sasson NJ, Bodfish JW. Reward circuitry function in autism spectrum disorders. SCAN 2012; 7: 160-172. http://dx.doi.org/10.1093/scan/nsq095 DOI: https://doi.org/10.1093/scan/nsq095
Sabatino A, Rittenberg A, Sasson NJ, Turner-Brown L, Bodfish JW, Dichter GS. Functional neuroimaging of social and nonsocial cognitive control in autism. J Autism Dev Disord 2013; 43(Pt 12): 2903-2913. http://dx.doi.org/10.1007/s10803-013-1837-4 DOI: https://doi.org/10.1007/s10803-013-1837-4
Courchesne E, Townsend J, Akshoomoff NA, Saitoh O, Yeung-Courchesne R, Lincoln AJ, et al. Impairment in shifting attention in autistic and cerebellar patients. Behav Neurosci 1994; 108: 848-856. http://dx.doi.org/10.1037/0735-7044.108.5.848 DOI: https://doi.org/10.1037//0735-7044.108.5.848
Delmonte S, Gallagher L, O’Hanlon E, McGrath J, Balsters JH. Functional and structural connectivity of frontostriatal circuitry in autism spectrum disorder. Front Hum Neurosci 2013; 7 (Pt 430): 1-14. http://dx.doi.org/10.3389/fnhum.2013.00430 DOI: https://doi.org/10.3389/fnhum.2013.00430
McKeown MJ, Jung TP, Makeig S, Brown G, Kindermann SS, Lee T, Sejnowski TJ. Spatially independent activity patterns in functional MRI data during the Stroop color-naming task. Proc Natl Acad Sci USA 1998; 95: 803-810. http://dx.doi.org/10.1073/pnas.95.3.803 DOI: https://doi.org/10.1073/pnas.95.3.803
Boyd BA, McDonough SG, Bodfish JW. Evidence-based behavioral interventions for repetitive behaviors in autism. J Autism Dev Disord 2012; 42: 1236-1248. http://dx.doi.org/10.1007/s10803-011-1284-z DOI: https://doi.org/10.1007/s10803-011-1284-z
Biswal BB, Mennes M, Zuo X, Gohel S, Kelly C, Smith SM,
et al. Toward discovery science of human brain function. PNAS 2010; 107(Pt 10): 4734-4739. http://dx.doi.org/10.1073/pnas.0911855107 DOI: https://doi.org/10.1073/pnas.0911855107
Monk CS, Peltier SJ, Wiggins JL, Weng S, Carrasco M, Risi S, Lord C. Abnormalities of intrinsic functional connectivity in autism spectrum disorders. Neuroimage 2009; 47: 764-772. http://dx.doi.org/10.1016/j.neuroimage.2009.04.069 DOI: https://doi.org/10.1016/j.neuroimage.2009.04.069
Weng SJ, Wiggins JL, Peltier SJ, Carrasco M, Risi S, Lord C. Alterations of resting state functional connectivity in the default network in adolescents with autism spectrum disorders. Brain Res 2010; 1313: 202-214. http://dx.doi.org/10.1016/j.brainres.2009.11.057 DOI: https://doi.org/10.1016/j.brainres.2009.11.057
Stieltjes B, Kaufmann WE, van Zijl PC, Fredericksen K, Pearlson GD, Solaiyappan M et al. Diffusion tensor imaging and axonal tracking in the human brainstem. Neuroimage 2001; 14: 723-735. http://dx.doi.org/10.1006/nimg.2001.0861 DOI: https://doi.org/10.1006/nimg.2001.0861
Thomas C, Humphreys K, Jung K, Minshew N, Behrmann M. The anatomy of the callosal and visual association pathways in high-functioning autism: a DTI tractography study. Cortex 2011; 47(Pt 7): 863-873. http://dx.doi.org/10.1016/j.cortex.2010.07.006 DOI: https://doi.org/10.1016/j.cortex.2010.07.006
Thakkar KN, Polli FE, Joseph R, Tuch D, Hadjikhani N, Barton J, et al. Response monitoring, repetitive behavior and anterior cingulate abnormalities in autism spectrum disorders. Brain 2008; I3I: 2464-2478. http://dx.doi.org/10.1093/brain/awn099 DOI: https://doi.org/10.1093/brain/awn099
Zikopolous B, Barbas H. Changes in prefrontal axons may disrupt the network in autism. J Neurosci 2010; 30(Pt 44): 14595-14609. http://dx.doi.org/10.1523/JNEUROSCI.2257-10.2010 DOI: https://doi.org/10.1523/JNEUROSCI.2257-10.2010
Langen M, Leemans A, Johnston P, Ecker C, Daly E, Murphy CM, et al. Frontal striatal circuitry and inhibitory control in autism: Findings from diffusion tensor imaging tractography. Cortex 2012; 48: 183-193. http://dx.doi.org/10.1016/j.cortex.2011.05.018 DOI: https://doi.org/10.1016/j.cortex.2011.05.018
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