Behavioural aspects of cerebellar function in adults with Asperger syndrome
Original Article Scientific Papers
Received: 16 May 2005 Accepted: 23 August 2005 DOI:
Cite this article as: Gowen, E. & Miall, R.C. Cerebellum (2005) 4: 279. doi:10.1080/14734220500355332 Abstract
Aside from social deficits, Asperger and autistic individuals also exhibit motor control abnormalities such as impaired gait, balance, manual dexterity and grip. One brain area that has consistently been reported on autopsy and imaging studies to be abnormal in such individuals is the cerebellum. As the cerebellum controls sensorimotor coordination and lesions here typically cause hypotonia, dysmetria and dyscoordination, we performed a series of quantitative tests aimed at investigating cerebellar function in Asperger individuals. Tests examining visually guided movement (rapid pointing), speeded complex movement (finger tapping, rapid hand turning), muscle tone (catching dropped weight), prediction, coordination and timing (balance, grip force and interval timing) were conducted on 12 Asperger subjects and 12 age and IQ matched controls. In comparison to control subjects, Asperger subject’s demonstrated: (i) decreased pointing accuracy and rate, (ii) increased postural instability, and (iii) decreased timing accuracy. IQ was found to co-vary with some parameters of each of these tasks and no further impairments were found on the remaining tests. We suggest that these specific deficits reflect impairment in the ability to integrate sensory input with appropriate motor commands and are consistent with cerebellar dysfunction in Asperger syndrome.
Key words Cerebellum Asperger syndrome balance timing References
Hill EL, Frith U. Understanding autism: Insights from mind and brain. Philos Trans R Soc Lond B Biol Sci. 2003;358:281–9.
Frith U. Emanuel Miller lecture: Confusions and controversies about Asperger syndrome. J Child Psychol.Psychiatry. 2004;45:672–86.
Hallett M, Lebiedowska MK, Thomas SL, Stanhope SJ, Denckla MB, Rumsey J. Locomotion of autistic adults. Arch Neurol. 1993;50:1304–08.
Weimer AK, Schatz AM, Lincoln A, Ballantyne AO, Trauner DA. ‘Motor’ impairment in Asperger syndrome: evidence for a deficit in proprioception. J Dev Behav Pediatr. 2001;22:92–101.
Rinehart NJ, Bradshaw JL, Brereton AV, Tonge BJ. Movement preparation in high-functioning autism and Asperger disorder: A serial choice reaction time task involving motor reprogramming. J Autism Dev Disord. 2001;31:79–88.
Hardan AY, Kilpatrick M, Keshavan MS, Minshew NJ. Motor performance and anatomic magnetic resonance imaging (MRI) of the basal ganglia in autism. J Child Neurol. 2003;18:317–24.
Ghaziuddin M, Butler E, Tsai L, Ghaziuddin N. Is clumsiness a marker for Asperger syndrome? J Intellect Disabil Res. 1994;3(Pt 5): 519–27.
Gillberg C. Asperger syndrome in 23 Swedish children. Dev Med Child Neurol. 1989;31:520–31.
Green D, Baird G, Barnett AL, Henderson L, Huber J, Henderson SE. The severity and nature of motor impairment in Asperger’s syndrome: A comparison with specific developmental disorder of motor function. J Child Psychol Psychiatry. 2002;43:655–68.
Miyahara M, Tsujii M, Hori M, Nakanishi K, Kageyama H, Sugiyama T. Brief report: Motor incoordination in children with Asperger syndrome and learning disabilities. J Autism Dev Disord. 1997;27:595–603.
Ito M. Historical review of the significance of the cerebellum and the role of Purkinje cells in motor learning. Ann NY Acad Sci. 2002;978:273–88.
Miall RC, Reckess GZ, Imamizu H. The cerebellum coordinates eye and hand tracking movements. Nat Neurosci. 2001;4:638–44.
Thach WT, Goodkin HP, Keating JG. The cerebellum and the adaptive coordination of movement. Ann Rev Neurosci. 1992;15:403–42.
Van Donkelaar P, Lee RG. Interactions between the eye and hand motor systems: Disruptions due to cerebellar dysfunction. J Neurophysiol. 1994;72:1674–85.
Ivry R, Keele SW, Diener HC. Dissociation of the lateral and medial cerebellum in movement timing and movement execution. Exp Brain Res. 1988;73:167–80.
Ivry R, Keele SW. Timing functions of the cerebellum. J Cogn Neurosci. 1989;1:136–52.
Allen G, Muller RA, Courchesne E. Cerebellar function in autism: Functional magnetic resonance image activation during a simple motor task. Biol Psychiatry. 2004;56:269–78.
Bailey A, Luthert P, Dean A, et al. A clinicopathological study of autism. Brain. 1998;121(Pt 5): 889–905.
Courchesne E. Brainstem, cerebellar and limbic neuroanatomical abnormalities in autism. Curr Opin Neurobiol. 1997;7:269–78.
Courchesne E, Townsend J, Saitoh O. The brain in infantile autism: Posterior fossa structures are abnormal. Neurology. 1994;44:214–23.
Kemper TL, Bauman M. Neuropathology of infantile autism. J Neuropathol Exp Neurol. 1998;57:645–52.
Abell F, Krams M, Ashburner J, et al. The neuroanatomy of autism: A voxel-based whole brain analysis of structural scans. Neuroreport. 1999;10:1647–51.
Murakami JW, Courchesne E, Press GA, Yeung-Courchesne R, Hesselink JR. Reduced cerebellar hemisphere size and its relationship to vermal hypoplasia in autism. Arch Neurol. 1989;46:689–94.
Wassmer E, Davies P, Whitehouse WP, Green SH. Clinical spectrum associated with cerebellar hypoplasia. Pediatr Neurol. 2003;28:347–51.
Allen G, Buxton RB, Wong EC, Courchesne E. Attentional activation of the cerebellum independent of motor involvement. Science. 1997;275:1940–3.
Schmahmann JD, Sherman JC. The cerebellar cognitive affective syndrome. Brain. 1998;121(Pt 4): 561–79.
Courchesne E, Townsend J, Akshoomoff NA, et al. Impairment in shifting attention in autistic and cerebellar patients. Behav Neurosci. 1994;108:848–65.
Singer-Harris NS, Courchesne E, Townsend J, Carper RA, Lord C. Neuroanatomic contributions to slowed orienting of attention in children with autism. Brain Res Cogn Brain Res. 1999;8:61–71.
Dow RS, Moruzzi G, editors. The physiology and pathology of the cerebellum. Minneapolis: University of Minnesota Press, 1958.
Henderson SE, Sugden D, editors. The movement assessment battery for children. London: The Psychological Corporation, 1992.
Bruininks RH, editor. The Bruininks-Oseretsky test of motor proficiency. Circle Pines, MN: American Guidance Service, 1978.
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. J Autism Dev Disord. 2001;31:5–17.
Szatmari P, Tuff L, Finlayson AJ, Bartolucci G. Asperger’s syndrome and autism: Neurocognitive aspects. J Am Acad Child Adoles Psychiatry. 1990;29:130–6.
Miall RC, Christensen LO. The effect of rTMS over the cerebellum in normal human volunteers on peg-board movement performance. Neurosci.Lett. 2004;371:185–9.
Kawato M, Kuroda T, Imamizu H, Nakano E, Miyauchi S, Yoshioka T. Internal forward models in the cerebellum: fMRI study on grip force and load force coupling. Prog Brain Res. 2003;142:171–88.
Muller F, Dichgans J. Dyscoordination of pinch and lift forces during grasp in patients with cerebellar lesions. Exp Brain Res. 1994;101:485–92.
Schmitz C, Martineau J, Barthelemy C, Assaiante C. Motor control and children with autism: deficit of anticipatory function? Neurosci Lett. 2003;348:17–20.
Lacquaniti F, Maioli C. Adaptation to suppression of visual information during catching. J Neurosci. 1989;9:149–59.
Lang CE, Bastian AJ. Cerebellar subjects show impaired adaptation of anticipatory EMG during catching. J Neurophysiol. 1999;82:2108–19.
Diener H, Dichgans J, Guschlbauer B, Bacher M, Langenbach P. Disturbances of motor preparation in basal ganglia and cerebellar disorders. Prog Brain Res. 1989;80:481–8.
Ouchi Y, Okada H, Yoshikawa E, Nobezawa S, Futatsubashi M. Brain activation during maintenance of standing postures in humans. Brain. 1999;122(Pt 2): 329–38.
Baloh RW, Jacobson KM, Beykirch K, Honrubia V. Static and dynamic posturography in patients with vestibular and cerebellar lesions. Arch Neurol. 1998;55:649–54.
Ho BC, Mola C, Andreasen NC. Cerebellar dysfunction in neuroleptic naive schizophrenia patients: Clinical, cognitive, and neuroanatomic correlates of cerebellar neurologic signs. Biol Psychiatry. 2004;55:1146–53.
Marvel CL, Schwartz BL, Rosse RB. A quantitative measure of postural sway deficits in schizophrenia. Schizophr Res. 2004;68:363–72.
Goldberg MC, Landa R, Lasker A, Cooper L, Zee DS. Evidence of normal cerebellar control of the vestibulo-ocular reflex (VOR) in children with high-functioning autism. J Autism Dev Disord. 2000;30:519–24.
Minshew NJ, Luna B, Sweeney JA. Oculomotor evidence for neocortical systems but not cerebellar dysfunction in autism. Neurology. 1999;52:917–22.
Takarae Y, Minshew NJ, Luna B, Sweeney JA. Oculomotor abnormalities parallel cerebellar histopathology in autism. J Neurol Neurosurg Psychiatry. 2004;75:1359–61.
Jancke L, Loose R, Lutz K, Specht K, Shah NJ. Cortical activations during paced finger-tapping applying visual and auditory pacing stimuli. Brain Res Cogn Brain Res. 2000;10:51–66.
Rao SM, Harrington DL, Haaland KY, Bobholz JA, Cox RW, Binder JR. Distributed neural systems underlying the timing of movements. J Neurosci. 1997;17:5528–35.
Sears LL. Finn PR, Steinmetz JE. Abnormal classical eyeblink conditioning in autism. J Autism Dev Disord. 1994;24:737–51.
Ivry RB, Spencer RM. The neural representation of time. Curr Opin Neurobiol. 2004;14:225–32.
Lewis PA, Miall RC. Distinct systems for automatic and cognitively controlled time measurement: Evidence from neuroimaging. Curr Opin Neurobiol. 2003;13:250–5.
Castelli F, Frith C, Happe F, Frith U. Autism, Asperger syndrome and brain mechanisms for the attribution of mental states to animated shapes. Brain. 2002;125:1839–49.
Theoret H, Haque J, Pascual-Leone A. Increased variability of paced finger tapping accuracy following repetitive magnetic stimulation of the cerebellum in humans. Neurosci Lett. 2001;306:29–32.
Morton J, Frith U. Causal modelling: A structural approach to developmental psychopathology. In: Cichetti D, et al., editor. Developmental psychopathology: Vol. 1. Theory and methods. New York: Wiley. 1995; pp 357–90.