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PLOS ONE  2013 

Saccade Adaptation Abnormalities Implicate Dysfunction of Cerebellar-Dependent Learning Mechanisms in Autism Spectrum Disorders (ASD)

DOI: 10.1371/journal.pone.0063709

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Abstract:

The cerebellar vermis (lobules VI-VII) has been implicated in both postmortem and neuroimaging studies of autism spectrum disorders (ASD). This region maintains the consistent accuracy of saccadic eye movements and plays an especially important role in correcting systematic errors in saccade amplitudes such as those induced by adaptation paradigms. Saccade adaptation paradigms have not yet been used to study ASD. Fifty-six individuals with ASD and 53 age-matched healthy controls performed an intrasaccadic target displacement task known to elicit saccadic adaptation reflected in an amplitude reduction. The rate of amplitude reduction and the variability of saccade amplitude across 180 adaptation trials were examined. Individuals with ASD adapted slower than healthy controls, and demonstrated more variability of their saccade amplitudes across trials prior to, during and after adaptation. Thirty percent of individuals with ASD did not significantly adapt, whereas only 6% of healthy controls failed to adapt. Adaptation rate and amplitude variability impairments were related to performance on a traditional neuropsychological test of manual motor control. The profile of impaired adaptation and reduced consistency of saccade accuracy indicates reduced neural plasticity within learning circuits of the oculomotor vermis that impedes the fine-tuning of motor behavior in ASD. These data provide functional evidence of abnormality in the cerebellar vermis that converges with previous reports of cellular and gross anatomic dysmorphology of this brain region in ASD.

References

[1]  American Psychological Association (2000) Diagnostic and statistical manual of mental disorders-4th edition Text Revision. Washington D.C.: American Psychiatric Press.
[2]  Developmental Disabilities Monitoring Network (2012) Prevalence of autism spectrum disorders–Autism and Developmental Disabilities Monitoring Network, 14 sites, United States, 2008. MMWR Surveill Summ 61: 1–19.
[3]  Fatemi SH, Aldinger KA, Ashwood P, Bauman ML, Blaha CD, et al. (2012) Consensus Paper: Pathological Role of the Cerebellum in Autism. Cerebellum 11: 777–807.
[4]  Abrahams BS, Geschwind DH (2010) Connecting genes to brain in the autism spectrum disorders. Arch Neurol 67: 395–399.
[5]  Ritvo ER, Freeman BJ, Scheibel AB, Duong T, Robinson H, et al. (1986) Lower Purkinje cell counts in the cerebella of four autistic subjects: initial findings of the UCLA-NSAC Autopsy Research Report. Am J Psychiatry 143: 862–866.
[6]  Bailey A, Luthert P, Dean A, Harding B, Janota I, et al. (1998) A clinicopathological study of autism. Brain 121 (Pt 5): 889–905.
[7]  Bauman M, Kemper TL (1985) Histoanatomic observations of the brain in early infantile autism. Neurology 35: 866–874.
[8]  Fatemi SH, Halt AR, Realmuto G, Earle J, Kist DA, et al. (2002) Purkinje cell size is reduced in cerebellum of patients with autism. Cell Mol Neurobiol 22: 171–175.
[9]  Whitney ER, Kemper TL, Bauman ML, Rosene DL, Blatt GJ (2008) Cerebellar Purkinje cells are reduced in a subpopulation of autistic brains: a stereological experiment using calbindin-D28k. Cerebellum 7: 406–416.
[10]  Bauman ML, Kemper TL (2005) Neuroanatomic observations of the brain in autism: a review and future directions. Int J Dev Neurosci 23: 183–187.
[11]  Akshoomoff N, Lord C, Lincoln AJ, Courchesne RY, Carper RA, et al. (2004) Outcome classification of preschool children with autism spectrum disorders using MRI brain measures. Journal of the American Academy of Child and Adolescent Psychiatry 43: 349–357.
[12]  Haas RH, Townsend J, Courchesne E, Lincoln AJ, Schreibman L, et al. (1996) Neurologic abnormalities in infantile autism. J Child Neurol 11: 84–92.
[13]  Kaufmann WE, Cooper KL, Mostofsky SH, Capone GT, Kates WR, et al. (2003) Specificity of cerebellar vermian abnormalities in autism: a quantitative magnetic resonance imaging study. J Child Neurol 18: 463–470.
[14]  Mitchell SR, Reiss AL, Tatusko DH, Ikuta I, Kazmerski DB, et al. (2009) Neuroanatomic alterations and social and communication deficits in monozygotic twins discordant for autism disorder. Am J Psychiatry 166: 917–925.
[15]  Scott JA, Schumann CM, Goodlin-Jones BL, Amaral DG (2009) A comprehensive volumetric analysis of the cerebellum in children and adolescents with autism spectrum disorder. Autism Res 2: 246–257.
[16]  Webb SJ, Sparks BF, Friedman SD, Shaw DW, Giedd J, et al. (2009) Cerebellar vermal volumes and behavioral correlates in children with autism spectrum disorder. Psychiatry Res 172: 61–67.
[17]  Courchesne E, Saitoh O, Yeung-Courchesne R, Press GA, Lincoln AJ, et al. (1994) Abnormality of cerebellar vermian lobules VI and VII in patients with infantile autism: identification of hypoplastic and hyperplastic subgroups with MR imaging. AJR Am J Roentgenol 162: 123–130.
[18]  Hardan AY, Minshew NJ, Harenski K, Keshavan MS (2001) Posterior fossa magnetic resonance imaging in autism. J Am Acad Child Adolesc Psychiatry 40: 666–672.
[19]  Courchesne E, Yeung-Courchesne R, Press GA, Hesselink JR, Jernigan TL (1988) Hypoplasia of cerebellar vermal lobules VI and VII in autism. N Engl J Med 318: 1349–1354.
[20]  Courchesne E, Karns CM, Davis HR, Ziccardi R, Carper RA, et al. (2001) Unusual brain growth patterns in early life in patients with autistic disorder: an MRI study. Neurology 57: 245–254.
[21]  Holttum JR, Minshew NJ, Sanders RS, Phillips NE (1992) Magnetic resonance imaging of the posterior fossa in autism. Biol Psychiatry 32: 1091–1101.
[22]  Piven J, Saliba K, Bailey J, Arndt S (1997) An MRI study of autism: the cerebellum revisited. Neurology 49: 546–551.
[23]  Izawa J, Pekny SE, Marko MK, Haswell CC, Shadmehr R, et al. (2012) Motor learning relies on integrated sensory inputs in ADHD, but over-selectively on proprioception in autism spectrum conditions. Autism research : official journal of the International Society for Autism Research 5: 124–136.
[24]  Asperger H (1991/1944) Autism and Asperger Syndrome. New York: Cambridge University Press. 37–92.
[25]  Kanner L (1943) Autistic disturbances of affective contact. Nervous Child 2: 217–250.
[26]  MacNeil LK, Mostofsky SH (2012) Specificity of dyspraxia in children with autism. Neuropsychology 26: 165–171.
[27]  Provost B, Heimerl S, Lopez BR (2007) Levels of gross and fine motor development in young children with autism spectrum disorder. Phys Occup Ther Pediatr 27: 21–36.
[28]  Mosconi MW, Takarae Y, Sweeney JA (2011) Motor impairments and dyspraxia in autism. In: DG. Amaral GD, & DH Geschwind, editor. Autism Spectrum Disorders. New York, NY: Oxford University Press, Inc.
[29]  Bhat AN, Galloway JC, Landa RJ (2012) Relation between early motor delay and later communication delay in infants at risk for autism. Infant Behav Dev 35: 838–846.
[30]  Bryson SE, Zwaigenbaum L, Brian J, Roberts W, Szatmari P, et al. (2007) A prospective case series of high-risk infants who developed autism. J Autism Dev Disord 37: 12–24.
[31]  Ozonoff S, Young GS, Goldring S, Greiss-Hess L, Herrera AM, et al. (2008) Gross motor development, movement abnormalities, and early identification of autism. J Autism Dev Disord 38: 644–656.
[32]  Sutera S, Pandey J, Esser EL, Rosenthal MA, Wilson LB, et al. (2007) Predictors of optimal outcome in toddlers diagnosed with autism spectrum disorders. J Autism Dev Disord 37: 98–107.
[33]  Bhat AN, Landa RJ, Galloway JC (2011) Current perspectives on motor functioning in infants, children, and adults with autism spectrum disorders. Phys Ther 91: 1116–1129.
[34]  Dewey D, Cantell M, Crawford SG (2007) Motor and gestural performance in children with autism spectrum disorders, developmental coordination disorder, and/or attention deficit hyperactivity disorder. J Int Neuropsychol Soc 13: 246–256.
[35]  Green D, Baird G, Barnett AL, Henderson L, Huber J, et al. (2002) The severity and nature of motor impairment in Asperger's syndrome: a comparison with specific developmental disorder of motor function. J Child Psychol Psychiatry 43: 655–668.
[36]  Luna B, Doll SK, Hegedus SJ, Minshew NJ, Sweeney JA (2007) Maturation of executive function in autism. Biol Psychiatry 61: 474–481.
[37]  Mosconi MW, Kay M, D'Cruz AM, Guter S, Kapur K, et al. (2010) Neurobehavioral abnormalities in first-degree relatives of individuals with autism. Arch Gen Psychiatry 67: 830–840.
[38]  Nowinski CV, Minshew NJ, Luna B, Takarae Y, Sweeney JA (2005) Oculomotor studies of cerebellar function in autism. Psychiatry Res 137: 11–19.
[39]  Takarae Y, Minshew NJ, Luna B, Sweeney JA (2004) Oculomotor abnormalities parallel cerebellar histopathology in autism. J Neurol Neurosurg Psychiatry 75: 1359–1361.
[40]  Takarae Y, Minshew NJ, Luna B, Krisky CM, Sweeney JA (2004) Pursuit eye movement deficits in autism. Brain 127: 2584–2594.
[41]  Minshew NJ, Luna B, Sweeney JA (1999) Oculomotor evidence for neocortical systems but not cerebellar dysfunction in autism. Neurology 52: 917–922.
[42]  Rosenhall U, Johansson E, Gillberg C (1988) Oculomotor findings in autistic children. J Laryngol Otol 102: 435–439.
[43]  Allen G, Courchesne E (2003) Differential effects of developmental cerebellar abnormality on cognitive and motor functions in the cerebellum: an fMRI study of autism. American Journal of Psychiatry 160: 262–273.
[44]  Muller RA, Kleinhans N, Kemmotsu N, Pierce K, Courchesne E (2003) Abnormal variability and distribution of functional maps in autism: an FMRI study of visuomotor learning. Am J Psychiatry 160: 1847–1862.
[45]  Mostofsky SH, Powell SK, Simmonds DJ, Goldberg MC, Caffo B, et al. (2009) Decreased connectivity and cerebellar activity in autism during motor task performance. Brain 132: 2413–2425.
[46]  Takarae Y, Minshew NJ, Luna B, Sweeney JA (2007) Atypical involvement of frontostriatal systems during sensorimotor control in autism. Psychiatry Res 156: 117–127.
[47]  MacAskill MR, Anderson TJ, Jones RD (2002) Adaptive modification of saccade amplitude in Parkinson's disease. Brain 125: 1570–1582.
[48]  Scudder CA, McGee DM (2003) Adaptive modification of saccade size produces correlated changes in the discharges of fastigial nucleus neurons. J Neurophysiol 90: 1011–1026.
[49]  Deubel H (1995) Separate adaptive mechanisms for the control of reactive and volitional saccadic eye movements. Vision research 35: 3529–3540.
[50]  Diedrichsen J, Verstynen T, Lehman SL, Ivry RB (2005) Cerebellar involvement in anticipating the consequences of self-produced actions during bimanual movements. J Neurophysiol 93: 801–812.
[51]  Izawa J, Criscimagna-Hemminger SE, Shadmehr R (2012) Cerebellar contributions to reach adaptation and learning sensory consequences of action. J Neurosci 32: 4230–4239.
[52]  Mostofsky SH, Bunoski R, Morton SM, Goldberg MC, Bastian AJ (2004) Children with autism adapt normally during a catching task requiring the cerebellum. Neurocase 10: 60–64.
[53]  Gidley Larson JC, Bastian AJ, Donchin O, Shadmehr R, Mostofsky SH (2008) Acquisition of internal models of motor tasks in children with autism. Brain 131: 2894–2903.
[54]  Desmurget M, Pelisson D, Grethe JS, Alexander GE, Urquizar C, et al. (2000) Functional adaptation of reactive saccades in humans: a PET study. Exp Brain Res 132: 243–259.
[55]  Xu-Wilson M, Chen-Harris H, Zee DS, Shadmehr R (2009) Cerebellar contributions to adaptive control of saccades in humans. J Neurosci 29: 12930–12939.
[56]  Golla H, Tziridis K, Haarmeier T, Catz N, Barash S, et al. (2008) Reduced saccadic resilience and impaired saccadic adaptation due to cerebellar disease. The European journal of neuroscience 27: 132–144.
[57]  Barash S, Melikyan A, Sivakov A, Zhang M, Glickstein M, et al. (1999) Saccadic dysmetria and adaptation after lesions of the cerebellar cortex. The Journal of Neuroscience 19: 10931–10939.
[58]  Ignashchenkova A, Dash S, Dicke PW, Haarmeier T, Glickstein M, et al. (2009) Normal spatial attention but impaired saccades and visual motion perception after lesions of the monkey cerebellum. J Neurophysiol 102: 3156–3168.
[59]  Takagi M, Zee DS, Tamargo RJ (1998) Effects of lesions of the oculomotor vermis on eye movements in primate: saccades. Journal of neurophysiology 80: 1911–1931.
[60]  McLaughlin S (1967) Parametric adjustment in saccadic eye movements. Perceptual Psychophysyiology 2: 359–362.
[61]  Wechsler D (1999) Wechsler Abbreviated Scale of Intelligence. San Antonio, TX.
[62]  Lord C, Rutter M, Le Couteur A (1994) Autism Diagnostic Interview-Revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. J Autism Dev Disord 24: 659–685.
[63]  Lord C, Risi S, Lambrecht L, Cook EH Jr, Leventhal BL, et al. (2000) The autism diagnostic observation schedule-generic: a standard measure of social and communication deficits associated with the spectrum of autism. J Autism Dev Disord 30: 205–223.
[64]  Reilly JL, Lencer R, Bishop JR, Keedy S, Sweeney JA (2008) Pharmacological treatment effects on eye movement control. Brain Cogn 68: 415–435.
[65]  Gibbons RD, Hedeker D, DuToit S (2010) Advances in analysis of longitudinal data. Annu Rev Clin Psychol 6: 79–107.
[66]  Alahyane N, Pelisson D (2005) Retention of saccadic adaptation in humans. Annals of the New York Academy of Sciences 1039: 558–562.
[67]  Straube A, Fuchs AF, Usher S, Robinson FR (1997) Characteristics of saccadic gain adaptation in rhesus macaques. Journal of neurophysiology 77: 874–895.
[68]  Straube A, Deubel H, Ditterich J, Eggert T (2001) Cerebellar lesions impair rapid saccade amplitude adaptation. Neurology 57: 2105–2108.
[69]  Salman MS, Sharpe JA, Eizenman M, Lillakas L, To T, et al. (2006) Saccadic adaptation in children. J Child Neurol 21: 1025–1031.
[70]  Desmurget M, Pelisson D, Urquizar C, Prablanc C, Alexander GE, et al. (1998) Functional anatomy of saccadic adaptation in humans. Nat Neurosci 1: 524–528.
[71]  Greco CM, Navarro CS, Hunsaker MR, Maezawa I, Shuler JF, et al. (2011) Neuropathologic features in the hippocampus and cerebellum of three older men with fragile X syndrome. Mol Autism 2: 2.
[72]  Havermann K, Lappe M (2010) The influence of the consistency of postsaccadic visual errors on saccadic adaptation. J Neurophysiol 103: 3302–3310.
[73]  Thier P, Dicke PW, Haas R, Barash S (2000) Encoding of movement time by populations of cerebellar Purkinje cells. Nature 405: 72–76.
[74]  Scudder CA, Batourina EY, Tunder GS (1998) Comparison of two methods of producing adaptation of saccade size and implications for the site of plasticity. J Neurophysiol 79: 704–715.
[75]  Imamizu H, Miyauchi S, Tamada T, Sasaki Y, Takino R, et al. (2000) Human cerebellar activity reflecting an acquired internal model of a new tool. Nature 403: 192–195.
[76]  Tseng YW, Diedrichsen J, Krakauer JW, Shadmehr R, Bastian AJ (2007) Sensory prediction errors drive cerebellum-dependent adaptation of reaching. J Neurophysiol 98: 54–62.
[77]  Albus J (1971) A theory of cerebellar function. Math BioScience 10: 25–61.
[78]  Ito M (1982) Cerebellar control of the vestibulo-ocular reflex–around the flocculus hypothesis. Annu Rev Neurosci 5: 275–296.
[79]  Marr D (1969) A theory of cerebellar cortex. J Physiol 202: 437–470.
[80]  Ito M, Karachot L (1989) Long-term desensitization of quisqualate-specific glutamate receptors in Purkinje cells investigated with wedge recording from rat cerebellar slices. Neurosci Res 7: 168–171.
[81]  Ohtsuka K, Noda H (1995) Discharge properties of Purkinje cells in the oculomotor vermis during visually guided saccades in the macaque monkey. J Neurophysiol 74: 1828–1840.
[82]  Kojima Y, Soetedjo R, Fuchs AF (2011) Effect of inactivation and disinhibition of the oculomotor vermis on saccade adaptation. Brain Res 1401: 30–39.
[83]  Arin DM, Bauman ML, Kemper TL (1991) The distribution of Purkinje cell loss in the cerebellum in autism. Neurology 41: 307.
[84]  Lee M, Martin-Ruiz C, Graham A, Court J, Jaros E, et al. (2002) Nicotinic receptor abnormalities in the cerebellar cortex in autism. Brain 125: 1483–1495.
[85]  Yip J, Soghomonian JJ, Blatt GJ (2008) Increased GAD67 mRNA expression in cerebellar interneurons in autism: implications for Purkinje cell dysfunction. J Neurosci Res 86: 525–530.
[86]  Yip J, Soghomonian JJ, Blatt GJ (2007) Decreased GAD67 mRNA levels in cerebellar Purkinje cells in autism: pathophysiological implications. Acta Neuropathol 113: 559–568.
[87]  Soetedjo R, Fuchs AF, Kojima Y (2009) Subthreshold activation of the superior colliculus drives saccade motor learning. J Neurosci 29: 15213–15222.
[88]  Quessy S, Quinet J, Freedman EG (2010) The locus of motor activity in the superior colliculus of the rhesus monkey is unaltered during saccadic adaptation. J Neurosci 30: 14235–14244.
[89]  Aizawa H, Wurtz RH (1998) Reversible inactivation of monkey superior colliculus. I. Curvature of saccadic trajectory. Journal of neurophysiology 79: 2082–2096.
[90]  Gaymard B, Rivaud-Pechoux S, Yelnik J, Pidoux B, Ploner CJ (2001) Involvement of the cerebellar thalamus in human saccade adaptation. Eur J Neurosci 14: 554–560.
[91]  Stanfield AC, McIntosh AM, Spencer MD, Philip R, Gaur S, et al. (2008) Towards a neuroanatomy of autism: a systematic review and meta-analysis of structural magnetic resonance imaging studies. Eur Psychiatry 23: 289–299.

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