Behavioural and neural basis of anomalous motor learning in children with autism

被引:101
作者
Marko, Mollie K. [1 ]
Crocetti, Deana [2 ]
Hulst, Thomas [3 ]
Donchin, Opher [4 ]
Shadmehr, Reza [1 ]
Mostofsky, Stewart H. [2 ,5 ,6 ]
机构
[1] Johns Hopkins Sch Med, Lab Computat Motor Control, Dept Biomed Engn, Baltimore, MD 21205 USA
[2] Kennedy Krieger Inst, Ctr Neurodev & Imaging Res, Baltimore, MD USA
[3] Erasmus MC, Dept Neurosci, Rotterdam, Netherlands
[4] Ben Gurion Univ Negev, Motor Learning Lab, Dept Biomed Engn, Beer Sheva, Israel
[5] Johns Hopkins Univ, Sch Med, Dept Neurol, Baltimore, MD 21205 USA
[6] Johns Hopkins Univ, Sch Med, Dept Psychiat & Behav Sci, Baltimore, MD 21205 USA
关键词
error sensitivity; proprioception; motor learning; reaching; cerebellum; autism; INTRINSIC FUNCTIONAL CONNECTIVITY; SPECTRUM DISORDER; CEREBELLAR CONTRIBUTIONS; INTERNAL-MODELS; REACH ADAPTATION; YOUNG-CHILDREN; IMITATION; BRAIN; ERROR; REPRESENTATION;
D O I
10.1093/brain/awu394
中图分类号
R74 [神经病学与精神病学];
学科分类号
摘要
Autism spectrum disorder is a developmental disorder characterized by deficits in social and communication skills and repetitive and stereotyped interests and behaviours. Although not part of the diagnostic criteria, individuals with autism experience a host of motor impairments, potentially due to abnormalities in how they learn motor control throughout development. Here, we used behavioural techniques to quantify motor learning in autism spectrum disorder, and structural brain imaging to investigate the neural basis of that learning in the cerebellum. Twenty children with autism spectrum disorder and 20 typically developing control subjects, aged 8-12, made reaching movements while holding the handle of a robotic manipulandum. In random trials the reach was perturbed, resulting in errors that were sensed through vision and proprioception. The brain learned from these errors and altered the motor commands on the subsequent reach. We measured learning from error as a function of the sensory modality of that error, and found that children with autism spectrum disorder outperformed typically developing children when learning from errors that were sensed through proprioception, but underperformed typically developing children when learning from errors that were sensed through vision. Previous work had shown that this learning depends on the integrity of a region in the anterior cerebellum. Here we found that the anterior cerebellum, extending into lobule VI, and parts of lobule VIII were smaller than normal in children with autism spectrum disorder, with a volume that was predicted by the pattern of learning from visual and proprioceptive errors. We suggest that the abnormal patterns of motor learning in children with autism spectrum disorder, showing an increased sensitivity to proprioceptive error and a decreased sensitivity to visual error, may be associated with abnormalities in the cerebellum.
引用
收藏
页码:784 / 797
页数:14
相关论文
共 66 条
  • [1] Afferent areas in the cerebellum connected with the limbs.
    Adrian, ED
    [J]. BRAIN, 1943, 66 : 289 - 315
  • [2] Differential effects of developmental cerebellar abnormality on cognitive and motor functions in the cerebellum: An fMRI study of autism
    Allen, G
    Courchesne, E
    [J]. AMERICAN JOURNAL OF PSYCHIATRY, 2003, 160 (02) : 262 - 273
  • [3] A clinicopathological study of autism
    Bailey, A
    Luthert, P
    Dean, A
    Harding, B
    Janota, I
    Montgomery, M
    Rutter, M
    Lantos, P
    [J]. BRAIN, 1998, 121 : 889 - 905
  • [4] The organization of the human cerebellum estimated by intrinsic functional connectivity
    Buckner, Randy L.
    Krienen, Fenna M.
    Castellanos, Angela
    Diaz, Julio C.
    Yeo, B. T. Thomas
    [J]. JOURNAL OF NEUROPHYSIOLOGY, 2011, 106 (05) : 2322 - 2345
  • [5] The statistical determinants of adaptation rate in human reaching
    Burge, Johannes
    Ernst, Marc O.
    Banks, Martin S.
    [J]. JOURNAL OF VISION, 2008, 8 (04):
  • [6] Environmental Consistency Determines the Rate of Motor Adaptation
    Castro, Luis Nicolas Gonzalez
    Hadjiosif, Alkis M.
    Hemphill, Matthew A.
    Smith, Maurice A.
    [J]. CURRENT BIOLOGY, 2014, 24 (10) : 1050 - 1061
  • [7] Impairment of actions chains in autism and its possible role in intention understanding
    Cattaneo, Luigi
    Fabbri-Destro, Maddalena
    Boria, Sonia
    Pieraccini, Cinzia
    Monti, Annalisa
    Cossu, Giuseppe
    Rizzolatti, Giacomo
    [J]. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2007, 104 (45) : 17825 - 17830
  • [8] Reduced sensitivity to minimum-jerk biological motion in autism spectrum conditions
    Cook, Jennifer
    Saygin, Ayse Pinar
    Swain, Rachel
    Blakemore, Sarah-Jayne
    [J]. NEUROPSYCHOLOGIA, 2009, 47 (14) : 3275 - 3278
  • [9] Unusual brain growth patterns in early life in patients with autistic disorder - An MRI study
    Courchesne, E
    Karns, CM
    Davis, HR
    Ziccardi, R
    Carper, RA
    Tigue, ZD
    Chisum, HJ
    Moses, P
    Pierce, K
    Lord, C
    Lincoln, AJ
    Pizzo, S
    Schreibman, L
    Haas, RH
    Akshoomoff, NA
    Courchesne, RY
    [J]. NEUROLOGY, 2001, 57 (02) : 245 - 254
  • [10] Size of Error Affects Cerebellar Contributions to Motor Learning
    Criscimagna-Hemminger, Sarah E.
    Bastian, Amy J.
    Shadmehr, Reza
    [J]. JOURNAL OF NEUROPHYSIOLOGY, 2010, 103 (04) : 2275 - 2284