Contribution of olivofloccular circuitry developmental defects to atypical gaze in autism

Brain Research

Volumn 1512, Issue , 2013, Pages 106-122

  Wegiel, Jerzy ^a   Kuchna, Izabela ^a   Nowicki, Krzysztof ^a   Imaki, Humi ^a   Wegiel, Jarek ^a   Ma, Yong Shuang ^a   Azmitia, Efrain C ^b   Banerjee, Probal ^c   Flory, Michael ^a   Cohen, Ira L ^a   London, Eric ^a   Ted Brown, W ^a   Komich Hare, Carolyn ^d   Wisniewski, Thomas ^e  

^a NEW YORK STATE INSTITUTE FOR BASIC RESEARCH IN DEVELOPMENTAL DISABILITIES   (United States)

^b NEW YORK UNIVERSITY   (United States)

^c CITY UNIVERSITY OF NEW YORK   (United States)

^d Autism Tissue Program   (United States)

^e NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Atypical gaze; Autism; Cerebellum; Dysplasia; Flocculus

Indexed keywords

ADOLESCENT; ADULT; ARTICLE; AUTISM; BASKET CELL; BERGMANN GLIA LAYER; BRAIN CELL; BRAIN DISEASE; CEREBELLUM; CEREBELLUM FLOCCULUS; CHILD; CLINICAL ARTICLE; EYE MOVEMENT DISORDER; FLOCCULAR DYSPLASIA; GAZE; GLIA; GRANULE CELL; HUMAN; HUMAN TISSUE; PRESCHOOL CHILD; PRIORITY JOURNAL; PURKINJE CELL; STELLATE CELL; UNIPOLAR BRUSH CELL;

ADOLESCENT; ADULT; AGED; AUTISTIC DISORDER; CEREBELLUM; CHILD; CHILD, PRESCHOOL; DEVELOPMENTAL DISABILITIES; DIAGNOSIS, COMPUTER-ASSISTED; FEMALE; HUMANS; MALE; MIDDLE AGED; NERVE TISSUE PROTEINS; NEURAL PATHWAYS; OCULAR MOTILITY DISORDERS; OLIVARY NUCLEUS; POSTMORTEM CHANGES; PURKINJE CELLS; PURSUIT, SMOOTH; YOUNG ADULT;

EID: 84879839725     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2013.03.037     Document Type: Article

References (92)

1. American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders-IV 2000
2. E.C. Azmitia, J.S. Singh, and P.M. Whitaker-Azmitia Increased serotonin axons (immunoreactive to 5HT transporter) in postmortem brains from young autism donors Neuropharmacology 60 2011 1347 1354
3. A. Bailey, P. Luthert, A. Dean, B. Harding, and I. Janota A clinicopathological study of autism Brain 121 1998 889 905
4. S. Baron-Cohen Mindblindness: An Essay on Autism and Theory of Mind 1995 MIT Press Cambridge, MA
5. S. Baron-Cohen, R. Campbell, A. Karmiloff-Smith, J. Grant, and J. Walker Are children with autism blind to mentalistic significance of the eyes? Br. J. Dev. Psychol. 13 1999 379 398
6. S. Baron-Cohen, S. Wheelwright, and J. Hill The "reading the mind in the eyes" test revised version: a study with normal adults, and adults with Asperger syndrome or high-functioning autism J. Child Psychol. Psychiatry 42 2001 241 252
7. E. Bastianelli Distribution of calcium-binding proteins in the cerebellum Cerebellum 2 2003 242 262
8. M.L. Bauman, and T.L. Kemper Observations of the Purkinje cells in the cerebellar vermis in autism J. Neuropathol. Exp. Neurol. 55 1996 613
9. T. Belton, and R.A. McCrea Contribution of the cerebellar flocculus to gaze control during active head movements J. Neurophysiol. 81 1999 3105 3109
10. T. Belton, and R.A. McCrea Role of the cerebellar flocculus region in the coordination of eye and head movements during gaze pursuit J. Neurophysiol. 84 2000 1614 1626
11. F. Benedetti, P.G. Montarolo, and S. Rabacchi Inferior olive lesion induces long-lasting functional modification in the Purkinje cells Exp. Brain Res. 55 1984 368 371
12. G.A. Bishop, C.W. Kerr, Y.F. Chen, and J.S. King The serotoninergic system in the cerebellum: origin, ultrastructural relationships, and physiological effects P. Trouillas, K. Fuxe, Serotonin, the Cerebellum, and Ataxia 1993 Raven New York 91 112
13. C. Chen, M. Kano, A. Abeliovich, L. Chen, S. Bao, J.J. Kim, K. Hashimoto, R.F. Thompson, and S. Tonegawa Impaired motor coordination correlates with persistent multiple climbing fiber innervation in PKC mutant mice Cell 83 1995 1233 1242
14. B. Cohen, P. John, S.B. Yakushin, J. Buettner-Ennever, and T. Raphan The nodulus and uvula: source of cerebellar control of spatial orientation of the angular vestibulo-ocular reflex Ann. N.Y. Acad. Sci. 978 2002 28 45
15. D. Cohen, and Y. Yarom Patches of synchronized activity in the cerebellar cortex evoked by mossy-fiber stimulation: questioning the role of parallel fibers Proc. Natl. Acad. Sci. USA 95 1998 15032 15036
16. J.D. Corrales, G.L. Rocco, S. Blaess, Q. Guo, and A.L. Joyner Spatial pattern of sonic hedgehog signaling through Gli genes during cerebellum development Development 131 2004 5581 5590
17. J.D. Corrales, S. Blaess, E.M. Mahoney, and A.L. Joyner The level of sonic hedgehog signaling regulates the complexity of cerebellar foliation Development 133 2006 1811 1821
18. E. Courchesne, G. Press, J. Murakami, D. Berthoty, and M. Grafe The cerebellum in sagittal plane-anatomic-MR correlation: 1. The vermis A. J. Roentgenol. 153 1989 829 835
19. E. Courchesne, C.M. Karns, H.R. Davids, R Ziccardi, and R.A. Carper Unusual brain growth patterns in early life in patients in the autistic disorder Neurology 57 2001 245 254
20. G. Dawson, A. Meltzoff, J. Osterling, and J. Rinaldi Neuropsychological correlates of early symptoms of autism Child Dev. 69 1998 1276 1285
21. G. Dawson, S. Webb, G.D. Schellenberg, S. Dager, S. Friedman, E. Aylward, and T. Richards Defining the broader phenotype of autism: genetic, brain, and behavioral perspectives Dev. Psychopathol. 14 2002 581 611
22. S. Dieudonne, and A. Dumoulin Serotonin-driven long-range inhibitory connections in the cerebellar cortex Neuroscience 20 2000 1837 1848
23. M.R. Diño, F.H. Willard, and E. Mugnaini Distribution of unipolar brush cells and other calretinin immunoreactive components in the mammalian cerebellar cortex J. Neurocytol. 28 1999 99 123
24. M.R. Diño, R.J. Schuerger, J.B. Liu, N.T. Slater, and E. Mugnaini Unipolar brush cell: a potential feed forward excitatory interneuron of the cerebellum Neuroscience 98 2000 625 636
25. S. Du Lac, J.L. Raymond, TJ Sejnowski, and SG. Lisberger Learning and memory in the vestibulo-ocular reflex Ann. Rev. Neurosci. 18 1995 409 441
26. S.H. Fatemi, A.R. Halt, and G. Realmuto Purkinje cell size is reduced in cerebellum of patients with autism Cell Mol. Neurobiol. 22 2002 171 175
27. S.A. Ferguson Neuroanatomical and functional alteration resulting from early postnatal cerebellar insults in rodents Pharmacol. Biochem. Behav. 55 1996 663 671
28. T. Gliga, and G. Csibra Seeing the face through the eyes: a developmental perspective on face expertise Progr. Brain Res. 164 2007 323 339
29. G. Gundappa-Sulur, E. De Schutter, and J.M. Bower Ascending granule cell axon: an important component of cerebellar cortical circuitry J. Comp. Neurol. 408 1999 580 596
30. T. Hashimoto, M. Tayama, K. Murakawa, T. Yoshimoto, and M. Miyazaki Development of the brainstem and cerebellum in autistic patients J. Aut. Dev. Disorder 25 1995 1 18
31. G. Hesslow, and C.H. Yeo The functional anatomy of skeletal conditioning J.W. Moore, A Neuroscientist's Guide to Classical Conditioning 2002 Springer-Verlag New York 86 146
32. S.M. Highstein, J. Porill, and P. Dean Report on a workshop concerning the cerebellum and motor learning, held in St. Louis October 2004 Cerebellum 4 2005 140 150
33. S. Hoehl, V.M. Reid, E. Parise, A. Handl, L. Palumbo, and T. Striano Looking at eye gaze processing and its neural correlates in infancy - implications for social development and autism spectrum disorder Child Dev. 80 2009 968 985
34. M. Ito The Cerebellum and Neural Control 1984 Raven Press New York
35. M. Ito Cerebellar long-term depression: characterization, signal transduction, and functional roles Physiol. Rev. 81 2001 1143 1195
36. M. Ito Cerebellar circuitry as a neuronal machine Prog. Neurobiol. 78 2006 272 303
37. M.H. Johnson, R. Griffin, G. Csibra, H. Halit, T. Farroni, and M. de Haan The emergence of the social brain network: evidence from typical and atypical development Dev. Psychopathol. 17 2005 599 619
38. V. Kaartinen, I. Gonzalez-Gomez, J.W. Voncken, L. Haataja, and E. Faure Abnormal function of astroglia lacking Abr and Bcr RacGAPs Development 128 2001 4217 4227
39. W.E. Kaufmann, K.L. Cooper, S.H. Mostofsky, G.T. Capone, and W.R. Kates Specificity of cerebellar vermian abnormalities in autism: a quantitative magnetic resonance imaging study J. Child Neurol. 18 2003 463 470
40. T.L. Kemper, and M.L. Bauman The contribution of neuropathologic studies to the understanding of autism Neurol. Clin. 11 1993 175 187
41. A. Kheradmand, and D.S. Zee Cerebellum and ocular motor control Front. Neurol. 2 2011 1 15
42. S.K.E. Koekkoek, A.M.V. Alphen, J.V.D. Burg, F. Grosveld, and N. Galjart Gain adaptation and phase dynamics of compensatory eye movements in mice Genes Function 1 1997 175 190
43. H. Komuro, and P. Rakic Distinct modes of neuronal migration in different domains of developing cerebellar cortex J. Neurosci. 18 1998 1478 1490
44. M. Lafarga, M.A. Andres, E. Calle, and M.T. Berciano Reactive gliosis of immature Bergman glia and microglial activation in response to cell death of granule cell precursors induced by methylazoxymethanol treatment in developing rat cerebellum Anat. Embryol. 198 1998 111 122
45. J. Laine, and H. Axelrad Lugaro cells target basket and stellate cells in the cerebellar cortex Neuroreport 9 1998 2399-2340
46. A.E. Lang, J. Duff, J.A. Saint-Cyr, L. Trepanier, and RE. Gross Posteroventral medial pallidotomy in Parkinson's disease J. Neurol. 246 Suppl 2 1999 II/28-41
47. S.R. Leekam, E. Hunnisett, and C. Moore Targets and cues: gaze-following in children with autism J. Child Psychol. Psychiatry 39 1998 951 962
48. S.R. Leekam, B. Lopez, and C. Moore Attention and joint attention in preschool children with autism Dev. Psychol. 36 2000 261 273
49. H.C. Leung, M. Suh, and R.E. Kettner Cerebellar flocculus and paraflocculus purkinje cell activity during circular pursuit in monkey J. Neurophysiol. 83 2000 13 30
50. H.P. Li, T. Miki, T. Yokoyama, K.Y. Lee, and H. Gu Regional differences in vulnerability of the cerebellar foliations of rats exposed to neonatal X-irradiation Neurosci. Lett. 402 2006 86 91
51. R. Lliňas Radial connectivity in the cerebellar cortex: a novel view regarding the functional organization of the molecular layer SL Palay, V Chan-Palay, The Cerebellum: New Vistas 1982 Springer Verlag New York 189 192
52. D.A. McCormick, J.E. Steinmetz, and R.F. Thompson Lesions of the inferior olivary complex cause extinction of the classically conditioned eyeblink response Brain Res. 359 1985 120 130
53. A. Mendlin, F.J. Martin, L.E. Rueter, and B.L. Jacobs Neuronal release of serotonin in the cerebellum of behaving rats: an in vivo microdialysis study J. Neurochem. 67 1996 617 622
54. E. Mugnaini, and A. Floris The unipolar brush cell: a neglected neuron of the mammalian cerebellar cortex J. Comp. Neurol. 339 1994 174 180
55. P. Mundy, M. Sigman, J. Ungerer, and T. Sherman Defining the social deficits of autism: the contribution of non-verbal communication measures J. Child Psychol. Psychiatry 27 1986 657 669
56. D. Necchi, C. Soldani, G. Bernocchi, and E. Scherini Development of the anatomical alteration of the cerebellar fissura prima Anat. Rec. 259 2000 150 156
57. H. Noda, and D.A. Suzuki The role of the flocculus of the monkey in fixation and smooth pursuit eye movements J. Physiol. 387 1979 611 628
58. M.G. Nunzi, S. Birnstiel, B.J. Bhattacharyya, N.T. Slater, and E. Mugnaini Unipolar brush cells form a glutamatergic projection system within the mouse cerebellar cortex J. Comp. Neurol. 434 2001 329 341
59. M. Ohki, H. Kitazawa, T. Hiramatsu, K. Kaga, T. Kitamura, J. Yamada, and S. Nagao Role of primate cerebellar hemisphere in voluntary eye movemen control revealed by lesion effects J. Neurophysiol. 101 2009 934 937
60. O. Oscarsson Functional units of the cerebellum-saggital zones and microzones Trends Neurosci. 2 1979 143 145
61. S.L. Palay, and V. Chan-Palay Cerebellar Cortex; Cytology and Organization 1974 Springer-Verlag New York
62. S.J. Palmen, H. van Engelan, P.R. Hof, and C. Schmitz Neuropathological findings in autism Brain 127 2004 2572 2583
63. M.B. Pisu, E. Roda., S. Guioli, D. Avella, and M.G. Bottone Proliferation and migration of granule cells in the developing rat cerebellum: cisplatin effects Anat. Rec. 287 2005 1226 1235
64. myd mouse are associated with disruptions in Bergmann glia organization and delayed migration of granule neurons Cerebellum 4 2005 261 270
65. P. Rakic Neuron-glia relationships during granule cell migration in developing cerebellar cortex. A Golgi and electron microscopic study in Macacus rhesus J. Comp. Neurol. 141 1971 283 312
66. P. Rakic Neuron glia interaction during brain development Trends Neurosci. 4 1981 184 187
67. E.R. Ritvo, B.J. Freeman, A.B. Scheibel, T. Duong, and H. Robinson Lower Purkinje cell counts in the cerebella of four autistic subjects: initial findings of the UCLA-NSAC autopsy research report Am. J. Psychiatry 143 1986 862 866
68. L.B. Rorke, M.H. Fogelson, and H.E. Riggs Cerebellar heterotopia in infancy Dev. Med. Child Neurol. 10 1968 644 650
69. U. Rosenhall, E. Johansson, and C. Gillberg Oculomotor findings in autistic children J. Laryngol. Otol. 102 1988 435 439
70. D.J. Rossi, S. Alford, E. Mugnaini, and N.T. Slater Properties of transmission at a giant glutamatergic synapse in cerebellum: the mossy fiber-unipolar brush cell synapse J. Neurophysiol. 74 1995 24 42
71. Y. Sato, and T. Kawasaki Identification of the Purkinje cell climbing fiber zone and its target neurons responsible for eye-movement control by the cerebellar flocculus Brain Res. Rev. 16 1991 39 64
72. J.E. Scharre, and M.P. Creedon Assessment of visual function in autistic children Optom. Vis. Sci. 69 1992 433 439
73. T. Striano, and V.M. Reid Social cognition in the first year Trends Cognit. Sci. 10 2006 471 476
74. A. Sudarov, and A.L. Joyner Cerebellum morphogenesis: the foliation pattern is orchestrated by multi-cellular anchoring centers Neural Dev. 2 2007 1 25
75. F Sultan, and J.M. Bower Quantitative Golgi study of the rat cerebellar molecular layer interneurons using principal component analysis J. Comp. Neurol. 393 1998 353 373
76. Y. Takarae, N.J. Minshew, B. Luna, C.M. Krisky, and J.A. Sweeney Pursuit eye movement deficits in autism Brain 127 2004 2584 2594
77. Y. Takarae, N.J. Minshew, B. Luna, and J.A. Sweeney Atypical involvement of frontostriatal systems during sensorimotor control in autism Psychiatry Res. 156 2007 117 127
78. J. Tan, A.H. Epema, and J. Voogd Zonal organization of the flocculovestibular nucleus projection in the rabbit: a combined axonal tracing and acetylcholinesterase histochemical study J. Comp. Neurol. 356 1995 51 71
79. W.T. Thach, H.P. Goodkin, and J.G. Keating The cerebellum and the adaptive coordination of movement Annu. Rev. Neurosci. 15 1992 403 442
80. P. Trouillas, and K. Fuxe Serotonin, the Cerebellum and Ataxia 1993 Raven New York
81. S. Trottier, B. Evrard, J.P. Vignal, J.M. Scarabin, and P. Chauvel The serotonergic innervation of the cerebral cortex in man and its changes in focal cortical dysplasia Epilepsy Res. 25 1996 79 106
82. J. Voogd, and F. Bigaré Topographical distribution of olivary and cortico nuclear fibers in the cerebellum: a Review J. Curveille, C. de Montigny, Y. Lamarre, The Inferior Olivary Nucleus: Anatomy and Physiology 1980 Raven New York 207 234
83. W. Waespe, B. Cohen, and T. Raphan Dynamic modification of the vestibulo-ocular reflex by the nodulus and uvula Science 228 1985 199 202
84. J Wegiel, I Kuchna, K. Nowicki, H. Imaki, and J. Wegiel The neuropathology of autism: Defects of neurogenesis and neuronal migration, and dysplastic changes Acta Neuropathol. 119 2010 755 770
85. J. Wegiel, N.C. Schanen, E.H. Cook, M. Sigman, and W.T. Brown Differences between the pattern of developmental abnormalities in autism associated with duplications 15q11.2-q13 and idiopathic autism J. Neuropathol. Exp. Neurol. 71 2012 382 397
86. Wegiel, J., Flory, M., Kuchna, I., Nowicki, K., Ma, S., et al., Brain-region specific trajectories of neuron volume growth during early childhood, adolescence and adulthood. Acta Neuropathol., submitted for publication.
87. E.R. Whitney, T.L. Kemper, M.L. Bauman, D.L. Rosene, and G.J. Blatt Cerebellar Purkinje cells are reduced in a subpopulation of autistic brains: a stereological experiment using Calbindin-D28k Cerebellum 7 2008 406 416
88. E.R. Whitney, T.L. Kemper, DL Rosene, ML Bauman, and GJ. Blatt Density of cerebellar basket and stellate cells in autism: evidence for a late developmental loss of Purkinje cells J. Neurosci. Res. 87 2009 2245 2254
89. G. Xiong, S. Nagao, and H. Kitazawa Mossy and climbing fiber collateral inputs in monkey cerebellar paraflocculus lobulus petrosus and hemispheric lobule VII and their relevance to oculomotor functions Neurosci. Lett. 468 2010 282 286
90. Q. Yue, G. Groszer, J.S. Gil, A.J. Berk, and A. Messing PTEN deletion in Bergmann glia leads to premature differentiation and affects laminar organization Development 132 2005 3281 3291
91. D.S. Zee, A Yamazaki, P.H. Butler, and G. Gucer Effects of ablation of the flocculus and paraflocculus on eye movement in the primate J. Neurophysiol. 46 1981 878 899
92. D.S. Zee, M.F. Walker, and S. Ramat The cerebellar contribution to eye movements based upon lesions: binocular three-axis control and the translational vestibulo-ocular reflex Ann. N.Y. Acad. Sci. 956 2002 178 189