Increased dendritic spine densities on cortical projection neurons in autism spectrum disorders

Brain Research

Volumn 1309, Issue , 2010, Pages 83-94

  Hutsler, Jeffrey J ^a   Zhang, Hong ^b  

^a UNIVERSITY OF NEVADA   (United States)

^b WUHAN UNIVERSITY   (China)

Author keywords

Autistic disorder; Cerebral cortex; Dendritic spine; Neuroanatomy; Pyramidal cell

Indexed keywords

ADOLESCENT; ADULT; ARTICLE; AUTISM; BRAIN CORTEX; BRAIN WEIGHT; CHILD; CLINICAL ARTICLE; COGNITION; CONTROLLED STUDY; DENDRITIC SPINE; DENSITY; FRONTAL LOBE; HUMAN; HUMAN TISSUE; NERVE CELL; NERVE PROJECTION; PARIETAL LOBE; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SCHOOL CHILD; SPINE DENSITY; TEMPORAL LOBE;

ADOLESCENT; ADULT; AGING; CELL SHAPE; CEREBRAL CORTEX; CHILD; CHILD DEVELOPMENT DISORDERS, PERVASIVE; COGNITION DISORDERS; DENDRITIC SPINES; EFFERENT PATHWAYS; FEMALE; HUMANS; MALE; MENTAL PROCESSES; MENTAL RETARDATION; MIDDLE AGED; NEURAL PATHWAYS; ORGAN SIZE; PYRAMIDAL CELLS; SILVER STAINING; SYNAPSES; YOUNG ADULT;

EID: 72049108920     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2009.09.120     Document Type: Article

References (95)

1. Akshoomoff N., Pierce K., and Courchesne E. The neurobiological basis of autism from a developmental perspective. Dev. Psychopathol. 14 (2002) 613-634
2. Amaral D., and Price J. Amygdalo-cortical projections in the monkey (Macaca fasicularis). J. Comp. Neurol. 230 (1984) 465-496
3. Aylward E., Minshew N., Field B., Sparks B., and Singh N. Effects of age on brain volume and head circumference in autism. Neurology 59 (2002) 175-183
4. Bailey A., Luthert P., Bolton P., Le Couteur A., Rutter M., and Harding B. Autism and megalencephaly. Lancet 341 (1993) 1225-1226
5. Bailey A., Luthert P., Dean A., Harding B., Janota I., Montgomery M., Rutter M., and Lantos P. A clinicopathological study of autism. Brain 121 (1998) 889-905
6. Bailey P., and von Bonin G. The Isocortex of Man (1951), University of Illinois Press, Urbana
7. Baron-Cohen S., Ring H.A., Wheelwright S., Bullmore E.T., Brammer M.J., Simmons A., and Williams S.C.R. Social intelligence in the normal and autistic brain: an fMRI study. Eur. J. Neurosci. 11 (1999) 1891-1898
8. Bauman M., and Kemper T. Histoanatomic observations of the brain in early infantile autism. Neurology 35 (1985) 866-872
9. Bauman M., and Kemper T. Neuroanatomic observations of the brain in autism: a review and future directions. Int. J. Dev. Neurosci. 23 (2005) 183-187
10. Belmonte M., Allen G., Beckel-Mitchener A., Boulanger L., Carper R., and Webb S. Autism and abnormal development of brain connectivity. J. Neurosci. 24 (2004) 9228-9231
11. Belmonte M., and Yurgelun-Todd D. Functional anatomy of impaired selective attention and compensatory processing in autism. Cogn. Brain Res. 17 (2003) 651-664
12. Benes F., Paskevich P., Davidson R., and Domesick V. Synaptic rearrangements in medial prefrontal cortex of haloperidol-treated rats. Brain Res. 348 (1985) 15-20
13. Benitez-Bribiesca L., De la Rosa-Alvarez I., and Mansilla-Olivares A. Dendritic spine pathology in infants with severe protein-calorie malnutrition. Pediatrics 104 (1999) e21
14. Bigler E., Tate D., Neeley E., Wolfson L., Miller M., Rice S., Cleavinger H., Anderson C., Coon H., Ozonoff S., Johnson M., Dinh E., Lu J., McMahon W., and Lainhart J. Temporal lobe, autism, and macrocephaly. Am. J. Neuroradiol. 24 (2003) 2066-2076
15. Boddaert N., Chabane N., Gervais H., Good C., Bourgeois M., Plumet M., Barthelemy C., Mouren M., Artiges E., Samson Y., Brunelle F., Frackowiak R., and Zilbovicius M. Superior temporal sulcus anatomical abnormalities in childhood autism: a voxel-based morphometry MRI study. Neuroimage 23 (2004) 364-369
16. Carper R., Moses P., Tigue Z., and Courchesne E. Cerebral lobes in autism: early hyperplasia and abnormal age effects. Neuroimage 16 (2002) 1038-1051
17. Casanova M., Buxhoeveden D., Switala A., and Roy E. Minicolumnar pathology in autism. Neurology 58 (2002) 428-432
18. Cherkassky V.L., Kana R.K., Keller T.A., and Just M.A. Functional connectivity in a baseline resting-state network in autism. NeuroReport 17 (2006) 1687-1690
19. Coben R., Clarke A.R., Hudspeth W., and Barry R.J. EEG power and coherence in autistic spectrum disorder. Clin. Neurophysiol. 119 (2008) 1002-1009
20. Cohen I., Sudhalter V., Pfadt A., Jenkins E., Brown W., and Vietze P. Why are autism and the fragile-X syndrome associated? Conceptual and methodological issues. Am. J. Hum. Genet. 48 (1991) 195-202
21. Courchesne E. Brain development in autism: early overgrowth followed by premature arrest of growth. Ment. Retard. Dev. Disabil. Res. Rev. 10 (2004) 106-111
22. Courchesne E., Carper R., and Akshoomoff N. Evidence of brain overgrowth in the first year of life in autism. J. Am. Med. Assn. 290 (2003) 337-344
23. Courchesne E., Muller R., and Saitoh O. Brain weight in autism: normal in the majority of cases, megalencephalic in rare cases. Neurology 52 (1999) 1057-1059
24. Courchesne E., and Pierce K. Why the frontal cortex in autism might be talking only to itself: local over-connectivity but long-distance disconnection. Curr. Opin. Neurobiol. 15 (2005) 225-230
25. Critchley H.D., Daly E.M., Bullmore E.T., Williams S.C.R., Van Amelsvoort T., Robertson D.M., Rowe A., Phillips M., McAlonan G., Howlin P., and Murphy D.G.M. The functional neuroanatomy of social behaviour-changes in cerebral blood flow when people with autistic disorder process facial expressions. Brain 123 (2000) 2203-2212
26. Dawson G., Ashman S., and Carver L. The role of early experience in shaping behavioral and brain development and its implications for social policy. Dev. Psychopathol. 12 (2000) 695-712
27. Demark J., Feldman M., and Holden J. Behavioral relationship between autism and fragile X syndrome. Am. J. Ment. Retard. 108 (2003) 314-326
28. Deutsch C., and Joseph R. Brief report: cognitive correlates of enlarged head circumference in children with autism. J. Autism Dev. Disord. 33 (2003) 209-215
29. Dietzmann K., and von Bossanyi P. Dendritic spines and immunoreactivity of synaptophysin in the frontal cortex of humans with infantile brain damage. A correlative study. Clin. Neuropathol. 13 (1994) 127-133
30. Feldman M., and Peters A. A technique for estimating total spine numbers on Golgi-impregnated dendrites. J. Comp. Neurol. 188 (1979) 527-542
31. Ferrer I., and Galofre E. Dendritic spine anomalies in fetal alcohol syndrome. Neuropediatrics 18 (1987) 161-163
32. Fiala J., Spacek J., and Harris K. Dendritic spine pathology: cause or consequence of neurological disorders?. Brain Res. Rev. 39 (2002) 29-54
33. Filipek P., Richelme C., Kennedy D., Rademacher J., Pitcher D., Zidel S., and Caviness V. Morphometric analysis of the brain in developmental language disorders and autism. Ann. Neurology 32 (1992) 475
34. Frith C. What do imaging studies tell us about the neural basis of autism?. Novartis Found. Symp. 251 (2003) 149-166
35. Frith C. Is autism a disconnection disorder?. Lancet Neurol. 3 (2004) 577
36. Gage N.M., Siegel B., Callen M., and Roberts T.P.L. Cortical sound processing in children with autism disorder: an MEG investigation. Neuroreport 14 (2003) 2047-2051
37. Garey L., Ong W., Patel T., Kanani M., Davis A., Mortimer A., Barnes T., and Hirsch S. Reduced dendritic spine density on cerebral cortical pyramidal neurons in schizophrenia. J. Neurol. Neurosurg. Psychiatry 65 (1998) 446-453
38. Gervais H., Belin P., Boddaert N., Leboyer M., Coez A., Sfaello I., Barthelemy C., Brunelle F., Samson Y., and Zilbovicius M. Abnormal cortical voice processing in autism. Nature Neuroscience 7 (2004) 801-802
39. Geschwind D.H., and Levitt P. Autism spectrum disorders: developmental disconnection. Curr. Opin. Neurobiol. 17 (2007) 103-111
40. Glaser E., and Van Der Loos H. Analysis of thick brain sections by obverse-reverse computer microscopy: application of a new, high clarity Golgi-Nissl stain. J. Neurosci. Methods 4 (1981) 117-125
41. Glasson E., Bower C., Petterson B., de Klerk N., Chaney G., and Hallmayer J. Perinatal factors and the development of autism: a population study. Arch. Gen. Psychiatry 61 (2004) 618-627
42. Guerin P., Lyon G., Barthelemy C., Sostak E., Chevrollier V., Garreau B., and Lelord G. Neuropathological study of a case of autistic syndrome with severe mental retardation. Dev. Med. Child Neurol. 38 (1996) 203-211
43. Halpain S., Spencer K., and Graber S. Dynamics and pathology of dendritic spines. Prog. Brain Res. 147 (2005) 29-37
44. Happé F. Autism: cognitive deficit or cognitive style?. Trends Cogn. Sci. 3 (1999) 216-222
45. Hardan A., Jou R., Keshavan M., Varma R., and Minshew N. Increased frontal cortical folding in autism: a preliminary MRI study. Psychiat. Res. 131 (2004) 263-268
46. Herbert M., Ziegler D., Deutsch C., O'Brien L., Lange N., Bakardjiev A., Hodgson J., Adrien K., Steele S., Makris N., Kennedy D., Harris G., and Caviness V.J. Dissociations of cerebral cortex, subcortical and cerebral white matter volumes in autistic boys. Brain 126 (2003) 1182-1192
47. Herbert M., Ziegler D., Makris N., Filipek P., Kemper T., Normandin J., Sanders H., Kennedy D., and Caviness V.J. Localization of white matter volume increase in autism and developmental language disorders. Ann. Neurol. 55 (2004) 530-540
48. Hughes J.R. Autism: the first firm finding = underconnectivity?. Epilepsy Behav. 11 (2007) 20-24
49. Hutsler J.J., Love T., and Zhang H. Histological and MRI assessment of cortical layering and thickness in autism spectrum disorders. Biol. Psychiat. 61 (2007) 449-457
50. Huttenlocher P., and Dabholkar A. Regional differences in synaptogenesis in human cerebral cortex. J. Comp. Neurol. 387 (1997) 167-178
51. Ijichi S., and Ijichi N. The prenatal autistic imprinting hypothesis: developmental maladaptation to the environmental changes between womb and the social world. Med. Hypotheses 62 (2004) 188-194
52. Irwin S., Galvez R., and Greenough W. Dendritic spine structural anomalies in fragile-X mental retardation syndrome. Cereb. Cortex 10 (2000) 1038-1044
53. Irwin S., Patel B., Idupulapati M., Harris J., Crisostomo R., Larsen B., Kooy F., Willems P., Cras P., Kozlowski P., Swain R., Weiler I., and Greenough W. Abnormal dendritic spine characteristics in the temporal and visual cortices of patients with fragile-X syndrome: a quantitative examination. Am. J. Med. Genet. 98 (2001) 161-167
54. Jacobs B., Driscoll L., and Schall M. Life-span dendritic and spine changes in areas 10 and 18 of human cortex: a quantitative Golgi study. J. Comp. Neurol. 386 (1997) 661-680
55. Jacobs B., Schall M., Prather M., Kapler E., Driscoll L., Baca S., Jacobs J., Ford K., Wainwright M., and Treml M. Regional dendritic and spine variation in human cerebral cortex: a quantitative Golgi study. Cereb. Cortex 11 (2001) 558-571
56. Just M.A., Cherkassky V.L., Keller T., and Minshew N. Cortical activation and synchronization during sentence comprehension in high-functioning autism: evidence of underconnectivity. Brain 127 (2004) 1811-1821
57. Just M.A., Cherkassky V.L., Keller T.A., Kana R.K., and Minshew N.J. Functional and anatomical cortical underconectivity in autism: evidence from an fMRI study of an executive function task and corpus callosum morphometry. Cereb. Cortex 17 (2007) 951-961
58. Kaufmann W., Cortell R., Kau C., Bukelis I., Tierney E., Gray R., Cox C., Capone G., and Stanard P. Autism spectrum disorder in fragile X syndrome: Communication, social interaction, and specific behaviors. Am. J. Med. Genet. 17 (2004) 225-234
59. Koenderink M., and Uylings H. Postnatal maturation of layer V pyramidal neurons in the human prefrontal cortex. A quantitative Golgi analysis. Brain Res. 678 (1995) 233-243
60. Koenderink M., Uylings H., and Mrzljak L. Postnatal maturation of the layer III pyramidal neurons in the human prefrontal cortex: a quantitative Golgi analysis. Brain Res. 653 (1994) 173-182
61. Koshino H., Carpenter P., Minshew N., Cherkassky V., Keller T., and Just M. Functional connectivity in an fMRI working memory task in high-functioning autism. Neuroimage 24 (2005) 810-821
62. Lee J.E., Bigler E.D., Alexander A.L., Lazar M., DuBray M.B., Chung M.K., Johnson M., Morgan J., Miller J.N., McMahon W.M., Lu J., Jeong E.-K., and Lainhart J.E. Diffusion tensor imaging of white matter in the superior temporal gyrus and temporal stem in autism. Neurosci. Lett. 424 (2007) 127-132
63. Lewis J.D., and Elman J.L. Growth-related neural reorganization and the autism phenotype: a test of the hypothesis that altered brain growth leads to altered connectivity. Dev. Sci. 11 (2008) 135-155
64. Lord C., Rutter M., and LeCouteur A. 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 (1994) 659-685
65. McAllister A.K. Dynamic aspects of CNS synapse formation. Ann. Rev. Neurosci. 30 (2007) 425-450
66. Meresse I.G., Zilbovicius M., Boddaert N., Robel L., Philippe A., Sfaello I., Laurier L., Brunelle F., Samson Y., Mouren M.C., and Chabane N. Autism severity and temporal lobe functional abnormalities. Annals Neurol. 58 (2005) 466-469
67. Michel A., and Garey L. The development of dendritic spines in the human visual cortex. Hum. Neurobiol. 3 (1984) 223-227
68. Miles J., Hadden L., Takahashi T., and Hillman R. Head circumference is an independent clinical finding associated with autism. Am. J. Med. Genet. 95 (2000) 339-350
69. Mizuno A., Villalobos M.E., Davies M.M., Dahl B.C., and Müller R.-A. Partially enhanced thalamocortical functional connectivity in autism. Brain Res. 1104 (2006) 160-174
70. Moessner R., Marshall C.R., Sutcliffe J.S., Skaug J., Pinto D., Vincent J., Zwaigenbaum L., Fernandez B., Roberts W., Szatmari P., and Scherer S.W. Contribution of SHANK3 mutations to autism spectrum disorder. Am. J. Hum. Gen. 81 (2008) 1289-1297
71. Muhle R., Trentacoste S., and Rapin I. The genetics of autism. Pediatrics 113 (2004) e472-486
72. Müller R.-A. The study of autism as a distributed disorder. Ment. Retard. Dev. Disabil. Res. Rev. 13 (2007) 85-95
73. Multani P., Myers R., Blume H., Schomer D., and Sotrel A. Neocortical dendritic pathology in human partial epilepsy: a quantitative Golgi study. Epilepsia 35 (1994) 728-736
74. Mundy P., and Neal R. Neural plasticity, joint attention, and a transactional social-orienting model of autism. Int. Rev. Res. Ment. Retardation 20 (2001) 139-168
75. Piven J., Arndt S., Bailey J., and Andreasen N. Regional brain enlargement in autism: a magnetic resonance imaging study. J. Am. Acad. Child. Adolesc. Psychiatr. 35 (1996) 530-536
76. Piven J., Arndt S., Bailey J., and Havercamp S. An MRI study of brain size in autism. Am. J. Psychiat. 152 (1995) 1145
77. Piven J., Nehme E., Simon J., Barta P., Pearlson G., and Folstein S. Magnetic resonance imaging in autism: measurement of the cerebellum, pons, and fourth ventricle. Biol. Psychiatry 31 (1992) 491-504
78. Rapin I. Autism. N. Engl. J. Med. 337 (1997) 97-104
79. Raymond G., Bauman M., and Kemper T. Hippocampus in autism: a Golgi analysis. Acta Neuropathol. (Berl.) 91 (1996) 117-119
80. Riley J. A reliable Golgi-Kopsch modification. Brain Res. Bull. 4 (1979) 127-129
81. Rinaldi T., Silberberg G., and Markram H. Hyperconnectivity of local neocortical microcircuitry induce by prenatal exposure to valproic acid. Cereb. Cortex 18 (2008) 763-770
82. Rippon G., Brock J., Brown C., and Boucher J. Disordered connectivity in the autistic brain: challenges for the 'new psychophyioslogy'. J. Psychophysiol. 63 (2007) 164-172
83. Rogers S., Wehner D., and Hagerman R. The behavioral phenotype in fragile X: symptoms of autism in very young children with fragile X syndrome, idiopathic autism, and other developmental disorders. J. Dev. Behav. Pediatr. 22 (2001) 409-417
84. Sabaratnam M. Pathological and neuropathological findings in two males with fragile-X syndrome. J. Intellect. Disabil. Res. 44 (2000) 81-85
85. Schultz, R.T., Gauthier, I., Klin, A., Fulbright, R.K., Anderson, A.W., Volkmar, F., Skudlarski, P., Lacadic, C., Cohen, D.J., Gore, J.C., 2000. Abnormal ventral temporal cortical activity during face discrimination among individuals with autism and Asperger syndrome. Vol. 57, ed.^eds., pp. 331-340.
86. Shaw P., Kabini N.J., Lerch J.P., Eckstrand K., Lenroot R., Gogtay N., Greenstein D., Clasen L., Evans A., Rapoport J.L., Giedd J.N., and Wise S.P. Neurodevelopmental trajectories of the human cerebral cortex. J. Neurosci. 281 (2008) 3586-3594
87. Spacek J. Dynamics of the Golgi method: a time-lapse study of the early stages of impregnation in single sections. J. Neurocytol. 18 (1989) 27-38
88. Spacek J. Dynamics of Golgi impregnation in neurons. Microsc. Res. Tech. 23 (1992) 264-274
89. Sparks B., Friedman S., Shaw D., Aylward E., Echelard D., Artru A., Maravilla K., Giedd J., Munson J., Dawson G., and Dager S. Brain structural abnormalities in young children with autism spectrum disorder. Neurology 59 (2002) 184-192
90. Suetsugu M., and Mehraein P. Spine distribution along the apical dendrites of the pyramidal neurons in Down's syndrome. A quantitative Golgi study. Acta Neuropathol. 50 (1980) 207-210
91. Swann J., Al-Noori S., Jiang M., and Lee C. Spine loss and other dendritic abnormalities in epilepsy. Hippocampus 10 (2000) 617-625
92. Takashima S., Chan F., Becker L., and Kuruta H. Aberrant neuronal development in hemimegalencephaly: immunohistochemical and Golgi studies. Pediatr. Neurol. 7 (1991) 275-280
93. Vidal C.N., Nicolson R., DeVito T.J., Hayashi K.M., Geago J.A., Drost D.J., Williamson P.C., Rajakumar N., Sui Y., Dutton R.A., and Toga A.W. Mapping corpus callosum deficits in autism: an index of aberrant cortical connectivity. Biol. Psychiatry 60 (2006) 218-225
94. von Economo C., and Koskinas G. Die Cytoarchitektonik der Hirnrinde des erwachsenen Menschen (1925), Julius Springer Verlag, Berlin
95. Williams R., Hauser S., Purpura D., DeLong G., and Swisher C. Autism and mental retardation: neuropathologic studies performed in four retarded persons with autistic behavior. Arch. Neurol. 37 (1980) 749-753