Abnormal microglial-neuronal spatial organization in the dorsolateral prefrontal cortex in autism

Brain Research

Volumn 1456, Issue , 2012, Pages 72-81

  Morgan, John T ^a   Chana, Gursharan ^b   Abramson, Ian ^c   Semendeferi, Katerina ^c   Courchesne, Eric ^a   Everall, Ian P ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Autism; Microglia; Neuron; Postmortem; Spatial organization

Indexed keywords

ARTICLE; AUTISM; AUTOPSY; BRAIN GROWTH; CELL ACTIVATION; CELL INTERACTION; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MICROGLIA; NERVE CELL; NERVE CELL DIFFERENTIATION; PREFRONTAL CORTEX; PRIORITY JOURNAL;

ADOLESCENT; ADULT; AUTISTIC DISORDER; AUTOPSY; CHILD; CHILD, PRESCHOOL; HUMANS; MALE; MICROGLIA; NEURONS; PREFRONTAL CORTEX; YOUNG ADULT;

EID: 84860611251     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2012.03.036     Document Type: Article

References (57)

1. G. Ahlsen, L. Rosengren, M. Belfrage, A. Palm, K. Haglid, A. Hamberger, and C. Gillberg Glial fibrillary acidic protein in the cerebrospinal fluid of children with autism and other neuropsychiatric disorders Biol. Psychiatry 33 1993 734 743 (Pubitemid 23205331)
2. E. Asare, G. Dunn, J. Glass, J. McArthur, P. Luthert, P. Lantos, and I. Everall Neuronal pattern correlates with the severity of human immunodeficiency virus-associated dementia complex. Usefulness of spatial pattern analysis in clinicopathological studies Am. J. Pathol. 148 1996 31 38 (Pubitemid 26019640)
3. A. Bailey, P. Luthert, A. Dean, B. Harding, I. Janota, M. Montgomery, M. Rutter, and P. Lantos A clinicopathological study of autism Brain 121 1998 889 905 (Pubitemid 28220896)
4. M. Bauman Neuroanatomic observations of the brain in pervasive developmental disorders J. Autism Dev. Disord. 26 1996 199 203
5. M.L. Bauman, and T.L. Kemper Neuroanatomic observations of the brain in autism Vol. M.L. Bauman, T.L. Kemper, The Neurobiology of Autism 1994 Johns Hopkins UP Baltimore 119 145
6. A. Bessis, D. Bernard, and A. Triller Tumor necrosis factor-alpha and neuronal development Neuroscientist 11 2005 277 281 (Pubitemid 41040856)
7. A. Bessis, C. Bechade, D. Bernard, and A. Roumier Microglial control of neuronal death and synaptic properties Glia 55 2007 233 238 (Pubitemid 46225955)
8. K. Blinzinger, and G. Kreutzberg Displacement of synaptic terminals from regenerating motoneurons by microglial cells Z. Zellforsch. Mikrosk. Anat. 85 1968 145 157
9. D.P. Buxhoeveden, K. Semendeferi, J. Buckwalter, N. Schenker, R. Switzer, and E. Courchesne Reduced minicolumns in the frontal cortex of patients with autism Neuropathol. Appl. Neurobiol. 32 2006 483 491 (Pubitemid 44401510)
10. R.A. Carper, and E. Courchesne Localized enlargement of the frontal cortex in early autism Biol. Psychiatry 57 2005 126 133 (Pubitemid 40094712)
11. R.A. Carper, P. Moses, Z.D. Tigue, and E. Courchesne Cerebral lobes in autism: early hyperplasia and abnormal age effects Neuroimage 16 2002 1038 1051
12. M.F. Casanova, D.P. Buxhoeveden, and C. Brown Clinical and macroscopic correlates of minicolumnar pathology in autism J. Child Neurol. 17 2002 692 695 (Pubitemid 36054407)
13. M.F. Casanova, D.P. Buxhoeveden, A.E. Switala, and E. Roy Minicolumnar pathology in autism Neurology 58 2002 428 432 (Pubitemid 34150918)
14. M.F. Casanova, I.A. van Kooten, A.E. Switala, H. van Engeland, H. Heinsen, H.W. Steinbusch, P.R. Hof, J. Trippe, J. Stone, and C. Schmitz Minicolumnar abnormalities in autism Acta Neuropathol (Berl) 112 2006 287 303 (Pubitemid 44275884)
15. G. Chana, S. Landau, C. Beasley, I.P. Everall, and D. Cotter Two-dimensional assessment of cytoarchitecture in the anterior cingulate cortex in major depressive disorder, bipolar disorder, and schizophrenia: evidence for decreased neuronal somal size and increased neuronal density Biol. Psychiatry 53 2003 1086 1098 (Pubitemid 36695084)
16. K.S. Christopherson, E.M. Ullian, C.C. Stokes, C.E. Mullowney, J.W. Hell, A. Agah, J. Lawler, D.F. Mosher, P. Bornstein, and B.A. Barres Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis Cell 120 2005 421 433 (Pubitemid 40222435)
17. D. Cotter, S. Landau, C. Beasley, R. Stevenson, G. Chana, L. MacMillan, and I. Everall The density and spatial distribution of GABAergic neurons, labelled using calcium binding proteins, in the anterior cingulate cortex in major depressive disorder, bipolar disorder, and schizophrenia Biol. Psychiatry 51 2002 377 386 (Pubitemid 34251175)
18. E. Courchesne, C. Karns, H.R. Davis, R. Ziccardi, R. Carper, Z. Tigue, K. Pierce, P. Moses, H.J. Chisum, C. Lord, A.J. Lincoln, S. Pizzo, L. Schreibman, R.H. Haas, N. Akshoomoff, and R.Y. Courchesne Unusual brain growth patterns in early life in patients with autistic disorder: an MRI study Neurology 57 2001 245 254 (Pubitemid 32667357)
19. N. Davoust, C. Vuaillat, G. Androdias, and S. Nataf From bone marrow to microglia: barriers and avenues Trends Immunol. 29 2008 227 234
20. G. Dawson, J. Munson, S.J. Webb, T. Nalty, R. Abbott, and K. Toth Rate of head growth decelerates and symptoms worsen in the second year of life in autism Biol. Psychiatry 61 2007 458 464 (Pubitemid 46185340)
21. Y.A. Dementieva, D.D. Vance, S.L. Donnelly, L.A. Elston, C.M. Wolpert, S.A. Ravan, G.R. DeLong, R.K. Abramson, H.H. Wright, and M.L. Cuccaro Accelerated head growth in early development of individuals with autism Pediatr. Neurol. 32 2005 102 108 (Pubitemid 40138691)
22. P.J. Diggle, and A.G. Chetwynd Second-order analysis of spatial clustering for inhomogeneous populations Biometrics 47 1991 1155 1163
23. C. Dissanayake, Q.M. Bui, R. Huggins, and D.Z. Loesch Growth in stature and head circumference in high-functioning autism and Asperger disorder during the first 3 years of life Dev. Psychopathol. 18 2006 381 393
24. K. Garbett, P.J. Ebert, A. Mitchell, C. Lintas, B. Manzi, K. Mirnics, and A.M. Persico Immune transcriptome alterations in the temporal cortex of subjects with autism Neurobiol. Dis. 30 2008 303 311
25. S. Gupta, S. Aggarwal, B. Rashanravan, and T. Lee Th1- and Th2-like cytokines in CD4 + and CD8 + T cells in autism J. Neuroimmunol. 85 1998 106 109 (Pubitemid 28255444)
26. H.C. Hazlett, M. Poe, G. Gerig, R.G. Smith, J. Provenzale, A. Ross, J. Gilmore, and J. Piven Magnetic resonance imaging and head circumference study of brain size in autism: birth through age 2 years Arch. Gen. Psychiatry 62 2005 1366 1376 (Pubitemid 41746614)
27. J.J. Hutsler, and H. Zhang Increased dendritic spine densities on cortical projection neurons in autism spectrum disorders Brain Res. 1309 2010 83 94
28. J.J. Hutsler, T. Love, and H. Zhang Histological and magnetic resonance imaging assessment of cortical layering and thickness in autism spectrum disorders Biol. Psychiatry 61 2007 449 457 (Pubitemid 46185329)
29. H. Jyonouchi, S. Sun, and H. Le Proinflammatory and regulatory cytokine production associated with innate and adaptive immune responses in children with autism spectrum disorders and developmental regression J. Neuroimmunol. 120 2001 170 179 (Pubitemid 33016737)
30. R. Kalla, Z. Liu, S. Xu, A. Koppius, Y. Imai, C.U. Kloss, S. Kohsaka, A. Gschwendtner, J.C. Moller, A. Werner, and G. Raivich Microglia and the early phase of immune surveillance in the axotomized facial motor nucleus: impaired microglial activation and lymphocyte recruitment but no effect on neuronal survival or axonal regeneration in macrophage-colony stimulating factor-deficient mice J. Comp. Neurol. 436 2001 182 201 (Pubitemid 32622530)
31. T. Kemper, and M. Bauman Neuropathology of infantile autism J. Neuropathol. Exp. Neurol. 57 1998 645 652 (Pubitemid 28335053)
32. G.W. Kreutzberg Microglia: a sensor for pathological events in the CNS Trends Neurosci. 19 1996 312 318 (Pubitemid 26349059)
33. S. Landau, and I.P. Everall Nonparametric bootstrap for k-functions arising from mixed-effects models with applications in neuropathology Stat. Sin. 18 2008 1375 1393
34. S. Landau, S. Rabe-Hersketh, and I.P. Everall Nonparametric one-way analysis of variance of replicated bivariate spatial point patterns Biom. J. 46 2004 19 34 (Pubitemid 41448941)
35. J.A. Laurence, and S.H. Fatemi Glial fibrillary acidic protein is elevated in superior frontal, parietal and cerebellar cortices of autistic subjects Cerebellum 4 2005 206 210 (Pubitemid 41354430)
36. X. Li, A. Chauhan, A.M. Sheikh, S. Patil, V. Chauhan, X.M. Li, L. Ji, T. Brown, and M. Malik Elevated immune response in the brain of autistic patients J. Neuroimmunol. 207 2009 111 116
37. J.T. Morgan, G. Chana, C.A. Pardo, C. Achim, K. Semendeferi, J. Buckwalter, E. Courchesne, and I.P. Everall Microglial activation and increased microglial density observed in the dorsolateral prefrontal cortex in autism Biol. Psychiatry. 68 2010 368 376
38. A. Nimmerjahn, F. Kirchhoff, and F. Helmchen Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo Science 308 2005 1314 1318 (Pubitemid 40746128)
39. M. Petrides, and D.N. Pandya Comparative architectonic analysis of the human and the macaque frontal cortex F. Boller, J. Grafman, Handbook of Neuropsychology Vol. 9 1994 Elsevier Science Ltd Amsterdam 17 58
40. G. Rajkowska, and P.S. Goldman-Rakic Cytoarchitectonic definition of prefrontal areas in the normal human cortex: I. Remapping of areas 9 and 46 using quantitative criteria Cereb. Cortex 5 1995 307 322
41. R.M. Ransohoff, and V.H. Perry Microglial physiology: unique stimuli, specialized responses Annu. Rev. Immunol. 27 2009 119 145
42. G.V. Raymond, M.L. Bauman, and T.L. Kemper Hippocampus in autism: a Golgi analysis Acta Neuropathol. 91 1996 117 119
43. E. Redcay, and E. Courchesne When is the brain enlarged in autism? A meta-analysis of all brain size reports Biol. Psychiatry 58 2005 1 9 (Pubitemid 40909929)
44. K. Schladitz, A. Sarkka, I. Pavenstadt, O. Haferkamp, and T. Mattfeldt Statistical analysis of intramembranous particles using freeze fracture specimens J. Microsc. 211 2003 137 153 (Pubitemid 36960547)
45. C.M. Schumann, and D.G. Amaral Stereological analysis of amygdala neuron number in autism J. Neurosci. 26 2006 7674 7679 (Pubitemid 44315187)
46. C.M. Schumann, C.S. Bloss, C.C. Barnes, G.M. Wideman, R.A. Carper, N. Akshoomoff, K. Pierce, D. Hagler, N. Schork, C. Lord, and E. Courchesne Longitudinal magnetic resonance imaging study of cortical development through early childhood in autism J. Neurosci. 30 2010 4419 4427
47. B.N. Shokouhi, B.Z. Wong, S. Siddiqui, A.R. Lieberman, G. Campbell, K. Tohyama, and P.N. Anderson Microglial responses around intrinsic CNS neurons are correlated with axonal regeneration BMC Neurosci. 11 2010 13
48. V.K. Singh, R.P. Warren, J.D. Odell, and P. Cole Changes of soluble interleukin-2, interleukin-2 receptor, T8 antigen, and interleukin-1 in the serum of autistic children Clin. Immunol. Immunopathol. 61 1991 448 455
49. B.F. Sparks, S.D. Friedman, D.W. Shaw, E. Aylward, D. Echelard, A.A. Artru, K.R. Maravilla, J.N. Giedd, J. Munson, G. Dawson, and S.R. Dager Brain sructural abnormalities in young children with autism spectrum disorder Neurology 59 2002 184 192 (Pubitemid 34779175)
50. M. Svensson, P. Eriksson, J. Persson, L. Liu, and H. Aldskogius Functional properties of microglia following peripheral nerve injury Neuropathol. Appl. Neurobiol. 20 1994 185 187 (Pubitemid 24123555)
51. B.D. Trapp, J.R. Wujek, G.A. Criste, W. Jalabi, X. Yin, G.J. Kidd, S. Stohlman, and R. Ransohoff Evidence for synaptic stripping by cortical microglia Glia 55 2007 360 368
52. I.A. van Kooten, S.J. Palmen, P. von Cappeln, H.W. Steinbusch, H. Korr, H. Heinsen, P.R. Hof, H. van Engeland, and C. Schmitz Neurons in the fusiform gyrus are fewer and smaller in autism Brain 131 2008 987 999 (Pubitemid 351499430)
53. D.L. Vargas, C. Nascimbene, C. Krishnan, A.W. Zimmerman, and C.A. Pardo Neuroglial activation and neuroinflammation in the brain of patients with autism Ann. Neurol. 57 2005 67 81 (Pubitemid 40053317)
54. I. Voineagu, X. Wang, P. Johnston, J.K. Lowe, Y. Tian, S. Horvath, J. Mill, R.M. Cantor, B.J. Blencowe, and D.H. Geschwind Transcriptomic analysis of autistic brain reveals convergent molecular pathology Nature 474 2011 380 384
55. H. Wake, A.J. Moorhouse, S. Jinno, S. Kohsaka, and J. Nabekura Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals J. Neurosci. 29 2009 3974 3980
56. S.J. Webb, T. Nalty, J. Munson, C. Brock, R. Abbott, and G. Dawson Rate of head circumference growth as a function of autism diagnosis and history of autistic regression J. Child Neurol. 22 2007 1182 1190
57. A.W. Zimmerman, H. Jyonouchi, A.M. Comi, S.L. Connors, S. Milstien, A. Varsou, and M.P. Heyes Cerebrospinal fluid and serum markers of inflammation in autism Pediatr. Neurol. 33 2005 195 201 (Pubitemid 41558217)