Sexual dimorphism in cerebellar structure, function, and response to environmental perturbations

Progress in Brain Research

Volumn 148, Issue , 2005, Pages 341-351

  Nguon, K ^a   Ladd, B ^a   Baxter, M G ^b   Sajdel Sulkowska, E M ^a,c  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

cerebellum; environmental impacts; female; hypergravity; male; PCBs; rat; sex differences

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; NERVE CELL ADHESION MOLECULE L1; POLYCHLORINATED BIPHENYL;

BEHAVIOR; BRAIN DEVELOPMENT; BRAIN FUNCTION; BRAIN WEIGHT; CEREBELLUM; DISEASE PREDISPOSITION; ENVIRONMENTAL FACTOR; FEMALE; GENE EXPRESSION; HUMAN; MALE; MENTAL DISEASE; MOLECULAR MECHANICS; MOTOR COORDINATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PHYSICAL ACTIVITY; PRIORITY JOURNAL; REVIEW; SEX DIFFERENCE;

EID: 12344251554     PISSN: 00796123     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0079-6123(04)48027-3     Document Type: Review

References (83)

1. Abdel-Rahman A., Dechkoskaia A., Mehta-Simmons H., Guan X., Khan W., Abou-Donia M. Increased expression of glial fibrillary acidic protein in cereberllum and hippocampus: differential effects on neonatal brain regional acetylcholinesterase following maternal exposure to combined chlorpyrifos and nicotine. J. Toxicol. Environ. Health. 66:2003;2047-2066
2. Asou H., Miura M., Kobayashi M., Uyemura K. The cell adhesion molecule L1 has specific role in neural cell migration. Neuroreport. 3:1992;481-484
3. Auger A.P. Sex differences in the developing brain: crossroads in the phosphorylation of cAMP response element binding protein. J. Neuroendocrinol. 15:2001;622-627
4. Baird G., Charman T., Baron-Cohen S., Cao C., Ashton-Miller J.A., Schutz A.B., Alexander N.B. Abilities to turn suddenly while walking: effects of age, gender, and available response time. J. Gerontol. A. Biol. Sci. Med. Sci. 52:1997;M88-M93
5. Baird, G., Charman, T., Baron-Cohen, S., Cox, A., Swettenham, J., Wheelwright, S. and Drew, A. (2001) A screening instrument for austim at 18 months of age; a 6-year follow-up study. J. Am. Acad. Child Adolesc. Psychiatry, 40: 737-738
6. Cao, C., Ashton-Miller, J.A., Schultz, A.B. and Alexander, N.B. (1997) Abilities to turn suddenly while walking: effects of age, gender, and available response time. J. Gerontol. A. Biol. Sci. Med. Sci., 52: M88-93
7. Chakrabarti S., Fombonne E. Pervasive developmental disorders in preschool children. JAMA. 285:2001;3141-3142
8. Ciesielski K.T., Harris R.J., Hart B.L., Pabst H.F. Cerebellar hypoplasia and frontal lobe cognitive deficits in disorders of early childhood. Neuropsychologia. 35:1997;643-655
9. Courchesne E. Neuroanatomic imaging in autism. Pediatrics. 87:1991;781-790
10. Courchesne E., Yeung-Courchesne R., Press G.A., Hesselink J.R., Jernigan T.L. Hypoplasia of cerebellar vermal lobules VI and VII in autism. N. Engl. J. Med. 318:1988;1349-1354
11. Courchesne E., Saitoh O., Yeung-Courchesne R., Press G.A., Lincoln A.J., Haas R.H., Schreibman L. Abnormality of cerebellar vermian lobules VI and VII in patients with infantile autism: identification of hypoplastic and hyperplastic subgroups with MR imaging. Am. J. Roentgenol. 162:1994;123-130
12. Courchesne E., Karns C.M., Davis H.R., Ziccardi R., Carper R.A., Tigue Z.D., Chisum H.J., Moses P., Pierce K., Lord C., Lincoln A.J., Pizzo S., Schreibma L., Haas R.H., Akshoomoff N.A., Courchesne R.Y. Unusual brain growth patterns in early life in patients with autistic disorder: an MRI study. Neurology. 57:2001;245-254
13. Courchesne E., Carper R., Akshoomoff N. Evidence of brain overgrowth in the first year of life in autism. JAMA. 290:2003;337-344
14. Crofton K.M., Kodavanti P.R., Derr-Yellin E.C., Casey A.C., Kehn L.S. PCBs, thyroid hormones, and ototoxity in rats: cross-fostering experiments demonstrate the impact of postnatal lactation exposure. Toxicol. Sci. 57:2000;131-140
15. Dam K., Seidler F.J., Slotkin T.A. Chlorpyrifos exposure during a critical neonatal period elicits gender-selective deficits in the development of coordination skill and locomotor activity. Brain Res. Dev. Brain. Res. 121:2000;179-187
16. de Cabo C., Paz Viveros M. Effects of neonatal naltrexone on neurological and somatic development in rats of both genders. Neurotoxicol. Teratol. 19:1997;499-509
17. Elsinger C.L., Rao S.M., Zimbelman J.L., Reynolds N.C., Blindauer K.A., Hoffman R.G. Neural basis for impaired time reproduction in Parkinson's disease: fMRI studies. J. Int. Neuropsychol. Soc. 9:2003;1088-1098
18. Faivre-Sarrailh C., Rami A., Fages C., Tardy M. Effect of thyroid deficiency on glial fibrillary acidic protein (GFAP) and GFAP-mRNA in the cerebellum and hippocampal formation of the developing rat. Glia. 4:1991;276-284
19. Fatemi S.H., Halt A.R., Stary J.M., Realmuto G.M., Jalali-Mousavi M. Reduction in anti-apoptotic protein Bcl-2 in autistic cerebellum. Neuroreport. 12:2001;929-933
20. Ferguson S.A., Paule M.G., Holson R.R. Functional effects of methylazoxymethanol-induced cerebellar hypoplasia in rats. Neurotoxicol. Teratol. 18:1996;529-537
21. Gaab N., Keenan J.P., Schlaug G. The effects of gender on the neural substrates of pitch memory. J. Cogn. Neurosci. 15:2003;810-820
22. Gaffney G.R., Tsai L.Y., Kuperman S., Minchin S. Cerebellar structure in autism. Am. J. Dis. Child. 141:1987;1330-1332
23. Goldey, E.S., Kehn, L.S., Rehnberg, G.L. and Crofton, K.M. (1995) Effects of developmental hypothyroidism on auditory and motor function in the rat. Toxicol. Appl. Pharmacol., 135: 67-76
24. Goldey, E.S. and Crofton, K.M. (1998) Thyroxine replacement attenuates hypothyroxinemia, hearing loss, and motor deficits following developmental exposure to Aroclor 1254 in rats. Toxicol. Sci., 45: 94-105
25. Gotohda T., Kuwada A., Morita K., Kubo S., Tokunaga I. Elevation of steroid 5 alpha-reductase mRNA levels in rat cerebellum by toluene inhalation: possible relation to GFAP expression. J. Toxicol. Sci. 25:2002;223-231
26. Guerra Araiza C., Coyoy-Salgado A., Camacho-Arroyo I. Sex differences in the regulation of progesterone receptor isoforms expression in the rat brain. Brain Res. Bull. 59:2002;105-109
27. Hadj-Sahraoui N., Frederic F., Delhaye-Bouchaud N., Mariani J. Gender effect on Purkinje cell loss in the cerebellum of the heterozygous reeler mouse. J. Neurogenet. 11:1996;45-58
28. Hany J., Lilienthal H., Roth-Harer A., Ostendorp G., Heizow B., Winneke G. Behavioral effects following single and combined maternal exposure to PCB 77 (3,4,3′,4′-tetrachlorobiphenyl) and PCB 47 (2,4,2′,4′- tetrachlorobiphenyl) in rats. Neurotoxicol. Teratol. 21:1999;147-156
29. Hashimoto T., Tayama M., Miyazaki M., Kuroda Y. Brainstem and cerebellar vermis involvement in autistic children. J. Child. Neurol. 8:1993;149-153
30. Hashimoto T., Tayama M., Miyazaki M., Kuroda Y. MRI measurements of the brain stem and cerebellum in high functioning autistic children. No. To. Hattatsu. 26:1994;3-8
31. Hatten M.E., Mason C.A., Liem R.K., Edmondson J.C., Bovolenta P., Shelanski M.L. Neron-astroglial interactions in vitro and their implications for repair of CNS injury. Cent. Nerv. Syst. Trauma. 1:1984;15-27
32. Heh C.W., Smith R., Wu J., Hazlett E., Asarnow R., Tanguay P., Buchsbaum M.S. Positron emission tomography of the cerebellum in autism. Am. J. Psychiatry. 146:1989;242-245
33. Ignelzi M.A. Jr., Miller D.R., Soriano P., Manes P.F. Impaired neurite outgrowth of src-minus cerebellar neurons on the cell adhesion molecule L1. Neuron. 12:1994;873-884
34. Johnson W.T., Prohaska J.R. Gender influences the effect of perinatal copper deficiency on cerebellar PKC gamma content. Biofactors. 11:2000;163-169
35. Juraska J.M. Gender differences in the dendritic tree of granule neurons in the hippocampal dentate gyrus of weaning age rats. Brain Res. Dev. Brain Res. 53:1990;291-294
36. Kaya H., Hany J., Fastbend A., Roth-Harer A., Winneke G., Lilienthal H. Effects of maternal exposure to a reconstituted mixture of polychlorinated biphenyls on sex-dependent behaviors and steroid hormone concentrations in rats: dose-response relationship. Toxicol. Appl. Pharmacol. 178:2002;71-81
37. Keilhauer G., Faissner A., Schachner M. Differential inhibition of nerone-neurone, neurone-astrocyte and astrocyte-astrocyte adhesion by L1, L2 and NCAM antibodies. Nature. 316:1985;728-730
38. Kemper T.L., Bauman M.L. The contribution of neuropathologic studies to the understanding of autism. Neurol. Clin. 11:1993;175-187
39. Kettenmann H., Wienrich M., Schachner M. Antibody L1 ejected from a micropipette identifies neurons without electrical activity. Neurosci. Lett. 41:1983;85-90
40. Konkle A.T., Baker S.L., Kenter A.C., Barbagallo L.S., Merali Z., Bielajev C. Evaluation of the effects of chronic mild stressors on hedonic and physiological responses: sex and strain compared. Brain Res. 992:2003;227-238
41. Levitt J.G., Blanton R., Capetillo-Cunliffe L., Guthrie D., Toga S.A., McCracken J.T. Cerebellar vermis lobules VIII-X in autism. Prog. Neuropsychopharmacol. Biol. Psychiatry. 23:1999;625-633
42. Li G.-H., Post J., Koibuchi N., Sajdel-Sulkowska E.M. Effect of thyroid hormone deficiency on the expression of glial and neuronal proteins in the developing rat cerebellum. Cerebellum. 3:2004;100-106
43. Liljelund P., Ghosh P., van den Pol A.N. Expression of the neuronal molecule L1 in the developing and adult rat brain. J. Biol. Chem. 268:1994;32886-32895
44. Markowski V.P., Cox C., Weiss B. Prenatal cocaine exposure produces gender-specific motor effects in aged rats. Neurotoxicol. Teratol. 20:1998;43-53
45. Mason C.A., Edmondson J.C., Hatten M.E. The extending astroglial process: development of glial shape in the growing tip, and interactions with neurons. J. Neurosci. 8:1988;3124-3134
46. Matsumoto, Y., Noji, S. and Mizunami, M. (2003) Time course of protein synthesis-dependent phase of olfactory memory in the cricket Gryllus bimacultus. Zoolog. Sci., 20: 409-416
47. Matsumoto-Miyai K., Ninomiya A., Yamasaki H., Tamura H., Nakamura Y., Shiosaka S. NMDA-dependent proteolysis of presynaptic adhesion molecule L1 in the hippocampus by neropsin. J. Neurosci. 23:2003;7727-7736
48. Mayhew T.M., MacLaren R., Henery C.C. Fractionator studies on Purkinje cells in human cerebellum: numbers in right and left halves of male and female brains. J. Anat. 169:1990;63-70
49. McFadyen M.P., Kusek G., Bolivar V.J., Flaherty L. Differences among eight inbred strains of mice in motor ability and motor learning on a rotorod. Genes. Brain Behav. 2:2003;214-219
50. Mwamengele G.L., Mayhew T.M., Dantzer V. Purkinje cell complements in mammalian cerebella and the biases incurred by counting nucleoli. J. Anat. 183:1993;155-160
51. Morse D.C., Plug A., Wesseling W., van den Berg K.J., Brouwer A. Persistent alterations in regional brain fibrillary acidic protein and synaptophysin levels following pre- and postnatal polychlorinated biphenyl exposure. Toxicol. Appl. Pharmacol. 139:1996;252-261
52. Moulding H.D., Martuza R.L., Rabkin S.D. Clinical mutations in the L1 neural cell adhesion molecule affect cell-surface expression. J. Neurosci. 20:2000;5696-5702
53. Murakami, J.W., Courchesne, E., Press, G.A., Yeung-Courchesne, R. and Hesseling, J.R., Arch. Neurol., 46: 689-69
54. Nguon, K., Li, G.-H. and Sajdel-Sulkowska, E.M. (2004) CNS development under altered gravity: cerebellar glial and neuronal protein expression in rat neonates exposed to hypergravity. Adv. Space Res. (in press).
55. Pierce K., Courchesne E. Evidence for a cerebellar role in reduced exploration and stereotyped behavior. Biol. Psych. 49:2001;655-664
56. Porterfield S.P., Hendrich C.E. The role of thyroid hormones in prenatal and neonatal neurological development-current perspectives. Endocr. Rev. 14:1993;94-106
57. Quadros P.S., Lopez V., De Vries G.J., Chung W.C., Wagner C.K. Progesterone receptors and the sexual differentiation of the medial preoptic nucleus. J. Neurobiol. 51:2002;24-32
58. Ramirez O., Jimenez E. Sexual dimorphism in rat cerebrum and cerebellum: different patterns of catalitycally active creatine kinase isoenzymes during postnatal development and aging. Int. J. Dev. Neurosci. 20:2002;627-639
59. Raz N., Gunning-Dixon F., Head D., Williamson A., Acker J.D. Age and sex differences in the cerebellum and the ventral pons: prospective MR study of healthy adults. AJNR Am. J. Neuroradiol. 22:2001;1161-1167
60. Rhees R.W., Lephart E.D., Eliason D. Effects of maternal separation during early postnatal development on male sexual behavior and female reproductive function. Behav. Brain Res. 123:2001;1-10
61. Rhyu I.J., Cho T.H., Lee N.J., Uhm C.S., Kim H., Suh Y.S. Magnetic resonance image-based cerebellar volumetry in health Korean adults. Neurosci. Lett. 270:1999;149-152
62. Rintala J., Jaatinen P., Kiianmaa K., Iikonen J., Kemppainen O., Sarviharju M., Hervonen A. dose-dependent decrease in glial fibrillary acidic protein-immunoreactivity in rat cerebellum after lifelong ethanol consumption. Alcohol. 23:2001;1-8
63. Rivto E.R., Freeman B.J., Scheibel A.B., Duong T., Robinson H., Guthrie D., Ritvo A. 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
64. Rutter M., Caspi A., Moffitt T. Using sex differences in psychopathology to study causal mechanisms: unifying issues and research strategies. J. Child Psychol. Psychiatry. 44:2003;1092-1115
65. Sajdel-Sulkowska E.M., Li G.-H., Ronca A.E., Baer L.A., Sulkowski G.M., Koibuchu N., Wade C.E. Effects of hypergravity exposure on the developing central nervous system: possible involvement of thyroid hormone. Exp. Biol. Med. 226:2001;790-798
66. Sajdel-Sulkowska E.M., Koibuchi N. Impact of thyroid status-disrupting environmental factors on brain development. Recent Res. Devel. Endocr. 3:2002;101-117
67. Sakamoto H., Mezaki Y., Shikimi H., Ukena K., Tsutsui K. Dendritic growth and spine formation in response to estrogen in the developing Purkinje cell. Endocrinology. 1444:2003;4466-4477
68. Schmahmann J.D. An emerging concept. The cerebellar contribution to higher function. Arch. Neurol. 48:1991;1178-1187
69. Scott F.J., Baron-Cohen S., Bolton P., Brayne C. Brief report: prevalence of autism spectrum conditions in children aged 5-11 years in Cambridgeshire, UK. Autism. 6:2002;231-237
70. Sedykh A.I., Leshchinskaia I.A., Duka T.I., Nerush P.A., Pavlov V.A. Effect of chronic emotional stress and low dose ethanol on the level of neuronal cell adhesion molecule and glail fibrillary acidic protein in rat brain. Ukr. Biokhim. Zh. 71:1999;97-103
71. Seo, B.W., Li, M.H., Hansen, L.G., Moore, R.W., Peterson, R.E. and Schantz, S.L. (1995) Effects of gestational and lactational exposure to coplanar polychlorinated biphenyl (PCB) congeners or 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on thyroid hormone concentrations in weanling rates. Toxicol Lett., 78: 253-262
72. Steward O., Kelley M.S., Torre E.R. The process of reinnervation in the dentate gyrus of adult rats: temporal relationship between changes in the levels of glial fibrillary acidic protein (GFAP) and GFAP mRNA in reactive astrocytes. Exp. Neurol. 124:1993;1676-1683
73. Suarez I., Bodega G., Rubio M., Fernandez B. Sexual dimorphism in the hamster cerebellum demonstrated by glial fibrillary acidic protein (GFAP) and vimentin. Glia. 5:1992;10-16
74. Sulkowski G.M., Li G.-H., Sajdel-Sulkowska E.M. Environmental impacts on the developing CNS: CD15, NCAM-L1, and GFAP expression in rat neonates exposed to hypergravity. Adv. Space Res. 33:2004;1423-1430
75. Sun X.Z., Zhang R., Cui C., Takahashi S., Kubota Y., Sawada K., Fukui Y. Expression of neural cell adhesion molecule L1 in the brain of rats exposed to X-irradiation in utero. J. Med. Invest. 50:2003;187-191
76. Thelen, K., Kedar, V., Panicker, A.K., Schmid, R.S., Midkiff, B.R. and Maness, P.F. (2002) The neural cell adhesion molecule L1 potentiates integrin-dependent cell migration to extracellular matrix protein. J. Neurosci., 22: 4918-4931
77. Toran-Allerand C.D., Bentham W., Miranda R.C., Anderson J.P. Insulin influences astroglial morphology and glial fibrillary acidic protein (GFAP) expression in organotypic cultures. Brain Res. 558:1991;296-304
78. Townsend J., Corchesne E., Covington J., Westerfield M., Harris N.S., Lyden P., Lowry T.P., Press G.A. Spatial attention deficits in patients with acquired developmental cerebellar abnormality. J. Neurosci. 19:1999;5632-5643
79. Trevarthen C. Autism as neurodevelopmental disorder affecting communication and learning in early childhood: prenatal origins, postnatal course and effective educational support. Prostglandins Leukot. Essent. Fatty Acids. 6:2000;41-46
80. Van Den Eaden S.K., Tanner C.M., Bernstein A.L., Fross R.D., Leimpeter A., Bloch D.A., Nelson L.M. Incidence of Parkinson's disease: variation by age, gender, and race/ethnicity. Am. J. Epidemiol. 157:2003;1015-1022
81. Vicedomini J.P., Nonneman A.J., DeKosky S.T., Scheff S.W. Perinatal glucocorticoids disrupt learning: a sexually dimorphic response. Physiol. Behav. 36:1986;145-149
82. Volkov N.D., Wang G.J., Fowler J.S., Hitzemann R., Pappas N., Pascani K., Wong C. Gender differences in cerebellar metabolism: test-retest reproducibility. Am. J. Psychiatry. 154:1997;119-121
83. Yamasaki, M., Sasaki, T. and Torii, M. (1991) Sex difference in the pattern of lower limb movement during treadmill walking. Eur. J. Appl. Physiol. Occup. Physiol., 62: 99-103