Synapse Replacement in the Striatum of the Adult Rat Following Unilateral Cortex Ablation

Journal of Comparative Neurology

Volumn 467, Issue 1, 2003, Pages 32-43

  McNeill, Thomas H ^a   Brown, Sally A ^a   Hogg, Elizabeth ^a   Cheng, Heng Wei ^a   Meshul, Charles K ^b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b PORTLAND VA MEDICAL CENTER   (United States)

Author keywords

Axons; Basal ganglia; Multiple synaptic boutons; Neuronal plasticity; Synapse

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; CORPUS STRIATUM; DENDRITIC SPINE; MALE; NERVE CELL PLASTICITY; NERVE ENDING; NERVE FIBER DEGENERATION; NEUROPIL; NONHUMAN; PRIORITY JOURNAL; RAT; REINNERVATION; SYNAPSE; ULTRASTRUCTURE;

ANIMALS; CEREBRAL CORTEX; CORPUS STRIATUM; DENDRITES; MALE; MICROSCOPY, ELECTRON; NERVE DEGENERATION; NERVE REGENERATION; NEURAL PATHWAYS; NEURONS; NEUROPIL; PRESYNAPTIC TERMINALS; RATS; RATS, INBRED F344; SYNAPSES; TIME FACTORS;

EID: 0242268618     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.10907     Document Type: Article

References (79)

1. Bouyer JJ, Park DH, Joh TH, Pickel VM. 1984. Chemical and structural analysis of the relation between cortical inputs and tyrosine hydroxylase-containing terminals in rat neostriatum. Brain Res 302:267-275.
2. Cepeda C, Levine MS. 1998. Dopamine and N-methyl-D-aspartate receptor interactions in the neostriatum. Dev Neurosci 20:1-18.
3. Cheng HW, Jiang T, Brown SA, Pasinetti GM, Finch CE, McNeill TH. 1994. Response of striatal astrocytes to neuronal deafferentation: an immunocytochemical and ultrastructural time course study. Neuroscience 62:425-439.
4. Cheng HW, Jiang T, Mori N, McNeill TH. 1997a. Upregulation of stathmin (p19) gene expression in adult rat brain during injury-induced synapse formation. Neuroreport 8:3691-3695.
5. Cheng HW, Rafols JA, Goshgarian HG, Anavi Y, Jiang T, McNeill TH. 1997b. Differential spine loss and regrowth of striatal neurons following multiple forms of deafferentation: a Golgi study. Exp Neurol 146:287-298.
6. Cheng HW, Jiang T, McNeill TH. 1998. Lesion-induced axon sprouting in the deafferented striatum of adult rat. Neurosci Lett 241:1-4.
7. Cospito JA, Kultas-Ilinsky K. 1981. Synaptic organization of motor corticostriatal projections in the rat. Exp Neurol 72:257-66.
8. Cotman CW, Nieto-Sampedro M, Harris EW. 1981. Synapse replacement in the nervous system of adult vertebrates. Physiol Rev 61:684-784.
9. Day JR, Laping NJ, McNeill TH, Schreiber SS, Pasinetti GM, Finch CE. 1990. Castration enhances expression of glial fibrillary acidic protein sulfated glycoprotein-2 in the intact and lesion-altered hippocampus of the adult male rat. Mol Endocrinol 4:1995-2002.
10. Desban M, Kemel ML, Glowinski J, Gauchy C. 1993. Spatial organization of patch and matrix compartments in the rat striatum. Neuroscience 57:661-671.
11. Difiglia M, Pasik T, Pasik P. 1978. A Golgi study of afferent fibers in the neostriatum of monkeys. Brain Res 152:341-347.
12. Donoghue JP, Herkenham M. 1986. Neostriatal projections from individual cortical fields conform to histochemically distinct striatal compartments in the rat. Brain Res 365:397-403.
13. Dube L, Smith AD, Bolam JP. 1988. Identification of synaptic terminals of thalamic or cortical origin in contact with distinct medium-size spiny neurons in the rat neostriatum. J Comp Neurol 267:455-471.
14. Feeney DM, Gonzalez A, Law WA. 1982. Amphetamine, haloperidol, and experience interact to affect of recovery after motor cortex injury. Science 21:855-857.
15. Feldman ML, Dowd C. 1975. Loss of dendritic spines in aging cerebral cortex. Anat Embryol 148:279-301.
16. Fiala JC, Allwardt B, Karris KM. 2002. Dendritic spines do not split during hippocampal LTP or maturation. Nat Neurosci 5:297-298.
17. Flores-Hernandez J, Cepeda C, Hernandez-Echeagaray E, Calvert CR, Jokel ES, Fienberg AA, Greengard P, Levine MS. 2002. Dopamine enhancement of NMDA currents in dissociated medium-sized striatal neurons: role of D1 receptors and DARPP-32. J Neurophysiol 88:3010-3020.
18. Freund TF, Powell JF, Smith AD. 1984. Tyrosine hydroxylase-immunoreactive boutons in synaptic contact with identified striatonigral neurons, with particular reference to dendritic spines. Neuroscience 13:1189-1215.
19. Geinisman Y, Gundersen HJG, Van Der Zee E, West MJ. 1996. Unbiased stereological estimation of the total number of synapses in a brain region. J Neurocytol 25:805-819.
20. Gerfen CR. 1992. The neostriatal mosaic: multiple levels of compartmental organization in the basal ganglia. Annu Rev Neurosci 15:285-320.
21. Gerfen CR, Wilson CJ. 1996. The basal ganglia. In: Swanson LW, Bjorklund A, Hokfelt T, editors. Handbook of chemical neuroanatomy. Vol 12. Amsterdam: Elsevier. p 371-468.
22. Gerfen CR, Baimbridge KG, Miller JJ. 1985. The neostriatal mosaic: compartmental distribution of calcium-binding protein and parvalbumin in the basal ganglia of the rat and monkey. Proc Natl Acad Sci U S A 82:8780-8784.
23. Glaser ME, Van der Loos H. 1981. Analysis of thick brain sections by obverse-reverse computer microscopy: application of a new, high clarity Golgi-Nissl stain. J Neurosci Methods 4:117-125.
24. Goldstein LB. 1993a. Beam-walking in rats: the measurement of motor recovery after injury to the cerebral cortex. Neurosci Protoc 10:1-13.
25. Goldstein LB. 1993b. Rapid and reliable measurement of lesion parameters for studies of motor recovery after sensorimotor cortex injury in rats. J Neurosci Methods 48:35-42.
26. Goldstein LB. 1993c. Basic and clinical studies of pharmacologic effects on recovery from brain injury. J Neural Transplant Plast 4:175-192.
27. Gray EG, Guillery RW. 1966. Synaptic morphology in the normal and degenerating nervous system. Int Rev Cytol 19:111-182.
28. Graybiel AM, Ragsdale CW. 1983. Biochemical anatomy of the striatum. In: Emson PC, editor. Chemical neuroanatomy. New York: Raven Press. p 317-504.
29. Guillery RW. 1970. Light- and electron-microscopic studies in normal and degenerating axons. In: Nauta WJH, Ebbesson SOE, editors. Contemporary research methods in neuroanatomy. New York: Springer. p 77-105.
30. Gundersen HJG, Jensen EB. 1987. The efficiency of systematic sampling in stereology and its prediction. J Microsc 147:229-263.
31. Gundersen HJG, Bagger P, Bendtsen TF, Evans SM, Korbo L, Marcussen N, Moller AM, Nielsen K, Nyengaard JR, Pakkenberg B, Sorensen F, Vesterby A, West MJ. 1988. The new stereological tool: disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. Acta Pathol Microbiol Scand 96:374-394.
32. Harris KM. 1995. How multiple-synapse boutons could preserve input specificity during an interneuronal spread of LTP. Trends Neurosci 18:365-369.
33. Higo N, Oishi T, Yamashita A, Matsuda K, Hayashi M. 2000. Expression of GAP-43 and SCG-10 mRNAs in the lateral geniculate nucleus of normal and monocularly deprived macaque moneys. J Neurosci 20:6030-6038.
34. Hokfelt T, Ungerstedt U. 1973. Specificity of 6-hydroxydopamine induced degeneration of central monoamine neurons: an electron and fluorescence microscopic study with special reference to intracerebral injection of the nigrostriatal dopamine system. Brain Res 60:269-297.
35. Howard CV, Reed MG. 1998. Unbiased stereology: three-dimensional measurement in microscopy. New York: BIOS Scientific.
36. Jones TA. 1999. Multiple synapse formation in the motor cortex oppisite unilateral sensorimotor cortex lesions in adult rats. J Comp Neurol 414:57-66.
37. Jones TA, Schallert T. 1992. Subcortical deterioration after cortical damage: effects of diazepam and relation to recovery of function. Behav Brain Res 51:1-13.
38. Jones TA, Klintsova AY, Kilman VL, Sirevaag AM, Greenough WT. 1997. Induction of multiple synapses by experience in the visual cortex of adult rats. Neurobiol Learn Mem 68:13-20.
39. Jones TA, Chu CJ, Grande LA, Gregory AD. 1999. Motor skills training enhances lesion-induced structural plasticity in the motor cortex of adult rats. J Neurosci 19:10153-10163.
40. Kartje GL, Schulz MK, Lopez-Yunez A, Schnell L, Schwab ME. 1999. Corticostriatal plasticity is restricted by myelin-associated neurite growth inhibitors in the adult rat. Ann Neurol 45:778-786.
41. Kemp JM, Powell TPS. 1971. The structure of the caudate nucleus in the cat: light and electron microscopy. Philos Trans R Soc Lond B Biol Sci 262:383-401.
42. Kincaid AE, Wilson CJ. 1996. Corticostriatal innervation of the patch and matrix in the rat neostriatum. J Comp Neurol 374:578-592.
43. Kitai ST, Kocsis JD, Wood J. 1976. Origin and characteristics of the corticocaudate afferents: an anatomical and electrophysiological study. Brain Res 118:137-141.
44. Matthews DA, Cotman C, Lynch G. 1976. An electron microscopic study of lesion-induced synaptogenesis in the dentate gyrus of the adult rat. I. Magnitude and time course of degeneration. Brain Res 115:1-21.
45. May PC, Finch CE. 1992. Sulphated glycoprotein-2: new relationship of this multifunctional protein to neurodegeneration. Trends Neurosci 15:391-396.
46. McGeorge AJ, Faull RLM. 1987. The organization of the projection from the cerebral cortex to the striatum in the rat. Neuroscience 29:503-537.
47. McNeill TH, Koek L, Brown SA, Rafols JA. 1990. Quantitative analysis of age-related dendritic changes in medium spiny I (MSI) striatal neurons of C57BL/6N mice. Neurobiol Aging 11:537-550.
48. McNeill TH, Mori N, Cheng HW. 1999. Differential regulation of the growth associated proteins GAP-43 and SCG-10 in response to unilateral cortex ablation in adult rats. Neuroscience 90:1349-1360.
49. McWilliams R, Lynch G. 1979. Terminal proliferation in the partially deafferented dentate gyrus: time course for the appearance and removal of degeneration and replacement of lost terminals. J Comp Neurol 187:191-198.
50. Meshul CK, Cogen JP, Cheng HW, Moore C, Krentz L, McNeill TH. 2000. Alterations in rat striatal glutamate synapses following a lesion of the cortico- and/or nigrostriatal pathway. Exp Neurol 165:191-206.
51. Napieralski JA, Butler AK, Chesselet MF. 1996. Anatomcial and functional evidence for lesion-specific sprouting of corticostriatal input in the adult rat. J Comp Neurol 373:484-497.
52. Page KJ, Hollister RD, Hyman BT. 1998. Dissociation of apolipoprotein and apolipoprotein receptor response to lesion in the rat brain: an in situ hybridization study. Neuroscience 85:1161-1171.
53. Pasinetti GM, Cheng H-W, Reinhard JF, Finch CE, McNeill TH. 1991. Molecular and morphological correlates following deafferentation. Adv Exp Biol Med 296:249-255.
54. Pasinetti GM, Cheng HW, Morgan DG, Lampert-Etchells M, McNeill TH, Finch CE. 1993. Astrocytic messenger RNA responses to striatal deafferentation in male rats. Neuroscience 53:199-211.
55. Paxinos G, Watson C. 1997. The rat brain in stereotaxic coordinates, 3rd ed. San Diego: Academic Press.
56. Peters A, Kaiserman-Abramof IR. 1970. The small pyramidal neuron of the rat cerebral cortex. The perikaryon, dendrites and spines. Am J Anat 127:321-356.
57. Poirier J, May PC, Osteburg HH, Geddes J, Cotman C, Finch CE. 1990. Selective alterations of RNA in rat hippocampus after entorhinal cortex lesioning. Proc Natl Acad Sci U S A 87:303-307.
58. Poirier J, Hess M, May PC, Finch CE. 1991. Astrocytic apolipoprotein E mRNA and GFAP mRNA in the hippocampus after entorhinal cortex lesioning. Brain Res Mol Brain Res 11:97-106.
59. Rafols JA, Cheng HW, McNeill TH. 1989. Golgi study of the mouse striatum: age-related dendritic changes in different neuronal populations. J Comp Neurol 279:212-227.
60. Ramon-Moliner E. 1970. The Golgi-Cox technique. In: Nauta WJH, Ebbesson SOE, editors. Contemporary research methods in neuroanatomy. New York: Springer. p 32-55.
61. Riederer BM, Pellier V, Antonsson B, Di Paolo G, Stimpson SA, Lutjens R, Catsicas S, Grenningloh G. 1997. Regulation of microtubule dynamics by the neuronal growth-associated protein SCG-10. Proc Natl Acad Sci U S A 94:741-745.
62. Salin P, Chesselet M-F. 1992. Paradoxical increase in striatal neuropeptide gene expression following ischemic lesions of the cerebral cortex. Proc Natl Acad Sci U S A 89:9954-9958.
63. Schauwecker PE, Cogen JP, Jiang T, Cheng HW, Collier TJ, McNeill TH. 1998. Differential regulation of astrocytic mRNAs in the rat striatum after lesions of the cortex or substantia nigra. Exp Neurol 149:87-96.
64. Smith AD, Bolam JP. 1990. The neural network of the basal ganglia as revealed by the study of synaptic connections of identified neurons. Trends Neurosci 13:259-265.
65. Smith Y, Bennett BD, Bolam JP, Parent A, Sadikot AF. 1994. Synaptic relationship between dopaminergic afferents and cortical or thalamic input in the sensorimotor territory of the striatum in monkey. J Comp Neurol 344:1-19.
66. Snyder SE, Cheng HW, Murray KD, Isackson PJ, McNeill TH, Salton SRJ. 1998. The mRNA encoding VGF, a neuronal peptide precursor, is rapidly regulated in the rat central nervous system by neuronal activity, seizure and lesion. Neuroscience 82:7-19.
67. Somogyi P, Bolam JP, Smith AD. 1981. Monosynaptic cortical input and local axon collaterals of identified striatonigral neurons. A light and electron microscopic study using the Golgi-peroxidase, transport-degeneration procedure. J Comp Neurol 195:567-584.
68. Sorra KE, Harris KM. 1993. Occurrence and three-dimensional structure of multiple synapses between individual radiatum axons and their target pyramidal cells in the hippocampal area CA1. J Neurosci 13:3736-3748.
69. Steward O. 1991. Synaptic replacement on cortical neurons following denervation. In: Peters A, Jones EG, editors. Cerebral cortex, vol 9. New York: Plenum Press. p 81-132.
70. Szele FG, Alexander C, Chesselet M-F. 1995. Expression of molecules associated with neuronal plasticity in the striatum after aspiration and thermocoagulatory lesions of the cerebral cortex in adult rats. J Neurosci 15:4429-4448.
71. Szentagothai J. 1963. The structure of the synapse in the lateral geniculate body. Acat Anat 5:166-185.
72. Toni N, Buchs PA, Nikonenko I, Bron CR, Muller D. 1999. LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature 402:421-425.
73. Uryu K, Mackenzie L, Chesselet MF. 2001. Ultrastructural evidence for differential axonal sprouting in the striatum after thermocoagulatory and aspiration lesions of the cerebral corex in adult rats. Neuroscience 105:307-316.
74. Valverde F. 1970. The Golgi method. A tool for comparative structural analysis. In: Nauta WJH, Ebbesson SOE, editors. Contemporary research methods in neuroanatomy. New York: Springer. p 12-31.
75. Weibel ER. 1979. Practical methods for biological morphometry. In: Parsons DF, editor. Stereological methods. New York: Academic Press.
76. Wilson CJ. 1987. Morphology and synaptic connections of crossed corticostriatal neurons in the rat. J Comp Neurol 263:567-580.
77. Woolley CS, Wenzel HJ, Schwartzkroin PA. 1996. Estradiol increases the frequency of multiple synapse boutons in the hippocampal CA1 region of the adult female rat. J Comp Neurol 373:108-117.
78. Xu ZC, Wilson CL, Emson PC. 1989. The restoration of the corticostriatal projection in rat neostriatal grafts: electron microscopic analysis. Neuroscience 29:539-550.
79. Yankova M, Hart SA, Woolley CS. 2001. Estrogen increases synaptic connectivity between single presynaptic inputs and multiple postsynaptic CA1 pyramidal cells: a serial electron-microscopic study. Proc Natl Acad Sci U S A 98:3525-3530.