Summary
High affinity glutamate uptake into corticofugal fiber terminals was measured in the ventrolateral thalamus and red nucleus at varying time intervals after lesions were made by kainic acid in the contralateral interpositus nucleus of the cerebellum in rats. Under similar conditions the density of cortical fiber terminals was estimated using the Fink-Heimer impregnation technique. 1. Glutamate uptake steadily increased in the ventrolateral thalamus up to 60 days after lesions in the contralateral cerebellum. 2. Similar changes were noted in the red nucleus. 3. The changes were dependent on the integrity of corticofugal fibers to the thalamus and red nucleus. 4. No changes in uptake of gammaaminobutyric acid were noted. 5. Saturation curves for glutamate uptake suggested a change in the maximal number of transport sites. 6. Fink-Heimer degeneration studies showed an increase in cortical terminals in the ipsilateral ventrolateral thalamus and in both rostral and caudal regions of the red nucleus following lesions in the contralateral interpositus nucleus. The data are consistent with an increase in the number of cortical fiber terminals in reaction to loss of cerebellar input to the ventrolateral thalamus and red nucleus. This study correlates anatomical and biochemical evidence for collateral sprouting in a model based on electrophysiologic data in the red nucleus and extends the model to include the thalamus.
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References
Bromberg MB, Gilman S (1978) Changes in rubral multiunit activity after lesions in the interpositus nucleus in the cat. Brain Res 152: 353–357
Bromberg MB, Penney JB, Stephenson BS, Young AB (1981) Evidence for glutamate as the neurotransmitter of corticothalamic and corticorubral pathways. Brain Res 215: 369–374
Brown LT (1974) Corticorubral projections in the rat. J Comp Neurol 154: 149–168
Cajal RS (1911) Histologie du systéme nerveux de l'homme et des vertébrés, Vol II. Maloine, Paris
Caughell KA, Flumerfelt BA (1977) The organization of the cerebellorubral projection: An experimental study in the rat. J Comp Neurol 176: 295–306
Fink RP, Heimer L (1967) Two methods for selective impregnation of degenerating axons and their synaptic endings in the central nervous system. Brain Res 4: 369–374
Gwyn DG, Flumerfelt BA (1974) A comparison of the distribution of cortical and cerebellar afferents in the red nucleus of the rat. Brain Res 69: 130–135
Kerkerian L, Nieoullon A, Dusticier N (1982) Brain glutamate uptake: regional distribution study from sensorimotor areas in the cat. Neurochem Int 4: 275–281
Kerkerian L, Nieoullon A, Dusticier N (1984) Topographical changes in high affinity glutamate uptake from the cat red nucleus, substantia nigra, thalamus and caudate nucleus following lesions of sensorimotor cortical areas. Exp Neurol 81: 598–612
McGeer PL, McGeer EG, Hattori T (1978) Kainic acid as a tool in neurobiology. In: McGeer EG, Olney JW, McGeer PL (eds) Kainic acid as a tool in neurobiology. Raven Press, New York, pp 123–138
Murakami F, Katsumaru H, Saito K, Tsukahara N (1982) A quantitative study of synaptic reorganization in red nucleus neurons after lesion of the nucleus interpositus of the cat: an electron microscopic study involving intracellular injection of horseradish peroxidase. Brain Res 242: 41–53
Nakamura Y, Mizuno N (1971) An electron microscopic study of the interpositorubral connections in the cat and rabbit. Brain Res 35: 283–286
Nakamura Y, Mizuno N, Konishi A, Sato M (1974) Synaptic reorganization of the red nucleus after chronic deafferentation from cerebellorubral fibers: an electron microscope study in the cat. Brain Res 82: 298–301
Nieoullon A, Dusticier N (1981) Increased glutamate decarboxylase activity in the red nucleus of the adult cat after cerebellar lesions. Brain Res 224: 129–139
Nieoullon A, Kerkerian L, Dusticier N (1984) High affinity glutamate uptake in the red nucleus and ventrolateral thalamus after lesion of the cerebellum in the adult cat: biochemical evidence for functional changes in the deafferented structures. Exp Brain Res 55: 409–419
Olney JW, de Gubareff T (1978) Extreme sensitivity of olfactory cortical neurons to kainic acid toxicity. In: McGeer EG, Olney JW, McGeer PL (eds) Kainic acid as a tool in neurobiology. Raven Press, New York, pp 201–217
Pamel G, Stephenson B, Penney JB, Bromberg MB, Young AB (1981) Biochemical evidence for sprouting of corticothalamic fibers after interpositus nucleus lesions in rat. Neurology 31: 150
Steward O (1982) Assessing the functional significance of lesion-induced neuronal plasticity. Int Rev Neurobiol 23: 197–254
Tsukahara N, Hultborn H, Murakami F, Fujito Y (1975) Electrophysiological study of formation of new synapses and collateral sprouting in red nucleus after partial denervation. J Neurophysiol 38: 1359–1374
Tsukahara N (1978) Synaptic plasticity in the red nucleus. In: Cotman CW (ed) Neuronal plasticity. Raven Press, New York, pp 113–130
Young AB, Bromberg MB, Penney JB (1981) Decreased glutamate uptake in subcortical areas deafferented by sensorimotor cortical ablation in the cat. J Neurosci 1: 241–249
Young AB, Penney JB, Dauth GW, Bromberg MB, Gilman S (1983) Glutamate or aspartate as a possible neurotransmitter of cerebral corticofugal fibers in the monkey. Neurology 33: 1513–1516
Young AB, Frey KA, Agranoff BW (1986) Receptor assays: in vitro and in vivo. In: Phelps M, Mazziotta J, Schelbert H (eds) Positron emission tomography and autoradiography: principles and applications for the brain and heart. Raven Press, New York, pp 73–111
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Bromberg, M.B., Pamel, G., Stephenson, B.S. et al. Evidence for reactive synaptogenesis in the ventrolateral thalamus and red nucleus of the rat: changes in high affinity glutamate uptake and numbers of corticofugal fiber terminals. Exp Brain Res 69, 53–59 (1987). https://doi.org/10.1007/BF00247028
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DOI: https://doi.org/10.1007/BF00247028