Summary
High affinity glutamate uptake (HAGU) was measured within the red nucleus (RN) and the ventrolateral thalamic area in intact adult cats and in animals which had undergone a large hemicerebellectomy 8 to 21 days before. In the side contralateral to the lesion, results show two types of changes in HAGU: 1. In the caudal parts of the RN and the ventrolateral thalamic nucleus (VL), a strong HAGU decrease was demonstrated suggesting some cerebellorubral and cerebellothalamic fibres use glutamate (Glu) as their neurotransmitter. 2. In the rostral parts of the RN and the VL, an increase in HAGU was detected. This increase was particularly large at thalamic level, which led us to perform a kinetic analysis of the uptake system. Results show that the increase observed in HAGU is related in the thalamic area to an increased affinity of the transport sites for Glu. The mechanism of the HAGU increase measured in the rostral VL after cerebellectomy was further investigated in the presence of acetylcholine (ACh) which we have previously shown to be possibly involved in the neurotransmission of some cerebellothalamic and cerebellorubral fibres. ACh was shown to exert an inhibitory effect on HAGU in the control situation. Decrease in affinity of the transport sites for Glu induced by ACh was more pronounced when HAGU was enhanced as a consequence of the cerebellar lesion. We hypothesized that the cerebellectomy enhances the activity of nerve terminals which take up Glu in the VL and that we have shown to be mainly related to corticothalamic neurons. The basic mechanism involved in this activation could be the withdrawal of presynaptic inhibitory controls on corticothalamic fibres due to the removal of the putative cholinergic cerebellar input. This hypothesis was extended to the RN where previous electrophysiological and anatomical studies have suggested that the cerebellar lesion induces a sprouting of corticorubral nerve terminals. The increase in HAGU in response to the cerebellar lesion could constitute an adaptive mechanism by which the CNS may compensate for the loss of the excitatory cerebellar input to the RN and thalamic neurons by increasing the corticofugal transmission.
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References
Agid Y, Javoy F, Glowinski J (1973) Hyperactivity of remaining dopaminergic neurons after partial destruction of the nigrostriatal dopaminergic system in the rat. Nature 245: 150–151
Bromberg MB, Penney JB Jr, Young AB, Stephenson BS (1980) Evidence for glutamate as the neurotransmitter of corticothalamic and corticorubral pathways. Neurology 30: 396
Cajal RS (1911) Histologie du système nerveux de l'homme et des vertébrés. Vol. II Maloine, Paris
Divac I, Fonnum F, Storm-Mathisen J (1977) High affinity uptake of glutamate in terminals of corticostriatal axons. Nature 266: 377–378
Duggan AW, Hall JG (1975) Inhibition of thalamic neurons by acetylcholine. Brain Res 100: 445–449
Fonnum F, Soreide A, Kvale I, Walker J, Waalas I (1981a) Glutamate in cortical fibers. In: Di Chiara G, Gessa GL (eds) Glutamate as a neurotransmitter, Adv Bioch Psychopharm, Vol 27. Raven Press, New York, pp 29–41
Fonnum F, Storm-Mathisen J, Divac I (1981b) Biochemical evidence for glutamate as neurotransmitter in corticostriatal and corticothalamic fibres in the rat brain. Neuroscience 6: 863–873
Franck K, Fuortes MGF (1957) Presynaptic and postsynaptic inhibition of monosynaptic reflexes. Fed Proc 16: 39–40
Henn FA, Goldstein MN, Hamberger A (1974) Uptake of the neurotransmitter candidate glutamate by glia. Nature 249: 663–664
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 (1983) 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
Logan WJ, Snyder SH (1971) Unique high affinity uptake system for glycine, glutamic and aspartic acids in central nervous tissue of the rat. Nature 234: 297–299
Lowry OH, Rosebrough NY, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193: 265–275
Massion J (1967) The mammalian red nucleus. Physiol Rev 47: 383–436
Moore R (1974) Central regeneration and recovery of function: the problem of collateral reinnervation. In: Stein DG, Rosen JJ, Butters N (eds) Plasticity and recovery of function in the central nervous system. Academic Press, New York, pp 111–128
Murakami F, Fujito Y, Tsukahara N (1976) Physiological properties of the newly-formed cortico-rubral synapses of red nucleus neurons due to collateral sprouting. Brain Res 103: 146–151
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
Murakami F, Tsukahara N, Fujito Y (1977) Analysis of unitary EPSPs mediated by the newly-formed cortico-rubral synapses after lesion of the interpositus nucleus. Exp Brain Res 30: 233–243
Murakami F, Tsukahara N, Fujito Y (1978) Properties of synaptic transmission of the newly-formed cortico-rubral synapses after lesion of the nucleus interpositus of the cerebellum. Exp Brain Res 30: 245–258
Murrin LC, Lewis MS, Kuhar MJ (1978) Amino acid transport: alterations due to synaptosomal depolarization. Life Sci 22: 2009–2016
Nadler JV, Cotman CW, Lynch GS (1974) Biochemical plasticity of short-axon interneurons: increased glutamate decarboxylase activity in the denervated area of rat dentate gyrus following entorhinal lesion. Exp Neurol 45: 403–413
Nagy JI, Vincent SR, Fibiger HC (1978) Altered neurotransmitter synthetic enzyme activity in some extrapyramidal nuclei after lesions of the nigro-striatal dopamine projection. Life Sci 22: 1777–1782
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
Nakamura Y, Mizuno N, Konishi A (1978) A quantitative electron microscope study of cerebellar axon terminals on the magnocellular red nucleus neurons in the cat. Brain Res 147: 17–27
Nieoullon A, Dusticier N (1980) Choline acetyltransferase activity in discrete regions of the cat brain. Brain Res 196: 139–149
Nieoullon A, Dusticier N (1981a) Decrease in choline acetyltransferase activity in the red nucleus of the cat after cerebellar lesion. Neuroscience 6: 1633–1641
Nieoullon A, Dusticier N (1981b) 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 (1983) Presynaptic dopaminergic control of high affinity glutamate uptake in the striatum. Neurosci Lett 43: 191–196
Palkovits M (1973) Isolated removal of hypothalamic or other brain nuclei of the rat. Brain Res 59: 449–450
Rispal-Padel L (1979) Functional characteristics of the cerebellothalamo-cortical pathway in the cat. In: Massion J, Sasaki K (eds) Cerebro-cerebellar interactions. North-Holland Biochemical Press, Amsterdam, pp 67–101
Snider RS, Niemer WT (1961) A stereotaxic atlas of the cat brain. University of Chicago Press, Chicago
Steward O (1982) Assessing the functional significance of lesioninduced neuronal plasticity. Int Rev Neurobiol 23: 197–254
Storm-Mathisen J (1977) Glutamic acid and excitatory nerve ending: reduction of glutamic acid uptake after axotomy. Brain Res 120: 379–386
Tsukahara N (1978) Synaptic plasticity in the red nucleus. In: Cotman CW (ed) Neuronal plasticity. Raven Press, New York, pp 113–130
Tsukahara N (1981) Sprouting and the neuronal basis of learning. TINS 4: 234–237
Tsukahara N, Hultborn H, Murakami F (1974) Sprouting of cortico-rubral synapses in red nucleus neurons after destruction of the nucleus interpositus of the cerebellum. Experientia 30: 57–58
Tsukahara N, Hultborn H, Murakami F, Fujito Y (1975) Electrophysiological study of formation of new synapses and collateral sprouting in red nucleus neurons after partial denervation. J Neurophysiol 38: 1359–1372
Ungerstedt U (1971) Postsynaptic supersensitivity after 6-hydroxydopamine induced degeneration of nigrostriatal dopamine system. Acta Physiol Scand 367: 69–93
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
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Nieoullon, A., Kerkerian, L. & Dusticier, N. 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 (1984). https://doi.org/10.1007/BF00235271
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DOI: https://doi.org/10.1007/BF00235271