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Following blockage of the protein transport by colchicine or by interruption of the rubrofugal descending pathway, choline acetyltransferase-immunoreactive neurons were found in the red nucleus of the rat. Their morphology and location suggest that they are rubrospinal neurons.
The effects of 5-hydroxytryptamine (5-HT) on the inhibitory responses evoked by gamma-aminobutyric acid (GABA) in neurons of the red nucleus (RN) were studied using a microiontophoretic technique. Extracellular unitary recordings performed in anesthetized rats demonstrated that 5-HT ejection influenced GABA-evoked inhibition in 94% of RN neurons, enhancing them in 52% and depressing them in 46% of cases. Both effects were specific and dose-dependent,although enhancements or depressions of the GABA responses were respectively inversely and directly related to the doses of 5-HT applied. The type of modulation exerted by 5-HT on the GABA responses was independent of the action of the amine on background firing. In fact, 5-HT induced an enhancement of the GABA responses in neurons mostly located in the rostral RN and a depression in those in the caudal RN. The application of 8-hydroxy-2(di-n-propylamino)tetralin, a specific 5-HT(1A) receptor agonist, enhanced GABA responses, whereas alpha-methyl-5-hydroxytryptamine, a 5-HT(2A) receptor agonist, depressed them. Both the 5-HT(2) antagonist methysergide and the 5-HT(2A) selective antagonist ketanserin were able to block partially or totally the depressive action of 5-HT on GABA responses. In contrast, the same 5-HT antagonists mimicked the enhancing action of 5-HT on the GABA responses or were ineffective. Application of bicuculline, a GABA(A) receptor antagonist, enhanced the excitatory action of 5-HT on the background firing and slightly reduced the inhibitory action. It is concluded that 5-HT is able to modulate GABA-evoked responses in RN neurons by acting on both 5-HT(1A) and 5-HT(2A) receptors. The functional significance of a serotonergic control on GABAergic inhibitory effects in RN is discussed.
In white non-strain rats with elaborated instrumental responses preliminary section of the rubro-spinal tract was shown to promote the compensatory restorative processes after the destruction of the red nucleus and the ventrolateral thalamic nucleus. Facilitation observed is considered to be a result of transfer of the motor activity to the cortico-spinal system due to activation of the inferior olive and the cerebellum.
Following a single electrocoagulating RF lesion aimed at left red nucleus, rabbits received classical conditioning of the nictitating membrane (NM) response. A tone was the conditioned stimulus (CS) and electrostimulation of the eye was the unconditioned stimulus (US). The US was applied to the right eye during the initial phase of training. It was then switched to the left eye to assess transfer of learning and ultimately switched back to the right eye. NM responses were recorded simultaneously from both eyes during each phase of training. Consistent with reports implicating a cerebellar-rubro circuit in this behavior, RN lesions disrupted acquisition of CRs in the eye contralateral to the lesion. Animals with disrupted NM CRs of the right eye resembled controls in showing transfer of conditioning to the left eye. CR-disrupting lesions did not affect UR amplitude.
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.
Integrins are cell surface receptors known to be important for regeneration in the peripheral nervous system. We have investigated the expression of integrin messenger RNAs in red nucleus neurons of adult rats after axotomy and administration of neurotrophic factors. Using radioactive in situ hybridization, messenger RNA for integrin subunits beta1, alpha3, alpha7 and alphaV could be detected. No change of any alpha subunit could be detected after axotomy. In contrast, a small upregulation of beta1 was detected after lesion. Administration of neurotrophin-3 induced a robust further increase in beta1 messenger RNA levels, whereas brain-derived neurotrophic factor did not. By analogy to the peripheral nervous system, we propose that integrins may be important for a regenerative response in central nervous system neurons.
The small effects of bilateral lesions of motor thalamus on motor control and the transient deficits induced by bilateral kainic red nucleus (RN) lesions have been explained by a parallel competitive role of the cortico- and rubro-spinal pathways. Either pathway can take over motor control if the other is damaged. In this study the effect of bilateral and simultaneous lesions of both RN and motor thalamus was analyzed on cats overtrained to reach toward a moving target. After lesion, accuracy was impaired, movement onset was delayed, and movement execution was perturbed. However, postoperative retraining led to full recovery of the preoperative accuracy level although movement latency remained higher. The relative mildness of the long-lasting deficit after lesioning 2 main motor brain structures underlines the robustness of overlearned movements and widens the idea of parallelism in the motor system to other (subcortical?) pathways.
After biotinylated dextranamine injection into the dorsal part of the red nucleus (RN) in the rat, labeled axons were distributed contralaterally in the lateral tegmental field including the parvicellular reticular formation (RFp), and ipsilaterally in the medial reticular formation. In the cervical spinal cord, labeled axons were present bilaterally with a contralateral dominance mainly in laminae V-VI and the dorsal part of laminae VII. After ipsilateral injections of rhodamine dextranamine, Fluoro-ruby (FR) into the RFp and Fluoro-gold (FG) into the upper cervical spinal cord, a population of FR-labeled neurons was found in the dorsal part of the contralateral RN, whereas the majority of FG-labeled neurons were located more ventrally. However, some of them were intermingled with FR-labeled neurons, and as many as one-third of FR-labeled neurons were labeled with FG. After combined injections of FR into the RFp and FG into the lower cervical spinal cord, RN neurons labeled with FG existed more ventrally than those retrogradely labeled from the upper cervical spinal cord, and less than 10% of FR-labeled neurons were labeled with FG. The present data suggest that axon collateral innervation of the RFp and the upper cervical spinal cord by single RN neurons may be responsible for coordinating head and orofacial movements.
The retrograde transport of horseradish peroxidase was used to study the topographic and laminar origins of the cortical projections to the parvocellular and the magnocellular divisions of the red nucleus in Macaca mulatta and Macaca fascicularis. Approximately 90% of the corticorubral projection is directed to the parvocellular division of the nucleus. Corticoparvocellular (CRp) neurons are pyramidally shaped, are smaller in size than corticospinal neurons, and are more numerous. They are found principally in sublamina Va of cytoarchitectonic areas 4 and 6, and in moderate quantities in sublamina Vb of posterior area 8 and area 5. In areas 4 and 6, the cells are grouped in clusters of three to 15 neurons each and are arranged in cellular bands of varying rostrocaudal thickness which course mediolaterally. With respect to functionally defined zones, CRp neurons are found throughout the supplementary motor area and the precentral motor cortex. In addition, they are found in parts of areas 5, 6, and 24 that project to these cortical motor areas, and that are thought to have "premotor" or movement-programming functions. The corticomagnocellular (CRm) projection arises principally from cells in sublamina Vb of the precentral arm and leg areas (area 4), and from adjacent parts of posterior area 6, CRm cells are pyramidally shaped, and their size distribution is bimodal, with peaks that correspond, respectively, to the modal diameters of CRp and of corticospinal neurons. These results and those of previous studies suggest that CRm neurons are involved principally in the control of hand and foot movements, with little effect on more proximal musculature. The massive CRp projection, however, is clearly part of a large cerebrocerebellar communication system, with motor and/or movement programming functions that have yet to be clearly defined.
Light microscopic-autoradiographic findings indicate that, following chronic lesions of cerebellorubral projections in the adult cat, somatosensory corticofugal axons in the cerebral crus give rise to collateral sprouts which reinnervate the deafferented red nucleus. These data strongly suggest that these new axons reinnervate the deafferented soma and proximal dendrites of the rubral neurons. This reactive synaptogenesis may complete with terminal sprouting from motor corticorubral synapses already present on the distal dendrites of the rubral neurons.
A comparative mapping of gamma-aminobutyric acid neurons identified by means of glutamic acid decarboxylase (GAD) immunohistochemistry was performed in the red nucleus (RN) in both intact and hemicerebellectomized adult cats (21 days postoperative). In the deafferented RN (contralateral to the lesion) as well as in the adjacent dorsolateral reticular formation, a marked increase in the number of GAD-positive perikarya was observed. In this mesencephalic area, some neurons may therefore increase their endogenous levels of immunodetectable GAD, as a response to cerebellar deafferentation. This can be viewed as one of the events contributing to functional recovery.
We examined the rubrospinal projection to forelimb motoneurons (Mns) in cats, in comparison with the corticospinal projection. Under pentobarbital anesthesia, intracellular recordings were made from forelimb Mns following stimulation of the red nucleus (RN) and the cerebral peduncle (CP). Single pulse stimulation of the RN produced excitatory postsynaptic potentials (EPSPs) in the majority of forelimb Mns (58/80, 72%). Segmental latencies of RN-EPSPs were shorter than 1.2 ms in 14 out of 22 Mns in which RN-EPSPs were detected in the C8-T1 segments, and in 3 of 36 Mns in the C6-C7 segments. The results suggest monosynaptic rubro-motoneuronal connections in a substantial portion of forelimb Mns particularly in the C8-T1 segments. There was no evidence suggesting monosynaptic connections between cerebral cortex and forelimb Mns.
In the rat, the extent of collateralization of projections from the cerebellar nuclei to the red nucleus and inferior olive was investigated using a retrograde double labeling technique. The combination of tracers selected, cholera toxin-beta-subunit and WGA-BSA-gold, not only enabled the use of small injection sites but also resulted in clearly distinguishable and permanently stained neurons that could be analyzed in counterstained sections.
Single unit extracellular recordings were obtained from cat lumbar spinal cord dorsal horn neurons activated by cutaneous inputs. The effect of electrical conditioning stimuli applied to the red nucleus (RN) was predominantly that of inhibition although in some cases excitation was seen. All the neurons that projected to the lateral cervical nucleus were inhibited; none of these were excited. These findings suggest that the RN may exert a dynamic modulatory action on the transmission of cutaneous information during the execution of a motor program.
In 4 rhesus monkeys wheat germ agglutinin-horseradish peroxidase (WGA-HRP) injections were made in the mesencephalic tegmentum. In 3 cases with injections involving the red nucleus (RN), rubrospinal fibers descended mainly contralaterally to terminate in laminae V, VI and dorsal VII of the spinal cord and in the lateral motoneuronal cell groups at the level of the cervical and lumbosacral enlargements. In all 4 cases the area of the interstitial nucleus of Cajal (INC) was injected, which resulted in labeled interstitiospinal fibers in the medial part of the ipsilateral ventral funiculus of the spinal cord. The results indicate that there is no major qualitative difference between the mesencephalic (RN and INC) and motor cortical projections to the spinal cord.
Responses of rubrospinal neurons (RSNs) to iontophoretic applications of L-glutamate (L-Glu), L-aspartate (L-Asp), quisqualate (Quis) and N-methyl-D-aspartate (NMDA) have been studied in the rat red nucleus (RN) in vivo. All agonists produced a dose-dependent increase of the firing rate and Quis was found to be the most efficient. The responses to NMDA and to a lesser extent to L-Asp were abolished by steady application of 2-amino-5-phosphonovalerate (2APV) whereas responses to Quis were unaffected and those to L-Glu poorly antagonized. On the other hand, NMDA-mediated excitations were insensitive to steady application of 6,7-dinitroquinoxaline-2,3-dione (DNQX) which abolished responses to Quis and to a lesser extent to L-Glu while those to L-Asp were less affected. These results show the presence of both NMDA and non-NMDA receptors on RSNs in the rat. A specific localization of the NMDA receptors on distal dendrites of these neurons is suggested.
Adult cats were trained to insert a forelimb into horizontally mounted transparent cylinders and then either depress a barrier or pull a sliding tray against resistance in order to receive food reward. Unilateral lesions of both bulbar pyramid and red nucleus resulted in severe neurological deficits. However, the instrumental tasks were soon accomplished at preoperative levels of rapidity and strength, although movements of the digits and wrist were reduced and adjustive movements occurred chiefly at more proximal joints. These results support our hypothesis that conditioned and unconditioned behaviors are mediated through different mechanisms.
The effects of cross-innervation of peripheral flexor and extensor nerves on the time course and properties of red nucleus (RN) neurons were studied in adult cats. The time course of corticorubral unitary EPSPs was examined. In operated cats, RN neurons innervating upper spinal segments (C-cells) manifested corticorubral unitary EPSPs with shorter time-to-peak and larger amplitude than in normal cats. The mean amplitude of these EPSPs was 0.41 +/- 0.11 mV; the mean time-to-peak was 1.14 +/- 0.51 ms (n = 18). These values differ from normal cats (0.33 +/- 0.09 mV, and 2.68 +/- 0.61 ms, n = 22). RN neuron membrane properties were examined in cross-innervated cats. The main time constant was 5.2 +/- 0.7 ms (n = 10), the shorter equalizing time constant, 0.69 +/- 0.19 ms (n = 10), the input resistance, 2.5 +/- 0.8 M omega. These values were not significantly different from those of normal cats. The electrotonic length was 1.2 (n = 10), somewhat larger than in normal cats. The number of converging interpositorubral synapses, estimated in eight cells from cross-innervated cats, ranged from 37 to 57. This was not significantly different from normal cats, and indicated that there is no large-scale degeneration of interpositorubral synapses after cross-innervation. These results suggest that sprouting and formation of functional synapses occur after cross-innervation of peripheral flexor and extensor nerves.