Participation of the red nucleus in motor initiation: Unit recording and cooling in cats

doi:10.1016/0166-4328(88)90098-8

Behavioural Brain Research

Volume 28, Issues 1–2, April–May 1988, Pages 207-216

https://doi.org/10.1016/0166-4328(88)90098-8 Get rights and content

Abstract

Cats were trained to release (Go) or not to release (No-go) a lever after a brief auditory signal, depending on the presence of an additional tone (No-go cue). Unit recording and cooling were made in the red nucleus (RN) contralateral to the performing limb. Three major results were found: (1) in the Go condition, we observed phasic increases of rubral firing, with a constant latency after the auditory signal and with an amplitude correlated to the latency of motor triggering (i.e. reaction time, RT); the tonic activity preceding the auditory signal could also be correlated to the RTs for some units; (2) in the No-go condition, there was no phasic increase of rubral firing after the auditory signal; the tonic activity during the presentation of the No-go cue was markedly decreased compared to the Go trials; (3) cooling of the RN increased the RTs and could also block the motor triggering. These results suggest that the RN is involved in setting and triggering a conditioned motor response according to sensory cues.

References (29)

J.F. Burton et al.
Dependence of the activity of interpositus and red nucleus neurons on the sensory input data generated by movement
Brain Res.
(1978)
F. Condé et al.
Demonstration of a rubrothalamic projection in the cat with some comments on the origin of the rubrospinal tract
Neuroscience
(1980)
F. Condé et al.
The rubro-olivary tract in the cat, as demonstrated with the method of retrograde transport of Horseradish peroxidase
Neuroscience
(1982)
C. Ghez et al.
Activity of red nucleus associated with a skilled forelimb movement in the cat
Brain Res.
(1977)
P.R. Kennedy et al.
Functional and anatomic differentiation between parvicellular and magnocellular regions of red nucleus in the monkey
Brain Res.
(1986)
E. Luschei et al.
Muscle potentials in reaction time
Exp. Neurol.
(1967)
G.N. Orlovsky
Activity of rubrospinal neurons during locomotion
Brain Res.
(1972)
J.B. Otero
Comparison between the red nucleus and precentral neurons during learned movement in the monkey
Brain Res.
(1976)
A.I. Shapovalov
Extrapyramidal monosynaptic and disynaptic control of mammalian motoneurons
Brain Res.
(1972)
M. Amalric et al.
Are coding schemes actually used? The cooling test demonstration

M. Amalric et al.

Cat red nucleus changes of activity during the motor initiation in a reaction time task

Exp. Brain Res.

(1883)

M. Bénita et al.

Effects of ventrolateral cooling on initiation of forelimb flexion by conditioned cats

Exp. Brain Res.

(1979)

P.D. Cheney

Response of rubromotoneuronal cells identified by spike-triggered averaging of EMG activity in awake monkey

Neurosci. Lett.

(1980)

P.D. Cheney et al.

Rubromotoneuronal cells: identification in the awake monkey and comparison with corticomotoneuronal cells

Neurosci. Lett.

(1986)

Cited by (28)

Noradrenergic modulation of glutamate-induced excitatory responses in single neurons of the red nucleus: An electrophysiological study
2015, Neuroscience
Citation Excerpt :
The red nucleus (RN) is a mesencephalic structure involved in various aspects of motor control including, according to recent theories, even phonation (Martin and Ghez, 1988; Schmied et al., 1988; Hicks and Onodera, 2012).
The effect induced by noradrenaline (NA) on the spiking activity evoked by glutamate (Glu) on single neurons of the mesencephalic red nucleus (RN) of the rat was studied extracellularly. Long-lasting microiontophoretic applications of the amine induced a significant and reversible depression of the responsiveness of RN neurons to Glu. This effect was mediated by noradrenergic alpha₂ receptors since it was mimicked by application of clonidine, an alpha₂ adrenoceptor agonist, and blocked or at least reduced by application of yohimbine, an antagonist of NA for the same receptors. The effect appears homogeneously throughout the nucleus and is independent of the effect of NA on baseline firing rate. Application of isoproterenol, a beta adrenoceptor agonist, either enhanced or depressed neuronal responses to Glu in a high percentage (86%) of the tested neurons. Moreover, application of timolol, a beta adrenoceptor antagonist, was able to strengthen the depressive effects induced by NA application on neuronal responsiveness to Glu.
Although these data suggest some involvement of beta adrenergic receptors in the modulation of neuronal responsiveness to Glu, the overall results indicate a short-term depressive action of NA, mediated by alpha₂ receptors, on the responsiveness of RN neurons and suggest that stress initially leads to an attenuation of the relay function of the RN.
The effect of brachium conjunctivum transection on a conditioned limb response in the cat
2000, Behavioural Brain Research
Seven cats were trained to perform a forelimb conditioned response to a paired tone conditioned stimulus (CS)/shock unconditioned stimulus (UCS). Brachium conjunctivum section ipsilateral to the trained limb was carried out following criterion conditioned response (CR) performance. Lesion sites were identified histologically and further confirmed by observation of cellular changes in the dentate and interpositus nuclei ipsilateral to the section. The brachium conjunctivum was found to have been sectioned in four of the seven subjects. Each of these animals demonstrated a total or near-total loss of the CR. Extended postoperative training resulted in no increase in CR performance levels. The unconditioned response (UCR) remained unaffected, as did limb placing, accuracy of striking at moving objects, grooming, running and walking. The results are discussed in the context of an earlier report by McCormick et al. [Bull Psychonom Soc 1981;18:103–5], in which section of the superior cerebellar peduncle was found to abolish a conditioned nictitating membrane response in the rabbit. Taken together, they support the contention of Lavond [Annu Rev Psychol 1993;44:317–42], Thompson [In: Sprague JM, Epstein AN, editors. Progress in Psychobiology and Physiological Psychology. New York: Academic Press 1983, pp. 167–96], Yeo et al. [Behav Brain Res 1984;13:261–66; Exp Brain Res 1985;60:87–98; Exp Brain Res 1985;60:99–113; Exp Brain Res 1992;88:623–38.] and others that the cerebellum represents a critical site for acquisition and retention of a conditioned memory trace.
The effect of rubrospinal tractotomy on a conditioned limb response in the cat
1999, Behavioural Brain Research
Five cats were trained to perform a forelimb conditioned response to a paired tone CS/shock UCS. Rubrospinal tract section ipsilateral to the trained limb was carried out following criterion CR performance. Lesion sites were identified histologically and further confirmed by observation of cellular changes in the red nucleus contralateral to the trained limb. Tractotomy resulted in total or near-total loss of the CR. Prolonged postoperative training resulted in no increase in CR performance levels. The UCR remained unaffected, as did limb placing, accuracy of striking at moving objects, grooming, running and walking. Training of the opposite limb in two subjects resulted in mean scores of 90 and 85% within three sessions. Control lesions in those subjects resulted in no changes in CR performance scores. The red nucleus receives a substantial input from sensorimotor cortex and cerebellum, both of which have been shown to represent essential parts of the brain circuitry involved in associative learning and memory. Since pyramidotomy has no effect on limb CR performance [Vonedia TJ. Exp Neurol 1976;19:483–493], the possible role of the red nucleus/rubrospinal tract is discussed in terms of a critical trigger area for the expression of a learned motor response.
Pharmacological inactivation in the analysis of the central control of movement
1999, Journal of Neuroscience Methods
In this review, we describe how pharmacological inactivation can be used to elucidate the central control of skilled limb movement. Local anesthetics and tetrodotoxin block neuronal cell bodies and passing fibers while γ-aminobutyric acid (GABA) and muscimol only block cell bodies. Blockade induction time is short (several minutes) for all the agents. Blockade duration produced by local anesthetics and GABA is 15–60 min, while that of tetrodotoxin and muscimol is up to several days. We describe our drug injection system, with an integrated microelectrode and a viewing port for visually monitoring drug flow into the injection cannula. We used glucose metabolism to assess the extent of inactivation. Intracortical lidocaine or muscimol injection produces a central core of maximal hypometabolism (1 mm radius), which could be due to drug spread, surrounded by an extensive region (several millimeters) of reduced hypometabolism, possibly due to reduced synaptic activity of neurons receiving projections from the core region. Drug injection only depresses neuronal activity, which contrasts with cooling, where there can be neuronal hyperexcitability at the periphery of the inactivation site. Our experiments in behaving animals show how pharmacological inactivation is an effective analytical tool for dissecting the differential functional contributions of subcortical and cortical forelimb representations to limb movement control.
Changes in motor performance and rubral single unit activity in cats after microinjections of serotonin into the red nucleus area
1991, Brain Research
The serotonergic control exerted on the red nucleus (RN) was studied in unrestrained cats during the performance of a simple reaction time task which consisted of releasing a lever in response to an auditory go-signal. The effects of microinjections of serotonin-oxalate salt into the rubral area on the motor activity and on the firing of neurons recorded concomitantly in the red nucleus were investigated. Injections of serotonin (5-HT) (200–400 ng) into the red nucleus or its dorsal border induced subtle alterations in the conditioned motor performances but had no major effects on the spontaneous motor behavior. The changes in the conditioned motor output (an increase in the static force exerted on the lever and a speeding up of the lever release) are reminiscent of the facilitatory influence of serotonin on various motor reflexes previously reported. Changes in the neuronal activity were observed concomitantly with the effects on the motor output: 5-HT either enhanced or reduced the firing rate of the rubral neurons. These effects were apparently dependent on the discharge pattern of the neurons during the static motor activity. The results suggest that the serotonergic input to the red nucleus may participate in motor control by exerting a dual modulatory action on the activity of rubral neurons.
Single-unit activity in red nucleus during the classically conditioned rabbit nictitating membrane response
1991, Neuroscience Research
Previous investigations have suggested that the cerebellum and associated brainstem structures, including the red nucleus, are essential for the expression of the classically conditioned nictitating membrane (NM) response. The present study examined the firing patterns of extracellularly-recorded single units in the red nucleus of the awake rabbit during differential conditioning. Tones were used as conditioned stimulus (CS+ and CS−) and periocular electrostimulation was used as the unconditioned stimulus (US). Most units exhibited one or more changes in firing rate during the presentation of the CS, and increases in firing were much more common than decreases. The onset of some of these changes appeared to be time-locked to the onset of the CS (‘CS-locked’ responses), while other changes were time-locked to the onset of the CR (‘CR-locked’ responses). About one-third of all CS-locked changes were CR-dependent, meaning that the neuronal response was reduced when the CR did not occur. About two-thirds of all CR-locked responses preceded the onset of the CR, and lead times varied considerably across units. Many CR-locked units were located in what has been described as a dorsal face region of the red nucleus. Most units responded to the US, and some of the US responses were CR-dependent: i.e., a smaller US response was evoked when a CR preceded the US than when the CR was absent. Our results support the notion that cerebellum-brainstem circuits are involved in generating NM CRs.

View all citing articles on Scopus

View full text

The magnocellular red nucleusParticipation of the red nucleus in motor initiation: Unit recording and cooling in cats

Abstract

Brain Res.

Neuroscience

Neuroscience

Brain Res.

Brain Res.

Exp. Neurol.

Brain Res.

Brain Res.

Brain Res.

Are coding schemes actually used? The cooling test demonstration

Cat red nucleus changes of activity during the motor initiation in a reaction time task

Exp. Brain Res.

Effects of ventrolateral cooling on initiation of forelimb flexion by conditioned cats

Exp. Brain Res.

Response of rubromotoneuronal cells identified by spike-triggered averaging of EMG activity in awake monkey

Neurosci. Lett.

Rubromotoneuronal cells: identification in the awake monkey and comparison with corticomotoneuronal cells

Neurosci. Lett.

The magnocellular red nucleus
Participation of the red nucleus in motor initiation: Unit recording and cooling in cats