Summary
The activity of 61 rubral neurones was recorded in association with microinjections of GABA, muscimol, bicuculline-methiodide or saline, in cat Red Nucleus area, during the performance of a reaction time task. The depressing action of GABA and muscimol on the firing of most neurones (17/23) suggests that, in a behavioural situation, an inhibitory GABAergic control can be exerted on rubral neurones discharging with different patterns during the reaction time task. The motor slowing down induced by GABA and muscimol is in agreement with a general reduction of the rubral output. Injections of bicuculline, whose antagonistic effects on GABA transmission are well established in the Red Nucleus, had various consequences on the firing of rubral neurones: 1) the decreases of activity related to the reaction time task were never suppressed, suggesting that these task-related inactivations are probably not mediated by GABA A receptors; 2) an enhancement of the tonic and phasic discharges was found for 1/4 of the neurones (7/29), which were either activated or not modulated in relation to the reaction time task, suggesting that a sustained GABA A-mediated inhibition, blocked by bicuculline, could be exerted on these neurones; 3) a reduction of the tonic and phasic discharges was observed for other neurones (15/29), which were either activated, inactivated or not modulated in relation to the reaction time task, suggesting that the activity of these neurones could be controlled by inhibitory processes not mediated by GABA A receptors, possibly enhanced or released by bicuculline. The delay in motor triggering induced by bicuculline could be related to the disruption of the pattern or rubral output during the reaction time task, as a result of the opposite changes affecting the firing of rubral neurones. A well-balanced GABAergic activity appears to be critical in the control of rubral firing during the performance of the reaction time task.
Similar content being viewed by others
References
Alger BE, Nicoll RA (1982) Pharmacological evidence for two kinds of GABA receptors on rat hippocampal pyramidal cells studied in vitro. J Physiol 328: 125–141
Altmann H, Ten Bruggencate G, Pickelmann P, Steinberg R (1976) Effects of GABA, glycine, picrotoxin and bicuculline methochloride on rubrospinal neurones in cats. Brain Res 111: 337–345
Amalric M, Condé H, Dormont JF, Farin D, Schmied A (1983a) Cat red nucleus changes of activity during the motor initiation of a reaction time task. Exp Brain Res 52: 210–218
Amalric M, Condé H, Dormont JF, Schmied A (1983b) Are coding schemes actually used? The cooling test demonstration. Exp Brain Res Suppl 7: 204–209
Amalric M, Dormont JF, Farin D, Schmied A (1988) Microinjections of GABA agonist and antagonist in the red nucleus: effects on neural activity and motor performance in the cat. Suppl Europ J Neurosci 11th meeting. ENA Abstr 11–12
Anderson ME (1971) Cerebellar and cerebral inputs to physiologically identified efferent cell groups in the red nucleus of the cat. Brain Res 30: 49–66
André D, Viullon-Cacciutolo G, Bosler O (1987) GABA nerve endings in the rat red nucleus combined detection with serotonin terminals using dual immunocytochemistry. Neuroscience 23: 1095–1102
Batson DE, Amassian VE (1986) A dynamic role of rubral neurons in contact placing by the adult cat. J Neurophysiol 56: 835–856
Beitz A, Ecklund L (1988) Colocalization of fixative-modified glutamate and glutaminase but not GAD in rubrospinal neurons. J Comp Neurol 274: 265–279
Boussaoud D, Joseph JP (1985) Role of cat substantia nigra reticulata in eye and head movements. II. Effects of pharmacological injections. Exp Brain Res. 57: 297–304
Bowery NG, Hudson AL, Price GW (1987) GABA A and GABA B receptor sites distribution in the rat central nervous system. Neuroscience 20: 365–383
Buee J, Deniau JM, Chevalier G (1986) Nigral modulation of cerebello-thalamo-cortical transmission in the ventral medial thalamic nucleus. Exp Brain Res 65: 241–244
Burton JF, Onoda N (1978) Dependence of the activity of interpositus and red nucleus neurons on sensory input data generated by movement. Brain Res 152: 41–63
Chevalier G, Vacher S, Deniau JM, Desban M (1985) Disinhibition as a basic process in the expression of striatal functions. 1. The striato-nigral influence on tecto-spinal/tecto-diencephalic neurons. Brain Res 334: 215–226
Condé F, Condé H (1973) Etude de la morphologie des cellules du noyau rouge par la methode de Golgi. Brain Res 53: 249–271
Condé F, Condé H (1982) The rubro-olivary tract in the cat, as demonstrated with the method of retrograde transport of horseradish peroxydase. Neuroscience 7: 715–724
Curtis DR, Duggan AW, Johnston GAR, McLennan H (1971) Antagonism between bicuculline and GABA in the cat brain. Brain Res 33: 57–73
Davis R, Vaughan PC (1969) Pharmacological properties of feline red nucleus. Int J Neuropharmacol. 8: 475–488
Dormont JF, Farin D, Schmied A, Amalric M (1989) Cat red nucleus activity preceding movement depends on initial conditions. Exp Brain Res 77: 271–282
Duggan AW, McLennAn H (1971) Bicuculline and inhibition in the thalamus. Brain Res 25: 188–191
Dykes RW, Landry P, Metherate R, Hicks TP (1984) Functional role of GABA in cat primary somatosensory cortex: shaping receptive fields of cortical neurons. J Neurophysiol 52: 1066–1093
Enna SJ, Collins JF, Snyder SH (1977) Stereospecificity and structure-activity requirements of GABA receptors binding in rat brain. Brain Res 124: 185–190
Ghez C, Vicario D (1978) Discharge of red nucleus neurons during voluntary muscle contraction: activity patterns and correlations with isometric force. J Physiol (Paris) 74: 283–285
Gibson A, Houk JC, Kohlerman N (1985) Relation between red nucleus discharges and movement parameters in trained macaque monkey. J Physiol (Lond) 358: 551–570
Godfraind JM, Krnjevic K, Pumain R (1970) Doubtful value of bicuculline as a specific antagonist of GABA. Nature 228: 675–676
Heyer EJ, Nowak LM, Macdonald R (1981) Bicuculline: a convulsant with synaptic and non-synaptic actions. Neurology 31: 1381–1390
Hicks TP, Metherate R, Landry P, Dykes RW (1986) Bicucullineinduced alterations of response properties in functionally identified ventroposterior thalamic neurones. Exp Brain Res 63: 248–264
Hill RG, Simmonds MA, Straughan DW (1973) A comparative study of some convulsant substances as gamma-aminobutyric acid in the feline cerebral cortex. Br J Pharmacol 49: 37–51
Hirsh JC, Burnod Y (1987) A synaptically evoked late hyperpolarization in the rat dorsolateral geniculate neurons in vitro. Neuroscience 23: 457–468
Holstege G, Tan J (1988) Projections from red nucleus and surrounding areas to the brain stem and spinal cord in the cat: an HRP and autoradiographical tracing study. Behav Brain Res 28: 33–57
Huffman RD, Davis R (1977) Pharmacology of the bracchium conjunctivum: red nucleus synaptic system in the baboon. J Neurosci Res 3: 175–192
Jasper HH, Ajmone-Marsan C (1954) A stereotaxic atlas of the diencephalon of the cat. Natl Coun Res Canada, Ottawa
Johnston GAR (1976) Physiological pharmacology of GABA and its antagonists in the vertebrate nervous system. In: Roberts E, Chase TN, Tower DB (eds) GABA in nervous system function. Plenum, New York, pp 395–411
Katsumaru H, Murakami F, Wu JY, Tsukahara N (1984) GABAergic intrinsic interneurons in the red nucleus of the cat demonstrated with combined immunocytochemistry and anterograde degeneration methods. Neurosci Res 1: 35–44
King JS, Dom RM, Martin GF (1974) Anatomical evidence for an intrinsic neuron in the red nucleus. Brain Res 67: 317–323
Lawrence DG, Kuypers HGM (1968) The functional organization of the motor system in the monkey. II. Effects of lesion of descending brain stem pathways. Brain 91: 15–36
Marshall KC, Flumerfelt BA, Gwyn DG (1980) Acetylcholinesterase activity and acetylcholine effects in the cerebello-rubro-thalamic pathway of the cat. Brain Res 190: 493–504
Martin JH, Ghez C (1988) Red nucleus and motor cortex: parallel motor systems for the initiation of skilled movement. Behav Brain Res 28: 217–227
Miller JJ, McLennan H (1974) The action of bicuculline upon acetylcholine-induced excitations of central neurones. Neuropharmacology 13: 785–787
Murakami F, Katsumaru H, Wu JY, Matsuda T, Tsukahara N (1983) Immunocytochemical demonstration of GABAergic synapses on identified rubrospinal neurons. Brain Res 267: 357–360
Newberry NR, Nicoll RA (1984) A bicuculline-resistant inhibitory post-synaptic potential in rat hippocampal pyramidal cells in vitro. J Physiol (Lond) 348: 239–254
Nicholson C (1985) Diffusion from an injected volume of a substance in brain tissue with arbitrary volume fraction and tortuosity. Brain Res 333: 325–329
Nieoullon A, Dusticier N (1981) Glutamate-decarboxylase distribution in discrete motor nuclei in the cat brain. J Neurochem 37: 202–209
Nowak LM, Young AB, Macdonald L (1982) GABA and bicuculline action on mouse spinal cord and cortical neurons in cell culture. Brain Res 244: 155–164
Oka H (1988) Functional organization of the parvocellular red nucleus in the cat. Behav Brain Res 28: 233–240
Olsen RW, Ban M, Miller T (1976) Studies on the neuropharmacological activity of bicuculline and related compounds. Brain Res 102: 283–299
Padel Y, Jeneskog T (1981) Inhibition of rubro-spinal cells by somesthetic afferent activity. Neurosci Lett 21: 177–182
Ranish NA, Soechting JF (1976) Studies of the control of simple motor tasks: effect of thalamic and red nuclei lesions. Brain Res 102: 339–345
Rees S, Cragg BG, Everitt AV (1982) Comparison of extracellular space in the mature and ageing rat brain using a new technique. J Neurol Sci 53: 347–357
Rice ME, Gerhardt GA, Hierl PM, Nagy G, Adams RN (1985) Diffusion coefficients of neurotransmitters and their metabolites in brain extracellular fluid space. Neuroscience 15: 891–902
Sakaguchi H, Kubota M, Nakamura M, Tsukahara N (1984) Effects of amino acids on cat red nucleus neurons in vitro. Exp Brain Res 54: 150–156
Schmied A, Amalric M, Dormont JF, Conde H, Farin D (1988) Participation of the red nucleus in motor initiation: unit recording and cooling in cats. Behav Brain Res 28: 207–216
Schmied A, Amalric M, Dormont JF, Farin D (1990) GABAergic mechanisms in the cat red nucleus: effects of intracerebral microinjections of muscimol or bicuculline on a conditioned motor task. Exp Brain Res 81: 523–532
Schmied A, Farin D, Dormont JF, Amalric M (1989) Alteration of rubral single unit activity and movement parameters after injection of GABA or serotonin in cat red nucleus area. Am Soc Neurosci Abstr 15: 159–161
Sillito AM (1975) The effectiveness of bicuculline as an antagonist of GABA and visually evoked inhibition in the cat's striate cortex. J Physiol (Lond) 250: 287–304
Simmonds MA (1980) Evidence that bicuculline and picrotoxine act at separate sites to antagonize gamma-aminobutyric acid in rat cuneate nucleus. Neurophysiology 19: 39–45
Smith A (1970) The effects of rubral lesion and stimulation on conditioned forelimb flexion responses in the cat. Physiol Behav 5: 1121–1126
Sperber EF, Wurpel JND, Sharpless NS, Moshe SL (1989) Intranigral GABAergic drug effects on striatal dopamine activity. Pharmacol Biochem Behav 32: 1067–1070
Straughan DW, Neal MJ, Simmonds MA, Collins GGS, Hill RG (1971) Evaluation of bicuculline as GABA antagonist. Nature 233: 352–354
Svenneby G, Roberts E (1973) Bicuculline and N-methyl-bicuculline, competitive inhibitors of brain acetylcholinesterase. J Neurochem 21: 1025–1026
Sybirska E, Gorska T (1980) Effects of red nucleus lesions on forelimb movements in the cat. Acta Neurobiol Exp 40: 821–841
Tsukahara N, Toyama K, Kosaka K, Udo M (1965) “Disfacilition” of red nucleus neurons. Experentia (Basel) 21: 533–545
Tsukahara N, Fuller DR, Brooks VB (1968) Collateral pyramidal influences of the corticospinal system. J Neurophysiol 31: 467–484
Viullon-Cacciutolo G, Bosler O, Nieoullon A (1984) GABA neurons in the cat red nucleus: a biochemical and immunohistochemical demonstration. Neurosci Lett 52: 129–134
Viullon-Cacciutolo G, Bosler A, Nieoullon A (1986) Immunohisto-chemical evidence of plasticity of gamma-aminobutyric acid neurons in the red nucleus and adjacent reticular formation after contralateral cerebellectomy in the adult cat. Neurosci Lett 70: 308–313
Wolfarth S, Kolasiewicz W, Sontag KH (1981) The effects of muscimol and picrotoxin injections into the cat substantia nigra. Naunyn-Schmiedeberg's Arch Pharmacol 317: 54–60
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Schmied, A., Amalric, M., Dormont, J.F. et al. GABAergic control of rubral single unit activity during a reaction time task. Exp Brain Res 84, 285–296 (1991). https://doi.org/10.1007/BF00231448
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00231448