Skip to main content
Log in

Voltage-dependent excitation of motoneurones from spinal locomotor centres in the cat

  • Original Paper
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

Lumbar motoneurones were recorded intracellularly during fictive locomotion induced by stimulation of the mesencephalic locomotor region in decerebrate cats. After blocking the action potentials using intracellular QX-314, and by using a discontinuous current clamp, it is shown that the excitatory component of the locomotor drive potentials behaves in a voltage-dependent manner, such that its amplitude increases with depolarisation. As the input to motoneurones during locomotion is comprised of alternating excitation and inhibition, it was desirable to examine the excitatory input in relative isolation. This was accomplished in spinalised decerebrate cats treated with nialamide and l-dihydroxy-phenylalanine (l-DOPA) by studying the excitatory post-synaptic potentials (EPSPs) evoked from the “flexor reflex afferents” (FRA) and extensor Ib afferents, both of which are likely to be mediated via the locomotor network. As expected, these EPSPs also demonstrate a voltage-dependent increase in amplitude. In addition, the input to motoneurones from the network for scratching, which is thought to share interneurones with the locomotor network, also results in voltage-dependent excitation. The possible underlying mechanisms of NMDA-mediated excitation and plateau potentials are discussed:both may contribute to the observed effect. It is suggested that this nonlinear increase in excitation contributes to the mechanisms involved in the production of the high rates of repetitive firing of motoneurones typically seen during locomotion, thus ensuring appropriate muscle contraction.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Barajon I, Gossard J-P, Hultborn H (1992) Induction of fos expression by activity in the spinal rhythm generator for scratching. Brain Res 588:168–172

    Google Scholar 

  • Berger AJ, Takahashi T (1990) Serotonin enhances a low-voltage-activated calcium current in rat spinal motoneurons. J Neurosci 10:1922–1928

    Google Scholar 

  • Berkinblit MB, Deliagina TG, Feldman AG, Gelfand IM, Orlovsky N (1978) Generation of scratching. II. Nonregular regimes of generation. J Neurophysiol 41:1058–1069

    Google Scholar 

  • Brownstone R, Hultborn H (1992) Regulated and intrinsic properties of the motoneurone: effect on input-output relations. In: Jami L, Pierrot-Deseilligny E, Zytnicki D (eds) Muscle afferents and spinal control of movements. Pergamon, Cambridge, pp 175–181

    Google Scholar 

  • Brownstone RM, Engberg I, Gosssard J-P, Hultborn H (1991a) Voltage-dependent excitation of motoneurones from spinal centres during fictive locomotion in the cat. Soc Neurosci Abstr 17:1028

    Google Scholar 

  • Brownstone RM, Gossard J-P, Hultborn H (1991b) Voltage-dependency of the motoneuronal locomotor drive potentials during fictive locomotion in the decerebrate cat (abstract). J Physiol (Lond) 438:216P

    Google Scholar 

  • Brownstone RM, Jordan LM, Kriellaars DJ, Noga BR, Shefchyk SJ (1992) On the regulation of repetitive firing in lumbar motoneurones during fictive locomotion in the cat. Exp Brain Res 90:441–455

    Google Scholar 

  • Conway BA, Hultborn H, Kiehn O (1987) Proprioceptive input resets central locomotor rhythm in the spinal cat. Exp Brain Res 68:643–656

    Google Scholar 

  • Conway BA, Hultborn H, Kiehn O, Mintz I (1988) Plateau potentials in alpha-motoneurones induced by intravenous injection of l-DOPA and clonidine in the spinal cat. J Physiol (Lond) 405:369–384

    Google Scholar 

  • Dale N (1986) Excitatory synaptic drive for swimming mediated by amino acid receptors in the lamprey. J Neurosci 6:2662–2675

    Google Scholar 

  • Dale N, Roberts A (1985) Dual-component amino-acid-mediated synaptic potentials: excitatory drive for swimming in Xenopus embryos. J Physiol (Lond) 363:35–59

    Google Scholar 

  • Domer FR, Feldberg W (1960) Scratching movements and facilitation of the scratch reflex produced by tubocurarine in cats. J Physiol (Lond) 153:35–51

    Google Scholar 

  • Douglas JR, Noga BR, Dai X, Jordan LM (1993) The effects of intrathecal administration of excitatory amino acid agonists and antagonists on the initiation of locomotion in the adult cat. J Neurosci 13:990–1000

    Google Scholar 

  • Frazier DT, Narahashi T Yamada M (1970) The site of action and active form of local anesthetics. II. Experiments with quaternary compounds. J Pharmacol Exp Ther 171:45–51

    Google Scholar 

  • Gossard J-P, Brownstone RM, Barajon I, Hultborn H (1994) Transmission in a locomotor-related group Ib pathway from hindlimb extensor muscles in the cat. Exp Brain Res 98:213–228

    Google Scholar 

  • Gossard J-P, Hultborn H, Barajon I, Kiehn O, Conway B (1990) Phasic modulation of EPSPs in extensor motoneurones evoked by Ib input during fictive locomotion in the spinal cat. Soc Neurosci Abstr 16:890

    Google Scholar 

  • Hoffer JA, Sugano N, Loeb GE, Marks WB, O'Donovan MJ, Pratt CA (1987) Cat hindlimb motoneurons during locomotion. II. Normal activity patterns. J Neurophysiol 57:530–553

    Google Scholar 

  • Hounsgaard J, Hultborn H, Jespersen B, Kiehn O (1988) Bistability of alpha-motoneurones in the decerebrate cat and in the acute spinal cat after intravenous 5-hydroxytryptophan. J Physiol (Lond) 405:345–367

    Google Scholar 

  • Hounsgaard J, Kiehn O (1989) Serotonin-induced bistability of turtle motoneurones caused by a nifedipine-sensitive calcium plateau potential. J Physiol (Lond) 414:265–282

    Google Scholar 

  • Hultborn H, Kiehn O (1992) Neuromodulation of vertebrate motor neuron membrane properties. Curr Opin Neurobiol 2:770–775

    Google Scholar 

  • Jankowska E (1992) Interneuronal relay in spinal pathways from proprioceptors. Prog Neurobiol 38:335–378

    Article  CAS  PubMed  Google Scholar 

  • Jankowska E, Jukes MGM, Lund S, Lundberg A (1967) The effect of DOPA on the spinal cord. 5. Reciprocal organization of pathways transmitting excitatory action to alpha motoneurones of flexors and extensors. Acta Physiol Scand 70:369–388

    Google Scholar 

  • Jiang ZG, Shen E, Dun NJ (1990) Excitatory and inhibitory transmission from dorsal root afferents to neonate rat motoneurons in vitro. Brain Res 535:110–118

    Google Scholar 

  • Jordan LM (1983) Factors determining motoneuron rhythmicity during fictive locomotion. In: Roberts A, Roberts B (eds) Neural origin of rhythmic movements. Symp Soc Exp Biol 37:423–444

  • Jordan LM, Brownstone RM, Noga BR (1992) Control of functional systems in the brainstem and spinal cord. Curr Opin Neurobiol 2:794–801

    Google Scholar 

  • Julien C, Rossignol S (1982) Electroneurographic recordings with polymer cuff electrodes in paralysed cats. J Neurosci Methods 5:267–272

    Google Scholar 

  • Katakura N, Chandler SH (1990) An iontophoretic analysis of the pharmacologic mechanisms responsible for trigeminal motoneuronal discharge during masticatory-like activity in the guinea pig. J Neurophysiol 63:356–369

    Google Scholar 

  • Kernell D (1986) Organization and properties of spinal motoneurones and motor units. Prog Brain Res 64:21–30

    Google Scholar 

  • Lundberg A (1979) Multisensory control of spinal reflex pathways. Prog Brain Res 50:11–28

    Google Scholar 

  • Nowak L, Bregestovski P, Ascher P, Herbet A, Prochiantz A (1984) Magnesium gates glutamate-activated channels in mouse central neurones. Nature 307:462–465

    Google Scholar 

  • Perret C (1983) Centrally generated patterns of motoneuron activity during locomotion in the cat. In: Roberts A, Roberts B (eds) Neural origin of rhythmic movements. Symp Soc Exp Biol 37:405–422

  • Pinco M, Lev-Tov A (1993) Synaptic exciation of alpha-motoneurons by dorsal root afferents in the neonatal rat spinal cord. J Neurophysiol 70:406–417

    Google Scholar 

  • Schmidt BJ, Smith JC, Feldman JL (1989) Involvement of excitatory amino acids (EAAs) in neurotransmission of rhythmic excitatory drive to motoneurons during locomotion in the rat spinal cord in vitro. Soc Neurosci Abstr 15:505

    Google Scholar 

  • Schomburg ED, Petersen N, Barajon I, Hultborn H (1993) Flexor reflex afferents (FRA) reset the step cycle during fictive locomotion in the cat (abstract). Acta Physiol Scand 149:22A

    Google Scholar 

  • Schwindt PC, Crill WE (1984) Membrane properties of cat spinal motoneurons. In: Davidoff R (ed) Handbook of the spinal cord. M Dekker, New York, pp 199–242

    Google Scholar 

  • Severin FV, Shik ML, Orlovskii GN (1967) Work of the muscles and single motor neurones during controlled locomotion. Biofizika 12:762–772

    Google Scholar 

  • Sherrington CS (1906) Observation of the scratch-reflex in the spinal dog. J Physiol (Lond) 34:1–50

    Google Scholar 

  • Shik MI, Severin FV, Orlovskii GN (1966) Control of walking and running by means of electrical stimulation of the mid-brain. Biofizika 11:659–666

    Google Scholar 

  • Wang YT, Bieger D, Neuman RS (1991) Activation of NMDA receptors is necessary for fast information-transfer at brainstem vagal motoneurons. Brain Res 567:260–266

    Google Scholar 

  • Wilson WA, Goldner MM (1975) Voltage clamping with a single microelectrode. J Neurobiol 6:411–422

    Google Scholar 

  • Zajac FE, Young JL (1980) Discharge properties of hindlimb motoneurons in decerebrate cats during locomotion induced by mesencephalic stimulation. J Neurophysiol 43:1221–1235

    Google Scholar 

  • Ziskind-Connheim L (1990) NMDA receptors mediate poly- and monosynaptic potentials in motoneurons of rat embryos. J Neurosci 10:125–135

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Brownstone, R.M., Gossard, J.P. & Hultborn, H. Voltage-dependent excitation of motoneurones from spinal locomotor centres in the cat. Exp Brain Res 102, 34–44 (1994). https://doi.org/10.1007/BF00232436

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00232436

Key words

Navigation