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Firing of spinal motoneurones due to electrical interaction in the rat: An in vitro study

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Summary

The excitatory interaction between spinal motoneurones was investigated by means of electromyogram (EMG) recordings from hindlimb muscles as well as intracellular ones from their innervating motoneurones in the isolated preparation of immature rats.

Stimulation of the muscle nerve to biceps femoris or medial gastrocnemius or of the L5 ventral root evoked early and late EMG responses in the muscle of the preparations with the dorsal roots cut. The early response was produced directly by volleys in the motor nerve. The late response was of spinal origin, since it disappeared after the severance of the ventral root. The thresholds and the conduction velocities of nerve fibres, which conducted the centripetal impulse causing the late response, were compatible with those of motor nerve fibres. The amplitude of the late response was 5–10% of that of the maximum early EMG response.

Intracellular recordings from spinal motoneurones revealed that stimulation of the ventral root elicited the double discharge composed of antidromic and delayed spike potentials. The delayed spike was never evoked after the spike potential elicited directly by a short depolarizing pulse. The double discharge was observed in about 6% of the motoneurones examined. The threshold of the stimulus intensity evoking the double discharge was in the range of those of motor nerve fibres. The latencies of the delayed excitation were 7.0–9.0 ms, comparable to the intraspinal delays of the late EMG response.

Stimulation of the ventral root at intensities subthreshold for antidromic activation was found to produce a small depolarizing potential in about 60% of the motoneurones examined. The amplitudes were 0.5–5.0 mV, and the onset and the peak latencies 2.0–7.0 ms and 5.0–8.0 ms, respectively. The potential was unaffected by the deficiency of calcium ions in the perfusing medium and persisted after the degeneration of the afferent fibres in the ventral root. It was thus concluded that the depolarizing potential was generated by electrical synapses between motoneurones.

In a few motoneurones the electrical synaptic potential was found to elicit spike potentials. Latencies of these spikes were similar to those of the delayed excitation in motoneurones with the double discharge. The time course of changes in the excitability in these motoneurones showed that the delayed excitation, hence the late EMG response, was also caused by the electrical synaptic potential.

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References

  • Arasaki K, Kudo N, Nakanishi T (1983) A recurrent discharge in the immature rat as a model of the human F response. Electroencephalogr Clin Neurophysiol (in press)

  • Coggeshall RE (1980) Law of separation of function of the spinal roots. Physiol Rev 60: 716–755

    Google Scholar 

  • Collins III WF (1983) Organization of electrical coupling between frog lumbar motoneurons. J Neurophysiol 49: 730–744

    Google Scholar 

  • Coombs JS, Curtis DR, Eccles JC (1957) The interpretation of spike potentials of motoneurones. J Physiol (Lond) 139: 198–231

    Google Scholar 

  • Dawson GD, Merton PA (1956) “Recurrent” discharges from motoneurones. Abstract. 20th International Congress of Physiology., Brussels, pp 221–222

  • Dimsdale JA, Kemp JM (1966) Afferent fibres in ventral nerve roots in the rat. J Physiol (Lond) 187: 25p-26p

    Google Scholar 

  • Eccles JC, Fatt P, Koketsu K (1954) Cholinergic and inhibitory synapses in a pathway from motor-axon collaterals to motoneurones. J Physiol (Lond) 126: 524–562

    Google Scholar 

  • Eccles JC (1955) The central action of antidromic impulses in motor nerve fibres. Pflügers Arch 260: 385–415

    Google Scholar 

  • Fulton BP, Miledi R, Takahashi T (1980) Electrical synapses between motoneurons in the spinal cord of the newborn rat. Proc R Soc Lond [Biol] 208: 115–120

    Google Scholar 

  • Gassel MM, Wiesendanger M (1965) Recurrent and reflex discharges in plantar muscles of the cat. Acta Physiol Scand 65: 138–142

    Google Scholar 

  • Gogan P, Gueritaud JP, Horcholle-Bassavit G, Tyc-Dumont S (1977) Direct excitatory interactions between spinal motoneurones of the cat. J Physiol (Lond) 272: 755–767

    Google Scholar 

  • Granit R, Kernell D, Smith RS (1963) Delayed depolarization and the repetitive response to intracellular stimulation of mammalian motoneurones. J Physiol (Lond) 168: 890–910

    Google Scholar 

  • Grinnell AD (1966) A study of the interaction between motoneurones in the frog spinal cord. J Physiol (Lond) 182: 612–648

    Google Scholar 

  • Harada Y, Takahashi T (1983) The calcium component of the action potential in spinal motoneurones of the rat. J Physiol (Lond) 335: 89–100

    Google Scholar 

  • Kato M, Hirata Y (1968) Sensory neurons in the spinal ventral roots of the cat. Brain Res 7: 479–482

    Google Scholar 

  • Kubota K, Brookhart JM (1963) Recurrent facilitation of frog motoneurones. J Neurophysiol 26: 877–893

    Google Scholar 

  • Kuno M, Llinás R (1970) Enhancement of synaptic transmission by dendritic potentials in chromatolysed motoneurones of the cat. J Physiol (Lond) 210: 807–821

    Google Scholar 

  • Lloyd DPC (1943) The interaction of antidromic and orthodromic volleys in a segmental spinal motor nucleus. J Neurophysiol 6: 143–151

    Google Scholar 

  • Loeb GE (1976) Ventral root projections of myelinated dorsal root ganglion cells in the cat. Brain Res 106: 159–165

    Google Scholar 

  • Magherini PC, Precht W, Schwindt PC (1976) Evidence for electrotonic coupling between frog motoneurons in the in situ spinal cord. J Neurophysiol 39: 474–483

    Google Scholar 

  • Magladery JW, McDougal DB Jr (1950) Electrophysiological studies of nerve and reflex activity in normal man. I. Identification of certain reflexes in the electromyogram and the conduction velocity of peripheral nerve fibers. Bull Johns Hopk Hosp 86: 265–290

    Google Scholar 

  • Mayer RF, Feldman RG (1967) Observations on the nature of the F wave in man. Neurology (NY) 17: 147–156

    Google Scholar 

  • Maynard CW, Leonard RB, Coulter JD, Coggeshall RE (1977) Central connections of ventral root afferents as demonstrated by the HRP method. J Comp Neurol 172: 601–608

    Google Scholar 

  • McLeod JG, Wray SH (1966) An experimental study of the F wave in the baboon. J Neurol Neurosurg Psychiat 29: 196–200

    Google Scholar 

  • Nelson PG (1966) Interaction between spinal motoneurons of the cat. J Neurophysiol 29: 275–287

    Google Scholar 

  • Nelson PG, Burke RE (1967) Delayed depolarization in cat spinal motoneurons. Exp Neurol 17: 16–26

    Google Scholar 

  • Otsuka M, Konishi S (1974) Electrophysiology of mammalian spinal cord in vitro. Nature (Lond) 252: 733–734

    Google Scholar 

  • Renshaw B (1941) Influence of discharge of motoneurons upon excitation of neighboring motoneurons. J Neurophysiol 4: 167–183

    Google Scholar 

  • Shapovalov AI, Shiriaev BI (1978) Two types of electrotonic EPSP evoked in amphibian motoneurons by ventral root stimulation. Exp Brain Res 33: 313–323

    Google Scholar 

  • Sonnhof U, Richter DW, Taugner R (1977) Electrotonic coupling between spinal motoneurons. An electrophysiological and morphological study. Brain Res 138: 197–215

    Google Scholar 

  • Spencer WA, Kandel ER (1961) Electrophysiology of hippocampal neurons. IV. Fast prepotentials. J Neurophysiol 24: 272–285

    Google Scholar 

  • Webber RH, Wemett A (1966) Distribution of fibers from nerve cell bodies in ventral roots of spinal nerves. Acta Anat (Basel) 65: 579–583

    Google Scholar 

  • Westerfield M, Frank E (1982) Specificity of electrical coupling among neurons innervating forelimb muscles of the adult bullfrog. J Neurophysiol 48: 904–913

    Google Scholar 

  • Wilson VJ (1959) Recurrent facilitation of spinal reflexes. J Gen Physiol 42: 703–713

    Google Scholar 

  • Wilson VJ, Burgess PR (1962) Disinhibition in the cat spinal cord. J Neurophysiol 25: 392–404

    Google Scholar 

  • Windle WF (1931) Neurons of the sensory type in the ventral roots of man and other mammals. Arch Neurol Psychiat (Chic) 26: 791–800

    Google Scholar 

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Arasaki, K., Kudo, N. & Nakanishi, T. Firing of spinal motoneurones due to electrical interaction in the rat: An in vitro study. Exp Brain Res 54, 437–445 (1984). https://doi.org/10.1007/BF00235469

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  • DOI: https://doi.org/10.1007/BF00235469

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