Skip to main content
Log in

Supraspinal facilitation of cutaneous polysynaptic EPSPs in cat medial gastrocnemius motoneurons

  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Summary

We examined the characteristics of postsynaptic potentials (PSPs) produced in antidromically-identified medial gastrocnemius (MG) α-motoneurons by electrical stimulation of low threshold (< 3×T) distal limb cutaneous afferents in the sural (SUR) nerve in adult cats anesthetized with α-chloralose, together with the effects on SUR PSPs of supraspinal conditioning stimulation of the contralateral red nucleus (RN) and pyramidal tract (PT). In the majority of MG motoneurons, SUR afferents with electrical thresholds < 1.5×T produced early excitatory synaptic potentials (EPSPs) with minimum central latency of about 2.0 ms, suggesting activation of a trisynaptic segmental pathway with two interposed interneurons. Such early EPSPs were often detectable with stimuli < 1.2×T, as determined by recording the compound action potential in the sciatic nerve and from the first appearance of the N1 wave of the cord dorsum potential. Inhibitory synaptic potentials (IPSPs) were regularly produced by SUR volleys of only slightly greater strength (often as low as 1.3×T) and these had minimum central latencies of about 3.0 ms (about 1.0 ms longer than the earliest EPSPs), suggesting a three interneuron central pathway.

Repetitive stimulation of RN and PT regularly produced facilitation of both EPSP and IPSP components in the SUR response, suggesting that these supraspinal systems directly or indirectly excite some of the same interneurons that convey the SUR effects to MG motoneurons. When using very low strength SUR stimuli, PT conditioning produced relatively pure facilitation of the SUR EPSPs but with larger SUR volleys, PT clearly facilitated both EPSPs and IPSPs. RN conditioning produced more parallel facilitation of SUR EPSPs and IPSPs. Supraspinal control of the polysynaptic pathway producing SUR EPSPs is of particular interest because of earlier evidence that this pathway is differentially distributed to motoneurons of fast twitch versus slow twitch MG motor units.

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.

Institutional subscriptions

Similar content being viewed by others

References

  • Baldissera F, Lundberg A, Udo M (1972) Stimulation of pre- and postsynaptic elements in the red nucleus. Exp Brain Res 15: 151–167

    Google Scholar 

  • Baldissera F, ten Bruggencate G, Lundberg A (1971) Rubrospinal monosynaptic connexion with last order interneurones of polysynaptic reflex paths. Brain Res 27: 390–392

    Google Scholar 

  • Burke RE (1967) Motor unit types of cat triceps surae muscle. J Physiol (Lond) 193: 141–160

    Google Scholar 

  • Burke RE (1968) Firing patterns of gastrocnemius motor units in the decerebrate cat. J Physiol (Lond) 196: 631–654

    Google Scholar 

  • Burke RE (1981) Motor units: Anatomy, physiology and functional organization. In: Brooks VB (ed) Handbook of physiology. Section I. The nervous system II. Motor control, part 1. American Physiological Society, Washington, pp 345–422

    Google Scholar 

  • Burke RE, Jankowska E, Bruggencate G ten (1970) A comparison of peripheral and rubrospinal synaptic input to slow and fast twitch motor units of triceps surae. J Physiol 207: 709–732

    Google Scholar 

  • Burke RE, Levine DN, Tsairis P, Zajac FE (1973a) Physiological types and histochemical profiles in motor units of the cat gastrocnemius. J Physiol (Lond) 234: 723–748

    Google Scholar 

  • Burke RE, Rymer WZ, Walsh JV (1973b) Functional specialization in the motor unit population of cat medial gastrocnemius muscle. In: Stein RB, Pearson KB, Smith RS, Redford JB (eds) Control of posture and locomotion. Plenum, New York, pp 29–44

    Google Scholar 

  • Burke RE, Rymer WZ, Walsh JV (1976) Relative strength of synaptic input from short-latency pathways to motor units of defined type in cat medial gastrocnemius. J Neurophysiol 39: 447–458

    Google Scholar 

  • Colebatch JG, Gillies JD (1979) Sural nerve effects on medial gastrocnemius motoneurones in the cat. J Physiol (Lond) 288: 401–410

    Google Scholar 

  • Davis LA, Gordon T, Hoffer JA, Jhamandas J, Stein RB (1978) Compound action potentials recorded from mammalian peripheral nerves following ligation or resuturing. J Physiol (Lond) 285: 543–559

    Google Scholar 

  • Desmedt JE, Godaux E (1978) Ballistic contractions in fast or slow human muscles: Discharge patterns of single motor units. J Physiol (Lond) 285: 185–196

    Google Scholar 

  • Eccles JC (1964) The physiology of synapses. Academic Press, New York

    Google Scholar 

  • Eccles RM, Lundberg A (1959) Synaptic actions in motoneurones by afferents which may evoke the flexion reflex. Arch Ital Biol 97: 199–221

    Google Scholar 

  • Endo K, Araki T, Kawai Y (1975) Contra- and ipsilateral cortical and rubral effects on fast and slow spinal motoneurone of the cat. Brain Res 88: 91–98

    Google Scholar 

  • Engberg I (1964) Reflexes to foot muscles in the cat. Acta Physiol Scand [Suppl 235] 62: 1–64

    Google Scholar 

  • Engberg I, Lundberg A, Ryall RW (1968) Reticulospinal inhibition of transmission in reflex pathways. J Physiol (Lond) 194: 201–223

    Google Scholar 

  • Garnett R, Stephens JA (1981) Changes in the recruitment threshold of motor units produced by cutaneous stimulation in man. J Physiol (Lond) 311: 463–473

    Google Scholar 

  • Henneman E, Clamann HP, Gillies JD, Skinner RD (1974) Rank order of motoneurons within a pool: Law of combination. J Neurophysiol 34: 1338–1349

    Google Scholar 

  • Henneman E, Olson CB (1965) Relations between structure and function in the design of skeletal muscles. J Neurophysiol 28: 581–598

    Google Scholar 

  • Henneman E, Somjen G, Carpenter DO (1965) Functional significance of cell size in spinal motoneurons. J Neurophysiol 28: 560–580

    Google Scholar 

  • Hongo T, Jankowska E, Lundberg A (1966) Convergence of excitatory and inhibitory action on interneurones in the lumbosacral cord. Exp Brain Res 1: 338–358

    Google Scholar 

  • Hongo T, Jankowska E, Lundberg A (1969a) The rubrospinal tract. I. Effects on alpha motoneurons innervating hindlimb muscles in cats. Exp Brain Res 7: 344–364

    Google Scholar 

  • Hongo T, Jankowska E, Lundberg A (1969b) The rubrospinal tract. II. Facilitation of interneuronal transmission in reflex paths to motoneurones. Exp Brain Res 7: 365–391

    Google Scholar 

  • Hongo T, Jankowska E, Lundberg A (1972) The rubrospinal tract. IV. Effects on interneurons. Exp Brain Res 15: 54–78

    Google Scholar 

  • Hultborn H, Illert M, Santini M (1976) Convergence on interneurones mediating the reciprocal Ia inhibition of motoneurones. III. Effects from supraspinal pathways. Acta Physiol Scand 96: 368–391

    Google Scholar 

  • Illert M, Lundberg A, Tanaka R (1976a) Integration in descending motor pathways controlling the forelimb in the cat. 1. Pyramidal effects on motoneurones. Exp Brain Res 26: 509–519

    Google Scholar 

  • Illert M, Lundberg A, Tanaka R (1976b) Integration in descending motor pathways controlling the forelimb in the cat. 2. Convergence on neurones mediating disynaptic cortico-motoneuronal excitation. Exp Brain Res 26: 521–540

    Google Scholar 

  • Kanda K, Burke RE, Walmsley B (1977) Differential control of fast and slow twitch motor units in the decerebrate cat. Exp Brain Res 29: 57–74

    Google Scholar 

  • Kostyuk PG (1976) Supraspinal mechanisms on a spinal level. In: Shahani M (ed) The motor system: neurophysiology and muscle mechanisms. Elsevier, Amsterdam, pp 211–235

    Google Scholar 

  • Loeb GE, Salcman M, Schmidt EM (1977) Parylene as a chronically stable, reproducible microelectrode insulator. IEEE, BME BME-24: 121–128

    Google Scholar 

  • Lundberg A (1969) Convergence of excitatory and inhibitory action on interneurones in the spinal cord. In: Brazier (MAB) The interneuron. UCLA Forum in Medical Sciences. University of California Press, pp 231–265

  • Lundberg A (1975) Control of spinal mechanisms from the brain. In: Brady RO (ed) The nervous system. The basic neurosciences. Raven Press, New York, pp 253–265

    Google Scholar 

  • Lundberg A (1979) Multisensory control of spinal reflex pathways. In: Pompeiano B (ed) Reflex control of posture and movement. Elsevier, Amsterdam (Progress in brain research, vol 50, pp 11–28)

    Google Scholar 

  • Lundberg A, Voorhoeve P (1962) Effects from the pyramidal tract on spinal reflex arcs. Acta Physiol Scand 56: 201–219

    Google Scholar 

  • Pinter MJ, Burke RE, O'Donovan MJ, Dum RP (1980) Supraspinal facilitation of short latency polysynaptic EPSPs produced by low threshold sural nerve afferents in medial gastrocnemius alpha motoneurons. Soc Neurosci Abstr 6: 25

    Google Scholar 

  • Rall W, Burke RE, Smith TG, Nelson PG, Frank K (1967) Dendritic location of synapses and possible mechaisms for the monosynaptic EPSP in motoneurons. J Neurophysiol 30: 1169–1193

    Google Scholar 

  • Rosenberg ME (1970) Synaptic connexions of alpha extensor motoneurones with ipsilateral and contralateral cutaneous nerves. J Physiol (Lond) 207: 231–255

    Google Scholar 

  • Smith JL, Betts B, Edgerton VR, Zernicke RF (1980) Rapid ankle extension during paw shakes: selective recruitment of fast ankle extensors. Neurophysiol 43: 612–620

    Google Scholar 

  • Stephens JA, Garnett R, Buller NP (1978) Reversal of recruitment order of single motor units produced by cutaneous stimulation during voluntary muscle contraction in man. Nature 272: 362–364

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Supported by USPHS Postdoctoral Fellowship 1F32NS 06131

Supported by Muscular Dystrophy Society of America Post-doctoral Fellowship

Supported by USPHS Postdoctoral Fellowship 1F32NS 05677

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pinter, M.J., Burke, R.E., O'Donovan, M.J. et al. Supraspinal facilitation of cutaneous polysynaptic EPSPs in cat medial gastrocnemius motoneurons. Exp Brain Res 45, 133–143 (1982). https://doi.org/10.1007/BF00235772

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00235772

Key words

Navigation