Summary
A hypothesis is forwarded regarding the role of secondary spindle afferents and the FRA (flexor reflex afferents) in motor control. The hypothesis is based on evidence (cf. Lundberg et al. 1987a, b) summarized in 9 introductory paragraphs. Group II excitation. It is postulated that subsets of excitatory group II interneurones (transmitting disynaptic group II excitation to motoneurones) may be used by the brain to mediate motor commands. It is assumed that the brain selects subsets of interneurones with convergence of secondary afferents from muscles whose activity is required for the movement. During movements depending on coactivation of static γ-motoneurones impulses in secondary afferents may servo-control transmission to α-motoneurones at an interneuronal level. The large group II unitary EPSPs in interneurones are taken to indicate that, given an adequate interneuronal excitability, impulses in single secondary afferents may fire the interneurone and produce EPSPs in motoneurones; interneuronal transmission would then be equivalent to that in a monosynaptic pathway but with impulses from different muscles combining into one line. It is postulated that impulses in the FRA are evoked by the active movements and that the role of the multisensory convergence from the FRA onto the group II interneurones is to provide the high background excitability which allows the secondary spindle afferents to operate as outlined above. The working hypothesis is put forward that a movement governed by the excitatory group II interneurones is initiated by descending activation of these interneurones, but is maintained in a later phase by the combined effect of FRA activity evoked by the movement and by spindle secondaries activated by descending activation of static γ-motoneurones. As in the original “follow up length servo” hypothesis (Rossi 1927; Merton 1953), we assume that a movement at least in a certain phase can be governed from the brain solely or mainly via static γ-motoneurones. However, our hypothesis implies that the excitatory group II reflex connexions have a strength which does not allow transmission to motoneurones at rest and that the increase in the gain of transmission during an active movement is supplied by the movement itself. Group II inhibition. It is suggested that the inhibitory reflex pathways like the excitatory ones have subsets of interneurones with limited group II convergence. When higher centres utilize a subset of excitatory group II interneurones to evoke a given movement, they may mobilize inhibitory subsets to inhibit muscles not required in the movement. Inhibition may be reciprocal of extensors during flexor activation (the spinal pattern), of flexors during extensor activation or of flexors and extensors in more complex movements involving cocontraction of other flexors and extensors. It is postulated that group II inhibition depends on conjoint activation from spindle afferents and other sources (descending and/or the FRA) so that inhibition may be coupled to group II excitation of other motoneurones. Such a coupling would correspond to the “α-γ-linkage in reciprocal Ia inhibition” (Lundberg 1970) and is denoted “α-γ-linkage in lateral group II inhibition”. FRA and other reflex pathways. Results are summarized showing that the FRA evoke convergent excitation in interneurones not only in group II reflex pathways but also in other reflex pathways like the reciprocal Ia inhibitory, the nonreciprocal group I inhibitory and probably also in specialized reflex pathways from cutaneous afferents. It is inferred that facilitation of reflex transmission by impulses in the FRA evoked by the active movement may be a general principle. In this way reflex transmission to α-motoneurones may be weak at rest and not disturb passive movements but have a high gain when the reflexes are required to regulate active movement.
Similar content being viewed by others
References
Andersson G, Sjölund B (1978) The ventral spino-olivocerebellar system in the cat. IV. Spinal transmission after administration of Clonidine and l-DOPA. Exp Brain Res 33: 227–240
Baldissera F, Hultborn H, Illert M (1981) Integration in spinal neuronal systems. In: Brooks VB (ed) Handbook of physiology, Sect I. The nervous system, Vol II. Motor control. Am Physiol Soc, Bethesda, MD, pp 509–595
Bergego C, Pierrot-Deseilligny E, Mazieres L (1981) Facilitation of transmission in Ib pathways by cutaneous afferents from the contralateral foot sole in man. Neurosci Lett 27: 297–301
Bernstein N (1967) The coordination and regulation of movements. Pergamon Press, Oxford
Binder MD, Houk JC, Nichols TR, Rymer WZ, Stuart DG (1982) Properties and segmental actions of mammalian muscle receptors: an update. Fed Proc 41: 2907–2918
Brink E, Jankowska E, McCrea DA, Skoog B (1983) Inhibitory interactions between interneurones in reflex pathways from group Ia and group Ib afferents in the cat. J Physiol (Lond) 343: 361–373
Brown AG (1981) Organization in the spinal cord. Springer, Berlin Heidelberg New York
Carpenter D, Engberg I, Funkenstein H, Lundberg A (1963) Decerebrate control of reflexes to primary afferents. Acta Physiol Scand 59: 424–437
Cooke JD, Larson B, Oscarsson O, Sjölund B (1971) Organization of afferent connections to cuneocerebellar tract. Exp Brain Res 13: 359–377
Eccles JC, Eccles RM, Lundberg A (1960) Types of neurone in and around the intermediate nucleus of the lumbosacral cord. J Physiol (Lond) 154: 89–114
Eccles JC, Kostyuk PG, Schmidt RF (1962) Presynaptic inhibition of the central actions of flexor reflex afferents. J Physiol (Lond) 161: 258–281
Eccles RM, Holmqvist B, Voorhoeve PE (1964) Presynaptic depolarization of cutaneous afferents by volleys in contralateral muscle afferents. Acta Physiol Scand 62: 474–484
Eccles RM, Lundberg A (1958) Integrative patterns of Ia synaptic actions on motoneurones of hip and knee muscles. J Physiol (Lond) 144: 271–298
Eccles RM, Lundberg A (1959) Synaptic actions in motoneurones by afferents which may evoke the flexion reflex. Arch Ital Biol 97: 199–221
Ellaway PH, Murphy PR, Tripathi A (1982) Closely coupled excitation of γ-motoneurones by group III muscle afferents with low mechanical threshold in the cat. J Physiol (Lond) 331: 481–498
Engberg I (1964) Reflexes to foot muscles in the cat. Acta Physiol Scand 62: Suppl 235
Fedina L, Hultborn H (1972) Facilitation from ipsilateral primary afferents of interneuronal transmission in the Ia inhibitory pathway to motoneurones. Acta Physiol Scand 86: 59–81
Fedina L, Hultborn H, Illert M (1975) Facilitation from contralateral primary afferents of interneuronal transmission in the Ia inhibitory pathway to motoneurones. Acta Physiol Scand 94: 198–221
Foster M (1879) A text book of physiology. Macmillan and Co, London
Fu TC, Schomburg ED (1974) Electrophysiological investigation of the projection of secondary muscle spindle afferents in the cat spinal cord. Acta Physiol Scand 91: 314–329
Ghez C, Kubota K (1977) Activity of red nucleus neurons associated with a skilled forelimb movement in the cat. Brain Res 129: 383–388
Ghez C, Vicario D (1978) The control of rapid limb movement in the cat. II. Scaling of isometric force adjustments. Exp Brain Res 33: 191–202
Granit R (1955) Receptors and sensory perception. Yale University Press, New Haven
Harrison PJ, Jankowska E (1985a) Sources of input to interneurones mediating group I non-reciprocal inhibition of motoneurones in the cat. J Physiol (Lond) 361: 379–401
Harrison PJ, Jankowska E (1985b) Organization of input to the interneurones mediating group I non-reciprocal inhibition of motoneurones in the cat. J Physiol (Lond) 361: 403–418
Holmqvist B (1961) Crossed spinal reflex actions evoked by volleys in somatic afferents. Acta Physiol Scand 52: Suppl 181
Holmqvist B, Lundberg A (1961) Differential supraspinal control of synaptic actions evoked by volleys in the flexion reflex afferents in alpha motoneurones. Acta Physiol Scand 54: Suppl 186
Hongo T, Okada Y (1967) Cortically evoked prend postsynaptic inhibition of impulse transmission to the dorsal spinocerebellar tract. Exp Brain Res 3: 163–177
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
Hongo T, Jankowska E, Lundberg A (1968) Post-synaptic excitation and inhibition from primary afferents in neurones of the spinocervical tract. J Physiol (Lond) 199: 569–592
Hongo T, Jankowska E, Lundberg A (1969) The rubrospinal tract. II. Facilitation of interneuronal transmission in reflex paths to motoneurones. Exp Brain Res 7: 365–391
Hongo T, Jankowska E, Lundberg A (1972) The rubrospinal tract. IV. Effects on interneurones. Exp Brain Res 15: 54–78
Hongo T, Kudo N, Yamashita M, Ishizuka N, Mannen H (1981) Transneuronal passage of intraaxonally injected horseradish peroxidase (HRP) from group Ib and II fibres into the secondary neurons in the dorsal horn of the cat spinal cord. Biomed Res 2: 722–727
Hongo T, Ishizuka N, Kudo N, Mannen H, Sasaki S, Yamashita M (1983a) Intraspinal morphology of group II muscle spindle afferents. Abstract. Symp. Reflex organization of the spinal cord and its descending control. Canberra, Australia
Hongo T, Jankowska E, Ohno T, Sasaki S, Yamashita M, Yoshida K (1983b) Inhibition of dorsal spinocerebellar tract cells by interneurones in upper and lower lumbar segments in the cat. J Physiol (Lond) 342: 145–160
Hongo T, Lundberg A, Phillips CG, Thompson RF (1984) The pattern of monosynaptic Ia-connections to hindlimb motor nuclei in the baboon: a comparison with the cat. Proc R Soc Lond B 221: 261–289
Hulliger M (1984) The mammalian muscle spindle and its central control. Rev Physiol Biochem Pharmacol 101: 1–110
Hultborn H (1972) Convergence on interneurones in the reciprocal Ia inhibitory pathway to motoneurones. Acta Physiol Scand 85: Suppl 375
Hultborn H (1976) Transmission in the pathway of reciprocal Ia inhibition to motoneurones and its control during the tonic stretch reflex. In: Homma S (ed) Understanding the stretch reflex. Prog Brain Res 44: 235–255
Hultborn H, Illert M, Santini M (1976a) Convergence on interneurones mediating the reciprocal Ia inhibition of motoneurones. II. Effects from segmentai flexor reflex pathways. Acta Physiol Scand 96: 351–367
Hultborn H, Illert M, Santini M (1976b) Convergence on interneurones mediating the reciprocal Ia inhibition of motoneurones. III. Effects from supraspinal pathways. Acta Physiol Scand 96: 368–391
Hultborn H, Jankowska E, Lindström S (1971) Recurrent inhibition from motor axon collaterals of transmission in the Ia inhibitory pathway to motoneurones. J Physiol (Lond) 215: 591–612
Jankowska E, Jukes MGM, Lund S, Lundberg A (1967a) 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
Jankowska E, Jukes MGM, Lund S, Lundberg A (1967b) The effect of DOPA on the spinal cord. 6. Half-centre organization of interneurones transmitting effects from the flexor reflex afferents. Acta Physiol Scand 70: 389–402
Jankowska E, Lundberg A, Stuart D (1973) Propriospinal control of last order interneurones of spinal reflex pathways in the cat. Brain Res 53: 227–231
Kniffki KD, Mense S, Schmidt RF (1981) Muscle receptors with fine afferent fibers which may evoke circulatory reflexes. Circ Res 48, Suppl I: 25–31
Lloyd DPC (1943) Neuron patterns controlling transmission of ipsilateral hind limb reflexes in cat. J Neurophysiol 6: 293–315
Lloyd DPC (1946) Integrative pattern of excitation and inhibition in two-neuron reflex arcs. J Neurophysiol 9: 439–444
Lundberg A (1959) Integrative significance of patterns of connections made by muscle afferents in the spinal cord. Symp XXI Int Physiol Congr, Buenos Aires, pp 1–5
Lundberg A (1964a) Ascending spinal hindlimb pathways in the cat. In: Eccles JC, Schadé JP (eds) Physiology of spinal neurons. Prog Brain Res 12: 135–163
Lundberg A (1964b) Supraspinal control of transmission in reflex paths to motoneurones and primary afferents. In: Eccles JC, Schadé JP (eds) Physiology of spinal neurons. Prog Brain Res 12: 197–221
Lundberg A (1970) The excitatory control of the Ia inhibitory pathway. In: Andersen P, Jansen JKS (eds) Excitatory synaptic mechanisms. Universitetsforlaget, Oslo, pp 333–340
Lundberg A (1971) Function of the ventral spinocerebellar tract. A new hypothesis. Exp Brain Res 12: 317–330
Lundberg A (1973) The significance of segmental spinal mechanisms in motor control. Symp. 4th International Biophysics Congress, Moscow
Lundberg A (1979) Multisensory control of spinal reflex pathways. In: Granit R, Pompeiano O (eds) Reflex control of posture and movement. Prog Brain Res 50: 11–28
Lundberg A (1981) Half-centres revisited. In: Szentágothai J, Palkovits M, Hámori J (eds) Regulatory functions of the CNS. Motion and organization principles. Adv Physiol Sci 1: 155–167
Lundberg A (1982) Inhibitory control from the brain stem of transmission from primary afferents to motoneurons, primary afferent terminals and ascending pathways. In: Sjölund B, Björklund A (eds) Brain stem control of spinal mechanisms. Elsevier Biomedical Press, Amsterdam New York, pp 179–224
Lundberg A, Malmgren K, Schomburg ED (1977) Cutaneous facilitation of transmission in reflex pathways from Ib afferents to motoneurones. J Physiol (Lond) 265: 763–780
Lundberg A, Malmgren K, Schomburg ED (1978) Role of joint afferents in motor control exemplified by effects on reflex pathways from Ib afferents. J Physiol (Lond) 284: 327–343
Lundberg A, Malmgren K, Schomburg ED (1987a) Reflex pathways from group II muscle afferents. I. Distribution and linkage of reflex actions to α-motoneurones. Exp Brain Res 65: 271–281
Lundberg A, Malmgren K, Schomburg ED (1987b) Reflex pathways from group II muscle afferents. 2. Functional characteristics of reflex pathways to α-motoneurones. Exp Brain Res 65: 282–293
Lundberg A, Norrsell U, Voorhoeve P (1963) Effects from the sensorimotor cortex on ascending spinal pathways. Acta Physiol Scand 59: 462–473
Lundberg A, Oscarsson O (1960) Functional organization of the dorsal spino-cerebellar tract in the cat. VII. Identification of units by antidromic activation from the cerebellar cortex with recognition of five functional subdivisions. Acta Physiol Scand 50: 356–374
Lundberg A, Oscarsson O (1961) Three ascending spinal pathways in the dorsal part of the lateral funiculus. Acta Physiol Scand 51: 1–16
Lundberg A, Oscarsson O (1962) Two ascending spinal pathways in the ventral part of the cord. Acta Physiol Scand 54: 270–286
Lundberg A, Voorhoeve P (1962) Effects from the pyramidal tract on spinal reflex arcs. Acta Physiol Scand 56: 201–219
Matthews PBC (1972) Mammalian muscle receptors and their central actions. Edward Arnold Publ Ltd, London
Merton PA (1951) The silent period in a muscle of the human hand. J Physiol (Lond) 114: 183–198
Merton PA (1953) Speculations on the servo-control of movement. In: Wolstenholme GEW (ed) The spinal cord. Churchill, London, pp 247–255
Oscarsson O (1973) Functional organization of spinocerebellar paths. In: Iggo A (ed) Handbook of sensory physiology, Vol II. Somatosensory systems. Springer, Berlin Heidelberg New York, pp 339–380
Pierrot-Deseilligny E, Bergego C, Katz R, Morin C (1981) Cutaneous depression of Ib reflex pathways to motoneurones in man. Exp Brain Res 42: 351–361
Prochazka A, Hulliger M (1983) Muscle afferent function and its significance for motor control mechanisms during voluntary movements in cat, monkey and man. In: Desmedt JE (ed) Motor control mechanisms in health and disease. Raven, New York, pp 93–132
Rossi G (1927) Asimmetrie toniche posturali, ed asimmetrie motorie. Arch Fisiol 25: 146–157
Sherrington CS (1906) The integrative action of the nervous system. Yale Univ Press, New Haven London
Smith AM, Hepp-Reymond M-C, Wyss UR (1975) Relation of activity in precentral cortical neurons to force and rate of force change during isometric contractions of finger muscles. Exp Brain Res 23: 315–332
Vedel JP, Mouillac-Baudevin J (1970) Contrôle pyramidal de l'activité des fibres fusimotrices dynamiques et statiques chez le chat. Exp Brain Res 10: 39–63
Wilson VJ, Talbot WH, Kato M (1964) Inhibitory convergence upon Renshaw cells. J Neurophysiol 27: 1063–1079
Yokota T, Voorhoeve PE (1969) Pyramidal control of fusimotor neurones supplying extensor muscles in the cat's forelimb. Exp Brain Res 9: 96–115
Author information
Authors and Affiliations
Additional information
This work was supported by the Swedish Medical Research Council (project no. 94)
Rights and permissions
About this article
Cite this article
Lundberg, A., Malmgren, K. & Schomburg, E.D. Reflex pathways from group II muscle afferents. Exp Brain Res 65, 294–306 (1987). https://doi.org/10.1007/BF00236301
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00236301