Abstract
Among the natural sensors, which provide proprioceptive feedback during movement, the muscle spindle has attracted most interest since the sensitivity of spindle afferents to length variations of the host muscle is subjected to efferent control by fusimotor neurones (mostly γ-motoneurones). These are themselves controlled from numerous centres of the nervous system. Functionally, the perhaps most important feature of γ-action is that the fusimotor system, with its static (γS, sensitivity reducing) and dynamic (γD, sensitivity enhancing) components, possesses the potential of providing flexible gain (or sensitivity) control of spindle feedback. One of the most relevant pending issues in the field of peripheral control of movement is whether, and under which circumstances, this potential is used during physiological motor performance.
This paper gives a brief overview of important functional properties of the sensory spindle afferents and of efferent fusimotor action and it addresses the question of fusimotor function during natural movement. It is pointed out, that strategies of fusimotor action, which have been encountered in reduced laboratory preparations, appear not be be adhered to during normal motor performance. An alternative concept of fusimotor function, the notion of fusimotor set, is presented. According to this, key features of fusmotor action are
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largely tonic γS and γD firing patterns (even during rhythmic movements, featuring rhythmic skeletomotor α-activity), suggesting independent central control of the skeletomotor and fusimotor systems,
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a dramatic switch from predominant and low-key static action (during routine motor performance) to predominant and powerful dynamic action (during unfamiliar motor tasks),
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gradual resetting of fusimotor drive of a given type during periods of motor adjustment.
Thus, proprioceptive feedback from spindle afferents is not invariant. It appears to be adapted to specific requirements of motor tasks, conceivably to optimize motor control.
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References
Appelberg B (1981) Selective central control of dynamic gamma motoneurones utilised for the functional classification of gamma cells. Ins Taylor A, Prochazka A (eds) Muscle receptors and movement. Macmillan, London, pp 97–107
Appenteng K Prochazka A (1984) Tendon organ firing during active muscle lengthening in awake, normally behaving cats. J Physiol(Lond) 353:81–92
Appenteng K, Morimoto T, Taylor A (1980) Fusimotor activity in masseter nerve of the cat during reflex jaw movements. J Physiol(Lond) 305:415–431
Burgess PR, Clark FJ (1969) Characteristics of knee joint receptors in the cat. J Physiol(Lond) 203:317–335
Burke D (1981) The activity of human muscle spindle endings in normal motor behavior. Int Rev Physiol 20:91–136
Cabelguen JM (1981) Static and dynamic fusimotor controls in various hindlimb muscles during locomotor activity in the decorticate cat. Brain Res 213:83–97
Carli G, Fontani G, Meucci M (1981) Static characteristics of muscle afferents from gluteus medius muscle: comparison with joint afferents of hip in cats. J Neurophysiol 45: 1085–1095
Clark FJ, Burgess PR (1975) Slowly adapting receptors in cat knee joint: can they signal joint angle? J Neurophysiol 36: 1448–1463
Critchlow V, von Euler C (1963) Intercostal muscle spindle activity and its gamma motor control. J Physiol(Lond) 168: 820–847
Eklund G, von Euler C, Rutkowski S (1964) Spontaneous and reflex activity of intercostal gamma motoneurones. J Physiol (Lond) 171:139–163
Evarts EV, Shinoda Y, Wise SP (1984) Neurophysiological approaches to higher brain functions. Wiley, New York
Goodwin GM, Luschei E (1975) Discharge of spindle afferents from jaw closing muscles during chewing in alert monkeys. J Neurophysiol 38: 560–571
Goodwin GM, Hulliger M, Matthews PBC (1975) The effects of fusimotor stimulation during small amplitude stretching on the frequency response of the primary ending of the mammalian muscle spindle. J Physiol(Lond) 253:175–206
Goslow GE, Reinking RM, Stuart DG (1973) The cat step cycle: hind limb joint angles and muscle lengths during unrestrained locomotion. J Morphol 141:1–41
Gottlieb S, Taylor A (1983) Interpretation of fusimotor activity in cat masseter nerve during reflex jaw movements. J Physiol(Lond) 345:423–438
Granit R (1955) Receptors and sensory perception. Yale University Press, New Haven
Hagbarth K-E (1981) Fusimotor and stretch reflex functions studied in recordings from muscle spindle afferents in man. In: Taylor A, Prochazka A (eds) Muscle receptors and movement. Macmillan, London, pp 277–286
Hasan Z (1983) A model of spindle afferent response to muscle stretch. J Neurophysiol 49:989–1006
Hulliger M (1984) The mammalian muscle spindle and its central control. Rev Physiol Biochem Pharmacol 101:1–110
Hulliger M (1986) The role of muscle spindle receptors and fusimotor neurones in the control of movement. Electroenceph Clin Neurophysiol (in press)
Hulliger M,(1986) An iterative and interactive simulation method for reconstruction of unknown inputs contributing to known outputs of neuronal systems (this volume)
Hulliger M, Prochazka A (1983) A new simulation method to deduce fusimotor activity from afferent discharge recorded in freely moving cats. J Neurosci Methods 8:197–204
Hulliger M, Sonnenberg R (1985) Does the paradoxical γD-mediated reduction of la sensitivity to small stretches persist during larger background movements? Neurosci Letters Suppl 22:S595
Hulliger M, Matthews PBC, Noth J, (1977a) Static and dynamic fusimotor action on the response of la fibres to low frequency sinusoidal stretching of widely ranging amplitude. J Physiol(Lond) 267:811–838
Hulliger M, Matthews PBC, Noth J (1977b) Effects of combining static and dynamic fusimotor stimulation on the response of the muscle spindle primary ending to sinusoidal stretching. J Physiol(Lond) 267:839–856
Hulliger M, Zangger P, Prochazka A, Appenteng K (1985) Fusimotor “Set” vs. α-γ linkage in voluntary movement in cats. In: Struppler A, Weindl A (eds) Electromyography and evoked potentials. Adv Appl Neurol Sci Is 56–63
Hulliger M, Prochazka A, Zangger P (1986) Fusimotor activity in freely moving cats. Tests of concepts derived from reduced preparations. In: Grillner S, Stein PSG, Forssberg H, Herman RM, Stuart DG, Wallén P (eds) Neurobiology of vertebrate locomotion. Macmillan, London (in press)
Jansen JKS, Walloe L (1970) Signal transmission between successive neurons in the dorsal spinocerebellar pathway. In: Schmitt FO (ed) The neurosciences, second study program. Rockefeller University Press, New York, pp 617–629
Laporte Y, Emonet-Dénand F, Jami L (1981) The skeletofusimotor or β-innervation of mammalian muscle spindles. TINS 4:97–99
Larson CR, Smith A, Luschei ES (1981) Discharge characteristics and stretch sensitivity of jaw muscle afferents in the monkey during controlled isometric bites. J Neurophysiol 46:130–142
Loeb GE (1984) The control and responses of mammalian muscle spindles during normally executed motor tasks. Exercise Sports Sci Rev 12:157–204
Loeb GE, Hoffer JA (1985) Activity of spindle afferents from cat anterior thigh muscles. II. Effects of fusimotor blockade. J Neurophysiol 54:565–577
Loeb GE, Hoffer JA, Pratt CA (1985) Activity of spindle afferents from cat anterior thigh muscles. I. Identification and patterns during normal locomotion. J Neurophysiol 54:549–564
Matthews PBC (1962) The differentiation of two types of fusimotor fibre by their effects on the dynamic response of muscle spindle primary endings. Q J Exp Physiol 47:324–333
Matthews PBC (1972) Mammalian muscle receptors and their central action. Arnold, London
Matthews PBC (1981a) Evolving views on the internal operation and functional role of the muscle spindle. J Physiol(Lond) 320:1–30
Matthews PBC (1981b) Muscle spindles: their messages and their fusimotor supply. In: Brookhart JM, Mountcastle VB, Brooks VB, (eds) Motor control, part 1. American Physiological Society, Bethesda, pp 189-228 (Handbook of physiology, sect 1, vol 2)
Matthews PBC, Stein RB (1969a) The sensitivity of muscle spindle afferents to small sinusoidal changes of length. J Physiol (Lond) 200:723–743
Matthews PBC, Stein RB (1969b) The regularity of primary and secondary muscle spindle afferent discharges. J Physiol (Lond) 202:59–82
Murphy PR, Stein RB, Taylor J (1984) Phasic and tonic modulation of impulse rates in γ-motoneurons during locomotion in premammillary cats. J. Neurophysiol 52:228–243
Perret C, Berthoz A (1973) Evidence of static and dynamic fusimotor actions on the spindle response to sinusoidal stretch during locomotor activities in the cat. Exp Brain Res 18: 178–188
Prochazka A (1984) Chronic techniques for studying neurophysiology of movement in cats. In: Lemon R, (ed) Methods of neuronal recording in conscious animals. IBRO handbook series: methods in the neurosciences 4. Wiley, Chichester, pp 113–128
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. Adv Neurol 39:93-132
Prochazka A, Hulliger M, Zangger P, Appenteng K (1985) “Fusimotor set”: new evidence for α-independent control of γ- motoneurones during movement in the awake cat. Brain Res 339:136–140
Proske U (1981) The Golgi tendon organ. Properties of the receptor and reflex action of impulses arising from tendon organs. Int Rev Physiol 25:127–171
Rossi A, Grigg P (1982) Characteristics of hip joint mechanoreceptors in the cat. J Neurophysiol 47:1029–1042
Schaible H-G, Schmidt RF (1983) Responses of fine medial articular nerve afferents to passive movement of knee joint. J Neurophysiol 49:1118–1126
Schaible H-G, Schmidt RF (1985) Effects of an experimental arthritis on the sensory properties of fine articular afferent units. J Neurophysiol 54:1109–1122
Schieber MH, Thach WT (1985) Trained slow tracking. II. Bidirectional discharge patterns of cerebellar nuclear, motor cortex, and spindle afferent neurons. J Neurophysiol 54: 1228–1270
Schwarz M, Sontag K-H, Wand P (1984) Non-dopaminergic neurons of the reticular part of substantia nigra can gate static fusimotor action onto flexors in cat. J Physiol(Lond) 354: 333–344
Sears TA (1964) Efferent discharges in alpha and fusimotor fibres of intercostal nerves of the cat. J Physiol(Lond) 174:295–315
Severin FV (1970) The role of the gamma motor system in the activation of the extensor alpha motor neurones during controlled locomotion. Biophysics 15:1138–1145
Severin FV, Orlovskii GN, Shik ML (1967) Work of the muscle receptors during controlled locomotion. Biophysics 12:575–586
Sjöström A, Zangger P (1976) Muscle spindle control during locomotor movements generated by the deafferented spinal cord. Acta Physiol Scand 97:281–291
Stein RB (1974) Peripheral control of movement. Physiol Rev 54:215–243
Taylor A, Appenteng K (1981) Distinctive modes of static and dynamic fusimotor drive in jaw muscles. In: Taylor A, Prochazka A, (eds) Muscle receptors and movement. Macmillan, London, pp 179–192
Taylor J, Stein RB, Murphy PR (1985) Impulse rates and sensitivity to stretch of soleus muscle spindle afferent fibers during locomotion in premammillary cats. J Neurophysiol 53: 341–360
Vallbo ÅB, Hulliger M (1981) Independence of skeletomotor and fusimotor activity in man? Brain Res 223:176–180
Vallbo ÅB, Hagbarth K-E, Torebjork HE, Wallin G (1979) Somatosensory, proprioceptive and sympathetic activity in human peripheral nerves. Physiol Rev 59:919–957
Walmsley B, Hodgson JA, Burke RE (1978) Forces produced by medial gastrocnemius and soleus muscles during locomotion in freely moving cats. J Neurophysiol 41:1203–1216
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© 1988 Springer-Verlag Berlin Heidelberg
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Hulliger, M. (1988). Proprioceptive Feedback for Sensory-Motor Control. In: Dario, P. (eds) Sensors and Sensory Systems for Advanced Robots. NATO ASI Series, vol 43. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-83410-3_2
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DOI: https://doi.org/10.1007/978-3-642-83410-3_2
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