Summary
The activity in α and γ efferent axon populations and in group I and group II afferent fibre populations innervating a flexor muscle, the sartorius medialis, was observed during spontaneous locomotor movements in the thalamic cat. Multi-unit discharges of each kind of fibre were obtained by electronic sorting of the action potentials from the overall activity of a thin, intact branch of the sartorius medialis nerve. The following results were obtained: (1) The γ-motoneurones have a phasic behaviour characterized by a single discharge period during the hip flexion (swing phase of the step-cycle). (2) The γ-motoneurones are co-activated with the homonymous α-motoneurones. (3) Between rhythmic α and γ discharges, i.e. during the hip extension (stance phase of the step cycle), both α- and γ-motoneurones were normally silent. However, in 5 out of 17 experiments, a few units of the γ population fired at very low frequency. (4) Two observations indicate that the γ-motoneurones that are co-activated with the α-motoneurones by central locomotor commands are predominantly of the static type. In actual locomotion, the rhythmic fusimotor discharges over-compensate the depressor effect on the firing rate of the group II afferents of the unloading of muscle spindles by the active shortening of the parent muscle. In fictive locomotion, when the transmission of the excitation is blocked by selective curarization in alpha skeleto-motor junctions alone, the rhythmic fusimotor discharges elicit in-phase modulations not only of the group I but also of the group II fibres. The group II afferent population consists almost entirely of fibres arising from spindle secondary endings which are located primarily on intrafusal muscle fibres whose contraction is exclusively controlled by static fusimotor motoneurones. In the two experimental circumstances, the analysis of the group I fibre discharge does not allow to decide whether dynamic γ motoneurones are firing or silent during rhythmic γ discharge. (5) The group I and group II afferent discharges during the step-cycle showed two frequency peaks, one static-fusimotor dependent while the contracting muscle shortened during the hip flexion (swing) phase, the other length-change dependent while the relaxed muscle was rapidly stretched during the first part of the hip extension (stance) phase. Then, during the second part of hip extension when the muscle was slowly stretched in the absence of fusimotor drive, the firing rate of the spindle afférents decreased to a low level. The spindle sensory endings during the extension phase showed low dynamic and static responsiveness like deefferented spindles. (6) The results obtained in sartorius medialis (flexor) muscle are discussed in comparison with the results previously obtained in gastrocnemii (extensor) muscles (Bessou et al. 1986). The consequences of the predominant activation of the static or dynamic fusimotor system in functionally different muscles are considered with respect to the proprioceptive or motor role of musclespindles during muscle contraction.
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References
Appelberg B, Bessou P, Laporte Y, (1966) Actions of static and dynamic fusimotor fibres on secondary endings of cat's spindles. J Physiol (Lond) 185: 160–171
Bessou P, Cabelguen JM, Montoya R, Pagès B (1986) Efferent and afferent activity in a gastrocnemius nerve branch during locomotion in the thalamic cat. Exp Brain Res 64: 553–568
Bessou P, Dupui Ph, Cabelguen JM, Joffroy M, Montoya R, Pagès B (1990) Discharge patterns of gamma motoneurone populations of extensor and flexor hindlimb muscles during walking in the thalamic cat. In: Allum JHJ, Hulliger M (eds) Afferent control of posture and locomotion. Progr Brain Res 80: 37–45
Bessou P, Dupui Ph, Joffroy M, Montoya R, Pagès B (1988) Modulation au cours de la marche de l'activité efférente et afférente d'un muscle fléchisseur chez le chat thalamique. Arch Int Physiol Biochim 96: A102
Bessou P, Emonet-Dénand F, Laporte Y (1965) Motor fibres innervating extrafusal and intrafusal fibres in the cat. J Physiol (Lond) 180: 649–672
Bessou P, Joffroy M, Pagès B (1981) Efferents and afférents in an intact muscle nerve: background activity and effects of sural nerve stimulation in the cat. J Physiol (Lond) 320: 81–102
Bessou P, Pagès B (1975) Cinematographic analysis of contractile events produced in intrafusal muscle fibres by stimulation of static and dynamic fusimotor axons. J Physiol (Lond) 252: 397–427
Eccles RM, Lundberg A (1958) Integrative pattern of la synaptic actions on motoneurones of hip and knee muscles. J Physiol (Lond) 144: 271–298
Emonet-Dénand F, Filippi GM, Hunt CC, Laporte Y, Petit J (1988) Changes in resistance to stretch elicited by the contraction of slow and fast motor units in cat peroneus longus in vivo. J Physiol (Lond) 406:42P
Emonet-Dérńand F, Houk J (1968) Etude comparative de la curarisation des synapses neuromusculaires des fibres fusimotrices gamma dynamiques et statiques chez le chat. J Physiol (Paris) 60: 367–372
Forssberg H, Grillner S, Halbertsma J (1980) The locomotion of the low spinal cat. 1. Coordination within a hindlimb. Acta Physiol Scand 108: 269–281
Griffiths RI, Hoffer JA (1987) Muscle fibers shorten when the whole muscle is being stretched in the “yield phase” of the freely walking cat. Soc Neurosci Abstr 13: 1214
Hoffer JA, Caputi AA, Pose IE, Griffiths RI (1990) Roles of muscle activity and load on the relationship between muscle spindle length and whole muscle length in the freely walking cat. In: Allum JHJ, Hulliger M (eds) Afferent control of posture and locomotion. Progr Brain Res 80:75–85
Hoffer JA, Loeb GE, Sugano N, Marks WB, O'Donovan MJ, Pratt CA (1987) Cat hindlimb motoneurones during locomotion. III. Functional segregation in sartorius. J Neurophysiol 57: 554–562
Houk J, Henneman E (1967) Responses of Golgi tendon organs to active contractions of the soleus muscle of the cat. J Neurophysiol30: 466–481
Hulliger M (1984) The mammalian muscle spindle and its central control. Rev Physiol Biochem Pharmacol 101: 1–110
Hulliger M, Dürmüller N, Prochazka A, Trend P (1990) Flexible fusimotor control of muscle spindle feedback during a variety of natural movements: In: Allum JHJ, Hulliger M (eds) Afferent control of posture and locomotion. Progr Brain Res 80: 87–101
Hulliger M, Horber F, Medved A, Prochazka A (1987) An experimental simulation method for iterative and interactive reconstruction of unknown (fusimotor) inputs contributing to known (spindle afferent) responses. J Neurosci Meth 21: 225–238
Hulliger M, Prochazka A (1983) A new simulation method to deduce fusimotor activity from afferent discharge recorded in freely moving cats. J Neurosci Meth 8: 197–204
Joffroy M (1975) Méthode de discrimination des potentiels unitaires constituant l'activité complexe d'un filet nerveux non sectionné. J Physiol (Paris) 70: 239–252
Laporte Y, Emonet-Dénand F, Jami L (1981) The skeletofusimotor or β-innervation of mammalian muscle spindle. Trends Neurosci4: 97–99
Lennerstrand G, Thoden U (1968) Position and velocity sensitivity of muscle spindles in the cat. II. Dynamic fusimotor single-fibre activation of primary endings. Acta Physiol Scand 74: 16–29
Loeb GE (1981) Somatosensory unit input to the spinal cord during normal walking. Can J Physiol Pharmacol 59: 627–635
Loeb GE, Duysens J (1979) Activity patterns in individual hindlimb primary and secondary muscle spindle afferents during normal movements in unrestrained cats. J Neurophysiol 42: 420–4440
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 Jl Exp Physiol 47: 234–333
Matthews PBC (1972) Mammalian muscle receptors and their central actions. Arnold, London
Murphy PR, Stein RB, Taylor J (1984) Phasic and tonic modulation of impulse rates in gamma motoneurones during locomotion in premammillary cats. J Neurophysiol 52: 228–243
Orlovskii GN (1969) Spontaneous and induced locomotion of the thalamic cat. Biophysics 14: 1154–1162
Perret C (1976) Neural control of locomotion in the decorticate cat. In: Herman RM, Grillner S, Stein PSG, Stuart DG (eds) Neural control of locomotion. Plenum Press, New York, pp 587–615
Perret C (1983) Centrally generated pattern of motoneurone activity during locomotion in the cat. In: Roberts A, Roberts B (eds) Neural origin of rhythmic movements. Cambridge University Press, Cambridge, pp 405–422
Perret C, Buser P (1972) Static and dynamic fusimotor activity during locomotor movements in the cat. Brain Res 40: 165–169
Perret C, Cabelguen JM (1980) Main characteristics of the hindlimb locomotor cycle in the decorticate cat with special reference to bifunctional muscles. Brain Res 187: 333–352
Petit J, Filippi GM, Emonet-Dénand F, Hunt CC, Laporte Y (1990) Changes in muscle stiffness produced by motor units of different types in peroneus longus muscle of cat. J Neurophysiol 63: 190–197
Philippson M (1905) L'autonomie et la centralisation dans le système nerveux des animaux. Trav Lab Physiol Inst Solway Bruxelles 7: 1–208
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
Prochazka A, Westerman RA, Ziccone SP (1976) Discharge of single hindlimb afférents in the freely moving cat. J. Neurophysiol 39: 1090–1104
Rasmussen S, Chan AK, Goslow Jr GE (1978) The cat step cycle: electromyographic patterns for hindlimb muscles during posture and unrestrained locomotion. J Morphol 155: 253–270
Rioult-Pedotti MS, Kohen R, Hulliger M (1988) On the ability of static and dynamic γ-motoneurones to maintain spindle Ia firing during muscle shortening. Eur J Neurosci Suppl 1: 269
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Bessou, P., Joffroy, M., Montoya, R. et al. Evidence of the co-activation of α-motoneurones and static γ-motoneurones of the sartorius medialis muscle during locomotion in the thalamic cat. Exp Brain Res 82, 191–198 (1990). https://doi.org/10.1007/BF00230851
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DOI: https://doi.org/10.1007/BF00230851