Abstract
The present investigation documents the patterns of primary afferent depolarization (PAD) of single, functionally identified muscle afferents from the medial gastrocnemius nerve in the intact, anesthetized cat. Classification of the impaled muscle afferents as from muscle spindles or from tendon organs was made according to several criteria, which comprised measurement of conduction velocity and electrical threshold of the peripheral axons, and the maximal frequency followed by the afferent fibers during vibration, as well as the changes in discharge frequency during longitudinal stretch, the projection of the afferent fiber to the motor pool, and, in unparalyzed preparations, the changes in afferent activity during a muscle twitch. In confirmation of a previous study, we found that most muscle spindle afferents (46.1–66.6%, depending on the combination of criteria utilized for receptor classification) had a type A PAD pattern. That is, they were depolarized by stimulation of group I fibers of the posterior biceps and semitendinosus (PBSt) nerve, but not by stimulation of cutaneous nerves (sural and superficial peroneus) or the bulbar reticular formation (RF), which in many cases inhibited the PBSt-induced PAD. In addition, we found a significant fraction of muscle spindle primaries that were depolarized by stimulation of group I PBSt fibers and also by stimulation of the bulbar RF. Stimulation of cutaneous nerves produced PAD in 9.1–31.2% of these fibers (type B PAD pattern) and no PAD in 8.2–15.4% (type C PAD pattern). In contrast to muscle spindle afferents, only the 7.7–15.4% of fibers from tendon organs had a type A PAD pattern, 23–46.1% had a type B and 50–61.5% a type C PAD pattern. These observations suggest that the neuronal circuitry involved in the control of the synaptic effectiveness of muscle spindles and tendon organs is subjected to excitatory as well as to inhibitory influences from cutaneous and reticulospinal fibers. As shown in the accompanying paper, the balance between excitation and inhibition is not fixed, but can be changed by crushing the afferent axons in the peripheral nerve and allowing subsequent reconnection of these afferent fibers with muscle receptors.
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References
Anden NE, Jukes MGM, Lundberg A (1966a) The effect of DOPA on the spinal cord. I. Influence on transmission from primary afferents. Acta Physiol Scand 63: 373–386
Anden NE, Jukes MGM, Lundberg A (1966b) The effect of DOPA on the spinal cord. 3. Depolarization evoked in the central terminals of ipsilateral Ia afferents by volleys in the flexor reflex afferents. Acta Physiol Scand 68: 322–336
Bianconi R, Van der Meulen JP (1963) The response to vibration of the end organs of mammalian muscle spindles. J Neurophysiol 26: 177–190
Binder MD, Stuart DG (1980) Responses of Ia and spindle group II afferents to single motor-unit contractions. J Neurophysiol 43: 621–629
Brink E, Jankowska E, Skoog B (1984) Convergence onto interneurons subserving primary afferent depolarization of group I afferents. J Neurophysiol 51: 432–449
Brown MC, Engberg I, Matthews PBC (1967) The relative sensitivity to vibration of muscle receptors of the cat. J Physiol (Lond) 192: 773–800
Cameron WE, Binder MD, Botterman BR, Reinking RM, Stuart DG (1981) “Sensory partitioning” of cat medial gastrocnemius muscle by its muscle spindles and tendon organs. J Neurophysiol 48: 32–47
Collins WF III, Mendell LM, Munson JB (1986) On the specificity sensory reinnervation of cat skeletal muscle. J Physiol (Lond) 375: 587–609
Czarkowska J, Jankowska E, Sybirska E (1981) Common interneurones in reflex pathways from group Ia and Ib afferents from knee flexors and extensors in the cat. J Physiol (Lond) 310: 367–380
Dutia MB, Ferrell WR (1980) The effect of suxamethonium on the response to stretch of Golgi tendon organs in the cat. J Physiol (Lond) 306: 511–518
Eccles JC, Magni F, Willis WD (1962) Depolarization of central terminals of group I afferent fibres from muscle. J Physiol (Lond) 160: 62–93
Eccles JC, Schmidt RF, Willis WD (1963) Depolarization of central terminals of group Ib afferent fibers of muscle. J Neurophysiol 26: 1–27
Edin BB, Vallbo AB (1990) Classification of human muscle stretch receptor afferents: a Bayesian approach. J Neurophysiol 63: 1314–1322
Eguibar JR, Quevedo J, Jiménez I, Rudomin P (1994) Selective cortical control of information flow through different intraspinal collaterals of the same muscle afferent fiber. Brain Res 643: 328–333
Enríquez M, Hernández O, Jiménez I, Rudomin P (1991) Is the PAD evoked in Ia fibers related to their responses to stretch? Soc Neurosci Abstr 17: 408.9
Enríquez M, Jiménez I, Rudomin P (In press) Changes in PAD patterns of group I muscle afferents after a peripheral nerve crush. Exp Brain Res
Harrison PJ, Jankowska E (1989) Primary afferent depolarization of central terminals of group II muscle afferents in the cat spinal cord. J Physiol (Lond) 411: 71–83
Horch KW, Lisney SJW (1981) Changes in primary afferent depolarization of sensory neurones during peripheral nerve regeneration in the cat. J Physiol (Lond) 313: 287–299
Houk J, Henneman E (1967) Responses of Golgi tendon organs to active contractions of the soleus muscle of the cat. J Neurophysiol 30: 446–481
Hunt CC (1954) Relation of function to diameter in afferent fibers of muscle nerves. J Gen Physiol 38: 117–131
Hunt CC, Kuffler SW (1951) Stretch receptors discharges during muscle contraction. J Physiol (Lond) 133: 298–315
Jami L (1992) Golgi tendon organs in mammalian skeletal muscle: functional properties and central actions. Physiol Rev 72: 623–666
Jankowska E, Riddell JS (1993) A relay input from group II muscle afferents in sacral segments of the cat spinal cord. J Physiol (Lond) 465: 561–580
Jiménez I, Rudomin P, Solodkin M (1988) PAD patterns of physiologically identified afferent fibers from the medial gastrocnemius muscle. Exp Brain Res 71: 643–657
Lennerstrand G (1968) Position and velocity sensitivity of muscle spindles in the cat. I. Primary and secondary endings deprived of fusimotor activation Acta Physiol Scand 73: 281–299
Lundberg A, Vyklicky L (1966) Inhibition of transmission to primary afferents by electrical stimulation of the brain-stem. Arch Ital Biol 104: 86–97
Matthews BHC (1933) Nerve endings in mammalian muscle. J Physiol (Lond) 78: 1–53
Matthews PBC (1972) Mammalian muscle receptors and their central actions. Arnold, London
Price RF, Dutia MB (1987) Properties of cat neck muscle spindle afferents and their excitation by succinylcholine Exp Brain Res 68: 619–630
Proske U, Morgan DL, Gregory JE (1992) Muscle history dependence of responses to stretch of primary and secondary endings of cat muscle spindles. J Physiol (Lond) 445: 81–95
Quevedo J, Eguibar JR, Jiménez I, Rudomin P (1995) Raphe magnus and reticulospinal actions on primary afferent depolarization of group I muscle afferents in the cat. J Physiol (Lond) 482: 623–640
Riddell JS, Jankowska E, Eide E (1993a) Depolarization of group II muscle afferents by stimuli applied to the locus coeruleus and raphe nuclei of the cat. J Physiol (Lond) 461: 723–741
Riddell JS, Jankowska E, Huber J (1993b) Primary afferent depoarization of group II afferents (abstract). J Physiol (Lond) 459: 499P
Romanes GJ (1951) The motor cell columns of the lumbosacral cord of the cat. J Comp Neurol 94: 313–364
Rudomin P, Button H (1969) Effects of conditioning afferent volleys on variability of monosynaptic responses of extensor motoneurons. J Neurophysiol 32: 140–157
Rudomin, P, Jiménez I, Solodkin M, Duenas S (1983) Sites of action of segmental and descending control of transmission on pathways mediating PAD of Ia- and Ib-afferent fibers in the cat spinal cord. J Neurophysiol 50: 743–769
Rudomin P, Solodkin M, Jiménez I (1986) PAD and PAH response patterns of group Ia- and Ib-fibers to cutaneous and descending inputs in the cat spinal cord. J Neurophysiol 56: 987–1006
Scott JJA (1990) Classification of muscle spindle afferents in the peroneous brevis muscle of the cat. Brain Res 509: 62–70
Snider RS, Niemer WT (1961) A stereotaxic atlas of the cat brain. University of Chicago Press, Chicago
Stephens JA, Reinking RM, Stuart DG (1975) Tendon organs of cat medial gastrocnemius: responses to active and passive forces as a function of muscle length. J Neurophysiol 38: 1217–1231
Sypert GW, Munson JB, Fleshman JW (1980) Effect of presynaptic inhibition on axonal potentials, terminal potentials, focal synaptic potentials, EPSPs in cat spinal cord. J Neurophysiol 44: 792–803
Taylor A, Rodgers JE, Fowle AJ, Durbaba R (1992) The effect of succinylcholine on cat gastrocnemius muscle spindle afferents of different types. J Physiol (Lond) 456: 629–644
Taylor A, Durbaba R, Rodgers JF (1993) Projection of cat jaw muscle spindle afferents related to intrafusal fibre influence. J Physiol (Lond) 465: 647–660
Wall PD (1982) The effect of peripheral nerve lesions and of neonatal capsaicin in the rat on primary afferent depolarization. J Physiol (Lond) 329: 21–35
Wall PD, Devor M (1981) The effect of peripheral nerve injury on dorsal root potentials and on transmission of afferent signals into the spinal cord. Brain Res 209: 95–111
Watt DGD, Stauffer EK, Taylor A, Reinking RM, Stuart DG (1976) Analysis of muscle receptor connections by spike-triggered averaging. 1. Spindle primary and tendon organ afferents. J Neurophysiol 39: 1375–1392
Willis WD, Núñez R, Rudomin P (1976) Excitability changes of terminal arborizations of single Ia and Ib afferent fibers produced by muscle and cutaneous conditioning volleys. J Neurophysiol 39: 1150–1159
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Enríquez, M., Jiménez, I. & Rudomin, P. Segmental and supraspinal control of synaptic effectiveness of functionally identified muscle afferents in the cat. Exp Brain Res 107, 391–404 (1996). https://doi.org/10.1007/BF00230421
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DOI: https://doi.org/10.1007/BF00230421