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Renshaw Cells Renshaw cells Elzbieta Jankowska The name Renshaw cells has been given to a group of inhibitory interneurons in the ventral horn of the vertebrate spinal cord in honor of B. Renshaw who first described them. Renshaw cells were the first type of spinal interneurons to be functionally, morphologically, and pharmacologically identified (Eccles et al., 1954; see Baldissera et al., 1981; Jankowska, 1992) and belong to the most extensively analyzed populations of spinal interneurons. Synaptic actions of Renshaw cells have been studied in most detail in the cat, but they have also been found, whenever investigated, in other species (including rat, mouse, chicken, monkey, and human). Renshaw cells have been of particular interest as the neurons most tightly coupled to spinal motor output neurons (motoneurons). Another reason for the continuous interest in Renshaw cells might be that they are one of the types of spinal interneurons most easily recognizable, in whole animals as well as in isolated spinal cord preparations and in spinal cord slices. Furthermore, neuronal networks including Renshaw cells have been of interest as models of negative feedback networks operating in different parts of the central nervous system. The coupling between Renshaw cells and -motoneurons is illustrated in Figure 1. The diagram shows that Renshaw cells are excited by nerve impulses in recurrent axon collaterals of -motoneurons and provide negative feedback (a disynaptically evoked recurrent inhibition) to these neurons. They respond with a high frequency burst of discharges lasting for several tenths of milliseconds to single volleys in motoneuron axons; such discharges are a characteristic feature of these interneurons and allow them to be differentiated from other interneurons. The discharges are generated by long-lasting excitatory postsynaptic potentials (EPSPs) (Figure 1, A and B; see Eccles et al., 1961; Walmsley and Tracey, 1981). The efficacy of transmission in synapses between recurrent axon collaterals of -motoneurons and Renshaw cells is very high because Renshaw cells may be activated, although with shorter-lasting bursts, by a single motoneuron (Hamm et al., 1987).The discharges are generated by long lasting EPSPs (Fig. lA, B; Eccles et al., 1961; Walmsley and Tracey, 1981) Renshaw cells evoke a widely distributed inhibition of populations of motoneurons that excite them, as well as of motoneurons that innervate synergist muscles (Figure 1, C and the diagram), but never those innervating antagonist muscles. However, recurrent inhibition has been found only in motoneurons of some muscles, the majority of limb muscles and of tail, back, intercostal, diaphragm, and neck muscles, but not of the most distal forelimb or hindlimb muscles, the perianal sphincters, and jaw and eye muscles. Renshaw cells may control activation of all types of motor units of a muscle as effectively, and no support has been found for preferential recurrent inhibition of slow motor units following activation of the fast ones, as suggested by earlier observations (Hultborn et al., 1979; Hultborn et al., 1988a; Hultborn et al., 1988b). Recurrent inhibition of -motoneurons is only one of the actions mediated by Renshaw cells. Other target neurons of these cells include interneurons mediating inhibition of motoneurons of antagonist muscles (Ia reciprocal inhibition between flexors and extensors, as indicated in the right part of the diagram in Figure 1), other Renshaw cells, gamma motoneurons, and cells of origin of the ventral spinocerebellar tract. Thus they modulate spinal neuronal activity at a premotoneuronal as well as a motoneuronal level ( see Baldissera et al., 1981; Jankowska, 1992). The adjustments in the degree of Ia reciprocal inhibition, and thereby of the balance in activation of antagonist muscles, can be singled out as one of the main functions Renshaw cells, because inhibition of interneurons mediating Ia reciprocal inhibition is particularly potent. Renshaw cells may practically block transmission via these interneurons and thereby assist in the cocontraction of flexors and extensors when such a cocontraction is more advantageous than activation of only one group of antagonists. Recent studies of functions of Renshaw cells in man show that these cells not only are used in local circuits but also contribute to adjusting centrally initiated voluntary movements (Hultborn and Pierrot Deseilligny, 1979). As for proposals for other functions of Renshaw cells put forward previously (see Hultborn et al., 1979; Windhorst, 1996), involvement of Renshaw cells in initiating rhythmic locomotor movements and an essential contribution to pathologically exaggerated spinal reflexes in spasticity have not been substantiated (McCrea et al., 1980; Katz and Pierrot-Deseilligny, 1982; Noga et al., 1987; Mazzocchio and Rossi, 1989). One of the means of controlling activity of Renshaw cells themselves is by a mutual inhibition between their subpopulations, that is, by other Renshaw cells (Ryall, 1970). Activity of Renshaw cells is coordinated with activity of other spinal interneurons by a number of neuronal systems that provide them with excitatory and inhibitory input of primary afferent and supraspinal origin in addition to their main input via motor axon collaterals. The projection areas of Renshaw cells were investigated both in physiologic experiments and after staining individual cells identified by functional criteria with intracellularly applied dyes (Eccles et al., 1954; Jankowska and Smith, 1973; Lagerback and Kellerth, 1985a). Both kinds of studies have shown that Renshaw cells are funicular neurons with axons passing over a distance of several millimeters in the white matter. The densest projection area and the strongest actions of Renshaw cells nevertheless are within 1-2 mm from the cell body. The projections are ipsilateral except in the lower sacral segments, where they are bilateral. Both the gross morphology and the ultrastructure of Renshaw cells have been analyzed (Jankowska and Lindstrom, 1971; Lagerback and Ronnevi, 1982b; Lagerback and Ronnevi, 1982a; Lagerback and Kellerth, 1985b; Lagerback and Kellerth, 1985a; Fyffe, 1990) Neurochemistry and membrane mechanisms of synaptic actions upon Renshaw cells and of Renshaw cells upon other neurons have been investigated using a number of experimental techniques that have successively become available (Curtis et al., 1976; Cullheim and Kellerth, 1981; Ryall, 1983; Schneider and Fyffe, 1992; Geiman et al., 2002). In synapses between Renshaw cells and their target neurons, the main transmitter is glycine (with strychnine as the antagonist). However, some actions of Renshaw cells, or actions of their subpopulations, have been found to depend on gamma-aminobutyric acid (GABA; depressed by bicuculline or picrotoxin). The synapses made upon Renshaw cells by motor axon collaterals are cholinergic: the early components of the synaptic responses are evoked via nicotinic receptors (blocked by dihydro-beta-erythroidine), and the late responses are evoked via muscarinic receptors (blocked by atropine). Inhibitory synapses on Renshaw cells have been recently investigated in particular detail. Neurons identified both functionally and morphologically as Renshaw cells were found to be characterized by exceptionally large clusters of gephyrine and glycine receptors on the soma and proximal dendrites (Alvarez et al., 1997), as illustrated in Figure 2. Using this feature as a distinguishing feature of Renshaw cells, both the presynaptic inhibitory content (GABAA and/or glycin) and subunit composition of GABAA and glycine postsynaptic receptors were recently defined (Schneider and Fyffe, 1992; Geiman et al., 2002). Characteristic features of Renshaw cells are also being used in an attempt to find genetic markers (transcription factors, homeodomain proteins) of these cells, which would allow future studies of their differentiation and development at a molecular level (Saueressig et al., 1999; Wenner and O'Donovan, 1999). 1. See also Motoneurons Neuron Spinal cord, organization Interneurons 2. References Alvarez FJ, Dewey DE, Harrington DA, Fyffe RE (1997): Cell-type specific organization of glycine receptor clusters in the mammalian spinal cord. J Comp Neurol 379:150-170 [MEDLINE] Baldissera F, Hultborn H, Illert M (1981): Integration in spinal neuronal systems. In: Handbook of Physiology. The nervous system. Motor control, Brooks VB, ed. Bethesda: American Physiological Society, pp. 509-595 Cullheim S, Kellerth JO (1981): Two kinds of recurrent inhibition of cat spinal alpha-motoneurones as differentiated pharmacologically. J Physiol 312:209-224 [MEDLINE] Curtis DR, Game CJ, Lodge D, McCulloch RM (1976): A pharmacological study of Renshaw cell inhibition. J Physiol 258:227-242 [MEDLINE] Eccles JC, Fatt P, Koketsu K (1954): Cholinergic and inhibitory synapses in a pathway from motor axon collaterals to motoneurones. J Physiol (Lond) 126:524-562 [MEDLINE] Eccles JC, Eccles RM, Iggo A, Lundberg A (1961): Electrophysiological investigations on Renshaw cells. J Physiol (Lond) 159:461-478 [MEDLINE] Fyffe RE (1990): Evidence for separate morphological classes of Renshaw cells in the cat's spinal cord. Brain Res 536:301-304 [MEDLINE] Geiman EJ, Zheng W, Fritschy JM, Alvarez FJ (2002): Glycine and GABA(A) receptor subunits on Renshaw cells: relationship with presynaptic neurotransmitters and postsynaptic gephyrin clusters. J Comp Neurol 444:275-289 [MEDLINE] Hamm TM, Sasaki S, Stuart DG, Windhorst U, et al. (1987): Distribution of
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