Neural organization of spindles in three hindlimb muscles of the rat

Abstract

The neuroanatomical organization of the dynamic (bag1) and static (bag2 and chain) intrafusal systems was compared by light and electron microscopy of serial sections among 71 poles of muscle spindle in soleus (SOL), extensor digitorum longus (EDL), and lumbrical (LUM) muscles in the rat. Eighty-four percent of 195 fusimotor (gamma) axons to the spindles innervated either the dynamic bag1 fiber or the static bag2 and/or chain fibers. Sixteen percent of the gamma axons coinnervated the dynamic and static intrafusal fibers. Some of these nonselective axons were branches of effernts that also gave rise to axons selective to either the dynamic or static types of intrafusal fibers in one or more spindles. Thus activation of individual stem gamma efferents might not have a purely dynamic or purely static effect on the integrated afferent outflow from spindles of a hindlimb muscles in the rat. In addition, primary afferents in all muscles had terminations that cross-innervated the dynamic bag1 and static bag1 and/or chain intrafusal fibers in individual spindles, an arrangement that may enhance the mixed dynamic/static behavior of afferents when different intrafusal fibers are activated concurrent. Spindles of the slow SOL and fast EDL muscles had similar features, whereas differences were observed in the organization of the proximal (SOL and EDL) and distal (LUM) muscles. Spindles in LUM muscles had fewer static intrafusal fibers, a higher ratio of dynamic to static gamma axons, and a higher incidence of skeletofusimotor (beta) innervation to intrafusal fibers than spindles in the SOL or EDL muscles. Thus, the relative contribution of dynamic and static systems to muscle afferent outflow may differ among spindles located in different segments of the rat hindlimb. However, the dynamic and static intrafusal systems of spindle were less sharply demarcated in each of the three hindlimb rat muscles than in the cat tenuissimus muscle.

Gamma motor neurons express distinct genetic markers at birth and require muscle spindle-derived GDNF for postnatal survival

“…In the rat, the incidence of γ and β efferents differ from muscle to muscle, but the large majority of motor inputs on intrafusal fibers in hindlimb muscles are γ motor axons [47]. Our findings in the Gfrα1-TLZ/Hb9::GFP mouse predict that these γ fusimotor endings should be TLZ+ and GFP-.…”

Phylogenetic preservation of α3 Na+,K+‐ATPase distribution in vertebrate peripheral nervous systems

“…In frogs, nearly all muscle spindles receive ␤ innervation but not ␥ innervation (see Shepherd, 1994). In rats, some muscles may have as many as 40% motor ␤ axons, whereas others have virtually none (lumbricales and soleus, respectively; Kucera et al, 1991). There is some morphological data showing presence of ␤ innervation in avian and human muscles (Swash and Fox, 1972;Maier, 1992); however, these data do not exclude the possibility that at least some spinal levels in these species have negligibly small numbers of ␤ motoneurons.…”

Formation of supernumerary muscle spindles at the expense of golgi tendon organs in ER81‐deficient mice

“…A lesser dependence of monosynaptic Ia afferent‐motoneuron connections in distal than proximal muscles on ER81 (Arber et al, 2000) may be the reason why spindles are present in distal but not proximal muscles of Er81 mutants. Only those DRG neurons that contact monosynaptically with motoneurons are hypothesized to acquire the Ia neuron phenotype and become capable of spindle induction, maintenance, or both (Kucera et al, 1991). This hypothesis is supported by the absence of muscle spindles in the nestin mutant mouse (NesPIXpNT3) in which sensory neurons, although present, fail to form ventral monosynaptic afferent‐motoneuron connections and terminate in the more dorsal regions of the spinal cord (Ringstedt et al, 1997, Ringstedt et al, 1998).…”