Quantitative analysis of cervical musculature in rats: Histochemical composition and motor pool organization. I. Muscles of the spinal accessory complex

Abstract

In this paper we characterize the architecture and segmental innervation, histochemical composition, muscle spindle populations, and motor pool organization of rat spinal accessory (SA) muscles: sternomastoid (SM), cleidomastoid (CM), cleidotrapezius (CT), and acromiotrapezius (AT). We also consider whether individual rat neck muscles are supplied by more than one population of motor neurons as they are in turtles and cats and whether in SA muscles motor neuron size scales with target muscle fiber type. SM, CM, and CT are ventral, parallel strap muscles. Each can be divided into grossly visible white and red compartments. AT is a dorsolateral sheetlike muscle that shows no gross compartmentalization. All four muscles are dominated by fast-twitch glycolytic (FG) and fast oxidative glycolytic (FOG) fibers, and FG fibers are significantly more numerous than the FOG type in three out of four muscles. Thus SA muscles in rats appear to be specialized for rapid, phasic head movements. Topographical analyses revealed that there is a striking compartmentalization of fiber types in the ventral muscles that corresponds to the red and white segments seen grossly. Spindles are found only in regions containing slow-twitch oxidative (SO) fibers. Cross-muscle comparisons indicate that there are significant differences between SA muscles in their fiber type composition. The motor pools of SA muscles form a single column from lower medulla to C5. Rostral cells lie dorsomedially in the ventral horn and, at the C1/C2 junction, the column shifts ventrolaterally. Within this column, each motor pool occupies a characteristic rostrocaudal position in the order SM:CM:CT:AT. Thus SM and (in part) CM motor neurons lie more medially than cells supplying the trapezius complex, suggesting that they may be under different patterns of synaptic drive. We saw no evidence that rat SA muscles are supplied by more than one population of motor neurons. Direct comparisons between the soma sizes of motor neurons that supply muscles or parts of muscles with significantly different histochemical compositions indicate that these size differences are in the direction predicted from their histochemical profiles, thus suggesting that in these muscles motor neuron soma size may scale with muscle fiber type.

Molecular Control of Spinal Accessory Motor Neuron/Axon Development in the Mouse Spinal Cord

“…The close similarity between anti-BEN and anti-ALCAM labeling supports our finding that BEN expression marks SACMNs. Consistent with SACMNs being confined to C1-C4 levels of the rodent spinal cord (Greene, 1935;Wentworth and Hinds, 1978;Gottschall et al, 1980;Brichta et al, 1987), anti-BEN-positive cell bodies and axons were not detected caudal to the cervical spinal cord in mouse embryos (data not shown). To further support our identification of anti-BEN as a marker of SACMN, we retrogradely labeled SACMN by introducing small crystals of DiI into the SAN in E12 wild-type mouse embryos.…”

“…Together with the results of previous anatomical (Greene, 1935;Wentworth and Hinds, 1978;Gottschall et al, 1980;Brichta et al, 1987;Snider and Palavali, 1990) and immunohistochemical (Schubert and Kaprielian, 2001) studies, the distribution of BEN suggests that SACMN/SAN development involves the following sequence of events: (1) ventrolaterally positioned SACMN cell bodies extend dorsally projecting axons away from the ventral midline, (2) SACMN cell bodies migrate dorsally and settle in the (A, B) brightly labels the hook-shaped SAN (arrow), as well as a variety of axons and cranial nerves/ganglia in an E10.5 mouse embryo. In a whole E10 mouse embryo, anti-BEN (C, D) rather selectively labels the SAN (arrow) and a small subset of cranial nerves/ganglia.…”

“…Spinal accessory motor neurons (SACMNs) are located within cervical regions of the spinal cord and selectively innervate the sternocleidomastoid and trapezius muscles in the neck and back (Greene, 1935;Wentworth and Hinds, 1978;Brichta et al, 1987;Snider and Palavali, 1990). Unlike most spinal motor neurons, SACMNs extend dorsally projecting axons along the lateral margins of the spinal cord that extend out of the CNS through the lateral exit point (LEP) (Snider and Palavali, 1990).…”

Sources of the motor and somatic sensory innervation of the trapezius muscle in the rat

“…Motor innervation of the trapezius muscle has been studied in many species including the rat (Gottschall et al, 1980;Kitamura and Sakai, 1982;Matesz and Szekely, 1983;Brichta et al, 1987;Ullah et al, 2007), rabbit (Ullah and Salman, 1986), cat (Rapoport, 1978;Satomi et al, 1985;Liinamaa et al, 1997), sheep (Clavenzani et al, 1994), primates (Augustine and White, 1986;Ueyama et al, 1990) and human (Routal and Pal, 2000). This innervation is accomplished mainly by the accessory nerve, but there are some papers reporting partial innervation of this muscle by motor fibres from spinal nerves (Zhao et al, 2006;Yan et al, 2007;Pu et al, 2008).…”

“…Many studies have reported that neurons in the medial column innervate the sternomastoid and the cleidomastoid muscles and the neurons in the lateral column innervate the trapezius muscle and a portion of the cleidomastoid muscle in the cat (Rapoport, 1978;Satomi et al, 1985;Liinamaa et al, 1997), rabbit (Ullah and Salman, 1986) and rat (Gottschall et al, 1980;Kitamura and Sakai, 1982;Matesz and Szekely, 1983;Brichta et al, 1987). Kitamura and Sakai (1982) reported localization of the SAN trapezius perikarya in C 2 (caudal half ), C 3 to C 5 and C 6 (rostral half ) spinal segments.…”