Motor nerve topology reflects myocyte morphology in hamster retractor and epitrochlearis muscles

Abstract

Neuromuscular activation is a primary determinant of metabolic demand and oxygen transport. The m. retractor and m. epitrochlearis are model systems for studying metabolic control and oxygen transport; however, the organization of muscle fibers and motor nerves in these muscles is unknown. We tested whether the topology of motor innervation was related to the morphology of muscle fibers in m. retractor and m. epitrochlearis of male hamsters (∼100 g). Respective muscles averaged 47 and 12 mm in length 100 and 35 mg in mass. Staining for acetylcholinesterase revealed neuromuscular junctions arranged in clusters throughout m. retractor and as a central band across m. epitrochlearis, suggesting differences in fiber morphology. For both muscles, complete cross‐sections contained ∼1,700 fibers. Fiber cross‐sectional areas were distributed nearly normal in m. epitrochlearis (mean = 1,559 ± 17 μm2) and skewed left (P < 0.05) in m. retractor (mean = 973 ± 15 μm2). Single fiber length (Lf) spanned muscle length (Lm) in m. epitrochlearis, while fibers tapered to terminate within m. retractor (Lf/Lm = 0.43 ± 0.02). With myelin staining, a single branch of ulnar nerve projected axons across the midregion of m. epitrochlearis. For m. retractor, the spinal accessory nerve branched to give rise to proximal and distal regions of innervation, with intermingling of axons between nerve branches. Nerve bundle cross‐sections stained for acetylcholinesterase indicate that each motor axon projects to an average of 65 muscle fibers in m. epitrochlearis and 100 in m. retractor. Differences in fiber morphology, innervation topology, and neuromuscular organization may contribute to the heterogeneity of metabolic demand and oxygen supply in skeletal muscle. J. Morphol. 246:103–117, 2000 © 2000 Wiley‐Liss, Inc.

Rapid dilation of arterioles with single contraction of hamster skeletal muscle

“…Our findings in the hamster may be explained by differences in the topology of motor innervation between the retractor muscle, which has neuromuscular junctions dispersed throughout the muscle compared with forearm or locomotor muscles, where motor end plates are confined to the central region of the muscle (31). In the hamster cremaster muscle, which also has a disperse motor innervation, somatic neuromuscular junctions are found closest to capillaries and small arterioles (25), and a similar distribution has been confirmed in retractor muscle (G. Gonzalez-Lomas, JWGE VanTeeffelen, and SS Segal, unpublished observations).…”

“…Moreover, this anatomical relationship is consistent with ROV being observed primarily in the more abundant distal (2A and 3A) versus proximal (1A and FA) branches of the resistance network. In addition to its unique neuromuscular junction distribution, the retractor muscle is a thin, strap-like muscle (31) and is reflected away from the hamster for intravital studies. This contrasts with intact forearm or locomotor muscles that contract within anatomically defined "compartments," whereby intramuscular pressure can increase during a contraction to levels that occlude arterial inflow while expelling venous effluent (1).…”

Microvessels Promote Motor Nerve Survival and Regeneration Through Local VEGF Release Following Ectopic Reattachment

“…The vigor of contraction increased noticeably from 14 to 21 d but not thereafter. Retractor muscles, typically ∼80 mg (41), atrophied ∼25% by 21 d and ∼30% by 28 d, with fatty streaks visible on gross observation.…”

“…The dorsal edge of each retractor muscle was reflected to expose the neurovascular pedicle. The accessory nerve (CN XI), which innervates the muscle, divides prior to entering the retractor muscle, creating 2–3 smaller nerve bundles and one primary trunk that enters with the primary vascular pedicle (41). The primary nerve trunk was dissected away from its associated feed artery and collecting vein; all nerve bundles were cut where they entered the muscle and reattached as a single stump 2–4 mm rostral to the original primary pedicle using 11‐O monofilament suture tied through the muscle.…”

Kinematic analysis of an appetitive food-handling behavior: the functional morphology of Syrian hamster cheek pouches

“…The topology of retractor innervation is highly variable, and ranges from fairly simple bifurcation of the spinal accessory nerve at two points to complex anastomoses between the branches (Segal et al, 2000). The failure of retractor denervation to affect the number of food items pouched might therefore be attributed to incomplete denervation procedures.…”