Neuromuscular specializations within human pharyngeal constrictor muscles.
OBJECTIVE
At present it is believed that the pharyngeal constrictor (PC) muscles are innervated by the vagus (X) nerve and are homogeneous in muscle fiber content. This study tested the hypothesis that adult human PCs are divided into 2 distinct and specialized layers: a slow inner layer (SIL), innervated by the glossopharyngeal (IX) nerve, and a fast outer layer (FOL), innervated by nerve X.


METHODS
Eight normal adult human pharynges (16 sides) obtained from autopsies were studied to determine 1) their gross motor innervation by use of Sihler's stain; 2) their terminal axonal branching by use of acetylcholinesterase (AChE) and silver stain; and 3) their myosin heavy chain (MHC) expression in PC muscle fibers by use of immunocytochemical and immunoblotting techniques. In addition, the specialized nature of the 2 PC layers was also studied in developmental (newborn, neonate, and senescent humans), pathological (adult humans with idiopathic Parkinson's disease [IPD]), and comparative (nonhuman primate [adult macaque monkey]) specimens.


RESULTS
When nerves IX and X were traced from their cranial roots to their intramuscular termination in Sihler's-stained specimens, it was seen that nerve IX supplied the SIL, whereas branches of nerve X innervated the FOL in the adult human PCs. Use of AChE and silver stain confirmed that nerve IX branches supplying the SIL contained motor axons and innervated motor end plates. In addition to distinct motor innervation, the SIL contained muscle fibers expressing slow-tonic and alpha-cardiac MHC isoforms, whereas the FOL contained muscle fibers expressing developmental MHC isoforms. In contrast, the FOL became obscured in the elderly and in the adult humans with IPD because of an increased proportion of slow muscle fibers. Notably, distinct muscle fiber layers were not found in the human newborn and nonhuman primate (monkey), but were identified in the 2-year-old human.


CONCLUSIONS
Human PCs appear to be organized into functional fiber layers, as indicated by distinct motor innervation and specialized muscle fibers. The SIL appears to be a specialized layer unique to normal humans. The presence of the highly specialized slow-tonic and alpha-cardiac MHC isoforms, together with their absence in human newborns and nonhuman primates, suggests that the specialization of the SIL maybe related to speech and respiration. This specialization may reflect the sustained contraction needed in humans to maintain stiffness of the pharyngeal walls during respiration and to shape the walls for speech articulation. In contrast, the FOL is adapted for rapid movement as seen during swallowing. Senescent humans and patients with IPD are known to be susceptible to dysphagia; and this susceptibility may be related to the observed shift in muscle fiber content.
Mu
Liancai
L
Department of Otolaryngology, The Mount Sinai School of Medicine, New York, NY 10029-6574, USA.
Sanders
Ira
I
D000328:Adult; D000367:Age Factors; D000368:Aged; D000818:Animals; D001369:Axons / Q000473:pathology; D002675:Child, Preschool; D049631:Esophageal Sphincter, Upper / Q000294:innervation* / Q000473:pathology; D005930:Glossopharyngeal Nerve / Q000473:pathology*; D006801:Humans; D007124:Immunoenzyme Techniques; D007223:Infant; D007823:Laryngeal Nerves / Q000473:pathology; D008253:Macaca mulatta; D009045:Motor Endplate / Q000000981:diagnostic imaging; D009046:Motor Neurons / Q000473:pathology*; D018656:Muscle Fibers, Fast-Twitch / Q000473:pathology; D018657:Muscle Fibers, Slow-Twitch / Q000473:pathology; D018995:Myosin Heavy Chains / Q000032:analysis; D009410:Nerve Degeneration / Q000473:pathology; D009620:Nodose Ganglion / Q000473:pathology; D010300:Parkinson Disease / Q000473:pathology; D010609:Pharyngeal Muscles / Q000294:innervation* / Q000473:pathology; D020033:Protein Isoforms / Q000032:analysis; D012016:Reference Values; D013045:Species Specificity; D017783:Superior Cervical Ganglion / Q000473:pathology; D014463:Ultrasonography; D014630:Vagus Nerve / Q000473:pathology*
D020033:Protein Isoforms; D018995:Myosin Heavy Chains