Rat whisker movement after facial nerve lesion: evidence for autonomic contraction of skeletal muscle.
Vibrissal whisking is often employed to track facial nerve regeneration in rats; however, we have observed similar degrees of whisking recovery after facial nerve transection with or without repair. We hypothesized that the source of non-facial nerve-mediated whisker movement after chronic denervation was from autonomic, cholinergic axons traveling within the infraorbital branch of the trigeminal nerve (ION). Rats underwent unilateral facial nerve transection with repair (N=7) or resection without repair (N=11). Post-operative whisking amplitude was measured weekly across 10weeks, and during intraoperative stimulation of the ION and facial nerves at ⩾18weeks. Whisking was also measured after subsequent ION transection (N=6) or pharmacologic blocking of the autonomic ganglia using hexamethonium (N=3), and after snout cooling intended to elicit a vasodilation reflex (N=3). Whisking recovered more quickly and with greater amplitude in rats that underwent facial nerve repair compared to resection (P<0.05), but individual rats overlapped in whisking amplitude across both groups. In the resected rats, non-facial-nerve-mediated whisking was elicited by electrical stimulation of the ION, temporarily diminished following hexamethonium injection, abolished by transection of the ION, and rapidly and significantly (P<0.05) increased by snout cooling. Moreover, fibrillation-related whisker movements decreased in all rats during the initial recovery period (indicative of reinnervation), but re-appeared in the resected rats after undergoing ION transection (indicative of motor denervation). Cholinergic, parasympathetic axons traveling within the ION innervate whisker pad vasculature, and immunohistochemistry for vasoactive intestinal peptide revealed these axons branching extensively over whisker pad muscles and contacting neuromuscular junctions after facial nerve resection. This study provides the first behavioral and anatomical evidence of spontaneous autonomic innervation of skeletal muscle after motor nerve lesion, which not only has implications for interpreting facial nerve reinnervation results, but also calls into question whether autonomic-mediated innervation of striated muscle occurs naturally in other forms of neuropathy.
Department of Surgery, Massachusetts General Hospital, Harvard Medical School, 55 Fruit Street, Boston, MA 02114, United States. Electronic address: james.heaton@mgh.harvard.edu.
James T
JT
Heaton
Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, 75 Francis Street, Boston, MA 02114, United States.
Shu Hsien
SH
Sheu
Department of Otology and Laryngology, Massachusetts Eye and Ear Infirmary, Harvard Medical School, 243 Charles Street, Boston, MA 02114, United States.
Marc H
MH
Hohman
Department of Otology and Laryngology, Massachusetts Eye and Ear Infirmary, Harvard Medical School, 243 Charles Street, Boston, MA 02114, United States.
Christopher J
CJ
Knox
Department of Otology and Laryngology, Massachusetts Eye and Ear Infirmary, Harvard Medical School, 243 Charles Street, Boston, MA 02114, United States.
Julie S
JS
Weinberg
Department of Otology and Laryngology, Massachusetts Eye and Ear Infirmary, Harvard Medical School, 243 Charles Street, Boston, MA 02114, United States; Department of Otorhinolaryngology and Head & Neck Surgery, Radboud University Nijmegen Medical Center, Nijmegen, The Netherlands.
Ingrid J
IJ
Kleiss
Department of Otology and Laryngology, Massachusetts Eye and Ear Infirmary, Harvard Medical School, 243 Charles Street, Boston, MA 02114, United States.
Tessa A
TA
Hadlock
D000818:Animals; D001341:Autonomic Nervous System / Q000166:cytology / Q000502:physiology*; D005154:Facial Nerve / Q000502:physiology*; D005260:Female; D009043:Motor Activity; D009119:Muscle Contraction; D018482:Muscle, Skeletal / Q000294:innervation*; D051381:Rats; D014738:Vibrissae / Q000294:innervation* / Q000502:physiology*
autonomic; infraorbital nerve; motor; paralysis; parasympathetic; reinnervation