Reorganization of cranial sympathetic pathways following neonatal ganglionectomy in the rat.

Postganglionic sympathetic innervation normally is distributed ipsilaterally to lateral cranial targets. However, contralateral outgrowth occurs following unilateral ganglionectomy in neonatal rats. This study was conducted to determine the prevalence, morphological features, ganglionic derivations, and temporal sequence of sympathetic reinnervation of denervated cranial targets. Unilateral superior cervical ganglionectomy of mature rats revealed exclusively ipsilateral distributions of catecholaminergic histofluorescent fibers to orbital targets (Meibomian gland, tarsal muscle, orbital muscle, iris, ciliary body, vasculature) and the circle of Willis, with the exception of the anterior cerebral artery. In mature rats following neonatal unilateral ganglionectomy, all targets were reinnervated by fibers displaying morphologies and target relationships similar to normal innervation, but with lower densities. Acute excision of the remaining superior cervical ganglion eliminated all fibers in 7 of 8 preparations. In adult rats receiving neonatal bilateral superior cervical ganglionectomies, cerebral vasculature was reinnervated consistently, and orbital targets contained fluorescent fibers in 6 of 16 cases, indicating that reinnervation can derive from other sources when superior ganglion outgrowth is prevented. Observations in developing rats revealed fibers along the cranial portion of the contralateral optic nerve sheath at 2-3 days postganglionectomy, and within the orbit at later ages, reaching the most distal targets by 14 days. It is concluded that widespread sympathetic reinnervation of orbital and cerebrovascular targets derives primarily from the contralateral superior ganglion. Orbital ingrowth apparently originates intracranially and enters the orbit by an atypical pathway within the optic foramen.