3-DIMENSIONAL ANALYSIS OF VESTIBULAR EFFERENT NEURONS INNERVATING SEMICIRCULAR CANALS OF THE GERBIL

Anterograde labeling techniques were used to examine peripheral innerv ation patterns of vestibular efferent neurons in the crista ampullares of the gerbil. Vestibular efferent neurons were labeled by extracellu lar injections of biocytin or biotinylated dextran amine into the cont ralateral or ipsilateral dorsal subgroup of efferent cell bodies (grou p e) located dorsolateral to the facial nerve genu. Anterogradely labe led efferent terminal field varicosities consist mainly of boutons en passant with fewer of the terminal type. The bouton swellings are loca ted predominately in apposition to the basolateral borders of the affe rent calyces and type II hair cells, but several boutons were identifi ed close to the hair cell apical border on both types. Three-dimension al reconstruction and morphological analysis of the terminal fields fr om these cells located in the sensory neuroepithelium of the anterior, horizontal, and posterior cristae were performed. We show that effere nt neurons densely innervate each end organ in widespread terminal fie lds. Subepithelial bifurcations of parent axons were minimal, with ext ensive collateralization occurring after the axons penetrated the base ment membrane of the neuroepithelium. Axonal branching ranged between the 6th and 27th orders and terminal field collecting area far exceeds that of the peripheral terminals of primary afferent neurons. The ter minal fields of the efferent neurons display three morphologically het erogeneous types: central, peripheral, and planum. All cell types poss ess terminal fields displaying a high degree of anisotropy with orient ations typically parallel to or within +/-45 degrees of the longitudin al axis if the crista. Terminal fields of the central and planum zones predominately project medially toward the transverse axis from the mo re laterally located penetration of the basement membrane by the paren t axon. Peripheral zone terminal fields extend predominately toward th e planum semilunatum. The innervation areas of efferent terminal field s display a trend from smallest to largest for the central, peripheral , and planum types, respectively. Neurons that innervate the central z one of the crista do not extend into the peripheral or planum regions. Conversely, those neurons with terminal fields in the peripheral or p lanum regions do not innervate the central zone of the sensory neuroep ithelium. The central zone of the crista is innervated preferentially by efferent neurons with cell bodies located in the ipsilateral group e. The peripheral and planum zones of the crista are innervated prefer entially by efferent neurons with cell bodies located in the contralat eral group e. A model incorporating our anatomic observations is prese nted describing an ipsilateral closed-loop feedback between ipsilatera l efferent neurons and the periphery and an open-loop feed-forward inn ervation from contralateral efferent neurons. A possible role for the vestibular efferent neurons in the modulation of semicircular canal af ferent response dynamics is proposed.