Morphological correlates of response dynamics and efferent stimulation in horizontal semicircular canal afferents of the toadfish, Opsanus tau

Abstract

1. We used the intraaxonal labeling technique to study correlations between the terminal dendritic morphology of horizontal semicircular canal primary afferents and their response dynamics to sinusoidal head rotation and combined electrical stimulation of central efferent vestibular neurons. Thirty-eight canal afferents were identified by their sensitivity and phase of response to rotation between 0.1 and 1.0 Hz (+/- 10 degrees/s) and were subsequently labeled with horseradish peroxidase or biocytin. The afferent's dendritic field and synaptic specializations in the neuroepithelium of the crista were examined under light microscopy. 2. Rate and regularity of background discharge of the afferent were not correlated with its axon diameter or relative location of its dendritic field in the crista. 3. Response sensitivity of the afferent to rotation was correlated both with the relative location of its dendritic field in the crista and with the number of terminal endings it possesses. Afferents having low sensitivities, slow dynamics, and few terminal endings supply the peripheral portions of the crista; afferents with higher sensitivities, faster dynamics, and greater number of terminal endings supply the more central portions. It is suggested that the differences in sensitivity among the afferents reflect principally the variations in both the cupular dynamics along the crista and the number of possible hair cell contact sites in the neuroepithelium. 4. Response phase of the afferent was correlated only with the extent of its dendritic processes along the transverse axis of the crista. Afferents having transversely oriented dendritic fields had less phase lags relative to acceleration than did those having a more longitudinally oriented dendritic field. 5. Efferent stimulation produced a change in both the afferent's discharge rate and its response sensitivity to rotation. Afferents discharge rate and its response sensitivity to rotation. Afferents having a centrally located dendritic field and acceleration afferents, defined by their response to rotation, were the most affected by efferent stimulation. These results suggest that efferent innervation is either directed toward, or most efficacious in, the central regions of the crista and that it may select specific hair cell-afferent complexes.

Efferent Actions in the Chinchilla Vestibular Labyrinth

“…Excitation, revealed by an increase in afferent discharge, is seen in a fraction of irregularly discharging afferents in the frog (Rossi et al 1980(Rossi et al , 1994Bernard et al 1985;Sugai et al 1991) and in calyx-bearing afferents in the turtle (Brichta and Goldberg 2000). It is the predominant action in the horizontal crista of the toadfish (Boyle and Highstein 1990;Boyle et al 1991) and in the entire vestibular labyrinth of mammals (Goldberg and Fernández 1980). The basis of the excitation may be heterogeneous.…”

“…More heterogeneous responses have been seen in vestibular organs of frogs (Rossi et al 1980(Rossi et al , 1994Bernard et al 1985;Sugai et al 1991) and turtles (Brichta and Goldberg 2000) and include both increases and decreases in afferent discharge. In the toadfish, the predominant effect is an increase in afferent discharge (Boyle and Highstein 1990;Boyle et al 1991). Studies in the squirrel monkey (Goldberg and Fernández 1980) and cat (McCue and Guinan 1994) have shown that the main efferent actions in mammals are excitatory.…”

Ionic Composition of Endolymph and Perilymph in the Inner Ear of the Oyster Toadfish,Opsanus tau

“…This species is well established as an animal model for the study of vestibular end-organ physiology (Boyle and Highstein, 1990a, b;Boyle et al, 1991;Rabbitt et al, 1994Rabbitt et al, , 1999Highstein et al, 1996;Ghanem et al, 1998;Ghanem, 2002). Ion-selective microelectrodes were the logical choice for the in vivo measurements due to the limited access and relatively small volumes of inner ear fluids.…”

Ultrastructural observations of efferent terminals in the crista Ampullaris of the toadfish, opsanus tau

“…The crista ampullaris of the toadfish horizontal semicircular canal is an inverted saddle-shaped structure which extends across the ampullary enlargement and is anchored at its distal end to the ampullary wall (for a detailed description, see Boyle et al 1991). Sensory hair cells and supporting cells form a compact receptor sheet that is estimated to be~940 µm long, and varying in width from 250-300 µm at the proximal and distal ends, respectively, to~130 µm at the central isthmus (Boyle et al 1991).…”

“…Sensory hair cells and supporting cells form a compact receptor sheet that is estimated to be~940 µm long, and varying in width from 250-300 µm at the proximal and distal ends, respectively, to~130 µm at the central isthmus (Boyle et al 1991). Classically, two types of receptor cells have been distinguished in the cristae of amniotes (reptiles, birds and mammals): flask-shaped type I and cylindrical type II hair cells.…”