Differential central projections of physiologically characterized horizontal semicircular canal vestibular nerve afferents in the toadfish,Opsanus tau

Abstract

Anatomical and neurophysiological studies were undertaken to examine the central projection pattern of physiologically characterized horizontal semicircular canal vestibular nerve afferents in the toadfish, Opsanus tau. The variations in individual response characteristics of vestibular nerve afferents to rotational stimulus provided a means of typing the afferents into descriptive classes; the afferents fell into a broad continuum across the spectrum from low-gain, velocity-sensitive to high-gain, acceleration-sensitive responses (Boyle and Highstein [1990b] J. Neurosci. 10:1557-1569; Boyle and Highstein [1990a] J. Neurosci. 10:1570-1582). In the present study, each afferent was typed as a low-gain, high-gain, or acceleration fiber during rotational or mechanical stimulation (Rabbitt et al. [1995] J. Neurophysiol. 73:2237-2260) and was then intracellularly injected with biocytin. The axons were reconstructed, and the morphology, synaptic boutons, and projection pattern of each axon were determined. The results indicated that the three descriptive classes of vestibular nerve afferents have unique as well as overlapping central projection patterns and destinations in the vestibular nuclei, with intranuclear parcellation in the anterior octavus, magnocellularis, tangentialis, posterior octavus, and descending octavus nuclei. In general, increased sensitivity and faster response dynamics were correlated with both a more extensive central projection and a progressive increase in morphological complexity. Low-gain, velocity-sensitive fibers were the simplest morphologically, with the fewest number of branches (n = 17) and shortest length (4,282 microm), and projections were confined to the middle portions of the vestibular nuclei. High-gain, velocity-sensitive fibers were morphologically more diverse than low-gain fibers, with a greater number of branches (n = 26), longer length (6,059 microm), 29% greater volume, and a more widespread projection pattern with projections to both the anterior and the middle portions of the vestibular nuclei. Acceleration fibers were morphologically distinct from low- and high-gain fibers, with more elaborate branching (n = 41), greatest overall length (17,370 microm) and volume (16% greater than high gains), and displayed the most extensive central projection pattern, innervating all vestibular nuclei except tangentialis. Thus, there are anatomically demonstrable differential central projections of canal afferents with different response dynamics within the vestibular complex of the fish.

Physiological evidence for binaural directional computations in the brainstem of the oyster toadfish,Opsanus tau(L.)

“…The ventral vestibular division of the DON (Highstein et al, 1992;Mensinger et al, 1997) also contributes homotopic projections to the commissural tract, leading to speculation that the commissural tract may be part of a common mode rejection circuit, as has been described in the electrosensory medulla of skates (New and Bodznick, 1990;Bodznick et al, 1999). Rejection of redundant bilateral information (or self-generated noise from opercular movements) may be a component of the DON commissural tract, but comparison of left and right auditory inputs by toadfish has an obvious role in directional hearing as well (Fay, 2005).…”

Afferent diversity and the organization of central vestibular pathways

“…The proximal innervation of neurons with the largest cell bodies is derived almost exclusively from irregular fibers (cf. A similar analysis has been done in the toadfish (Mensinger et al 1997). The authors classified horizontal-canal afferents by their gains and phases.…”

Gamma-aminobutyric acid is a neurotransmitter in the auditory pathway of oyster toadfish, Opsanus tau

“…The axons of primary auditory afferents innervating the saccule branch centrally to provide inputs to multiple sites along the rostro-caudal extent of the ipsilateral descending octaval nucleus (DON) (Edds-Walton et al, 1999). Although not clearly delineated anatomically, functional subdivisions have been demonstrated in the DON of toadfish: auditory processing occurs in the dorsal portion of the nucleus (Edds-Walton et al, 1999; Edds-Walton and Fay, 2008), whereas vestibular processing occurs more ventrally (Highstein et al, 1992; Mensinger et al, 1997). Moreover, tract-tracing studies combined with physiological recordings in the auditory midbrain have confirmed that a subset of cells in the ipsilateral and contralateral dorsal DON of the toadfish project to the auditory midbrain (torus semicircularis, TS)(Edds-Walton and Fay, 2003), along with ipsilateral and contralateral projections from secondary octaval populations.…”