Anatomic and physiological correlates in bullfrog vestibular nerve

V. Honrubia, L. F. Hoffman, S. Sitko, I. R. Schwartz


1. The correlations between anatomic and physiological characteristics of primary afferent neurons innervating the anterior semicircular canal in the bullfrog were investigated. These characteristics were examined separately in large groups of neurons, and the direct correlations between them were established in a subset of neurons by means of intraaxonal recording and labeling. 2. Anatomic features of the anterior canalicular nerve that were related with fiber diameter were studied. This nerve was composed of an average of 1,142 fibers (standard deviation of 171 in 5 samples), of which 42% were less than 2 microns in diameter and 8% were greater than 7 microns. The nerve branched into 6 clearly defined bundles, whose fiber diameter-dependent composition could be determined in 5 samples. In the 2 center bundles, 32% of the fibers had diameters greater than 7 microns. In contrast, these thick fibers comprised only 4% of the fiber population in the 2 lateralmost bundles, in which 44% of the fibers had diameters less than 2 microns. The projections of labeled afferent fibers were traced into the neuroepithelium, and it was demonstrated that all thick fibers, even those of the lateral bundles, turned toward more central regions of the crista. Consequently, in the bullfrog, there is a clear predominance of thick afferent fibers innervating the anterior crista's central region and thin fibers in the peripheral region. 3. The dendritic morphology of the broad classes of afferent fibers (i.e., thick and thin) was elucidated. Individually labeled thick afferents possessed dendrites forming short, thick, clawlike extensions to contact a few hair cells. The thinnest afferents were labeled through extracellular horseradish peroxidase (HRP) injections. In contrast to the thick fibers, thin afferents were characterized by an unbranched trajectory with serially located bouton-like structures that were apposed to successive hair cells. 4. The characteristics of spontaneous firing and the responses to rotational stimuli were determined for 138 anterior canalicular neurons. Spontaneous firing rates ranged from 0 to 95 spikes.s-1. The coefficient of variation (CV) of spontaneous firing ranged from 0.12 to 2.5. Response gains to high- (0.5 and 0.4 Hz) and medium- (0.05 Hz) frequency sinusoidal acceleration stimuli were positively correlated with CV (P less than 0.001) for neurons with a CV value less than or equal to 0.5. The gain of neurons characterized by more irregular spontaneous firing (CV values greater than 0.5) was uncorrelated with CV.(ABSTRACT TRUNCATED AT 400 WORDS)