PHYSIOLOGICAL IDENTIFICATION OF MORPHOLOGICALLY DISTINCT AFFERENT CLASSES INNERVATING THE CRISTAE AMPULLARES OF THE SQUIRREL-MONKEY

1. Semicircular-canal afferents in the squirrel monkey were characterized by their resting discharge, discharge regularity, sensitivity to galvanic currents delivered to the ear (beta*), the gain (g(2) HZ), and phase lead (phi(2) HZ) of their response to 2-Hz sinusoidal head rotations, and their antidromic conduction velocity. Discharge regularity was measured by a normalized coefficient of variation (CV *); the higher the CV*, the more irregular the discharge. g(2) HZ and phi(2) HZ were expressed relative to angular head velocity. 2. These physiological measures were used in an attempt to discern the discharge properties of the three morphological classes of afferents innervating the crista. Presumed bouton (B) fibers were identified as slowly conducting afferents. Presumed calyx (C) fibers were recognized by their irregular discharge and low rotational gains. The remaining fibers were considered to be dimorphic (D) units. Single letters (B, C, and D)are used to emphasize that the classification is based on circumstantial evidence and may be wrong for individual fibers. Of the 125 identified fibers, 13 (10%) were B units, 36 (29%) were C units, and 76 (61%) were D units. 3. B units were regularly discharging. D units ranged from regularly to irregularly discharging. C units were the most irregularly discharging afferents encountered. The mean resting discharge for the entire sample was 74 spikes/s. Resting rates were similar for regularly discharging B and D units and higher than those for irregularly discharging C and D units. 4. Except for their lower conduction velocities, the discharge properties of B units are indistinguishable from those of regularly discharging D units. Many of the discharge properties of B and D units vary with discharge regularity. There is a strong, positive relation when beta*, g(2) HZ or phi(2) HZ is plotted against CV *. For beta* or phi(2) HZ, C units conform to the relation for B and D units. In contrast, values of g(2) HZ for C units are three to four times lower than predicted from the relation for the other two classes. 5. Internal (axon) diameters (d(p)) of peripheral vestibular-nerve fibers were estimated from central antidromic conduction velocities. Thick fibers (d(p) greater than or equal to 4 mu m) were irregularly discharging, mostly C units. Medium-sized fibers (d(p) less than or equal to 1.5 mu m) included regular, intermediate, and irregular D units, as well as C units. Thin fibers (d(p) less than or equal to 1.5 mu m) were defined as B units. 6. By comparing antidromic estimates of d(p) with the axon diameters measured in a morphological study, inferences could be made as to the zones of the crista supplied by recorded units. The comparisons suggest that, as in the chinchilla C units and irregularly discharging D units are concentrated in the central zone of the crista, whereas B units and regularly discharging D units are most plentiful in the peripheral zone. The intermediate zone may contain a mixture of units, including some B and C units, as well as regularly and irregularly discharging D units. The results for D units imply that many of the discharge properties of an afferent reflect regional differences in transduction mechanisms shared by type I and type II hair cells. 7. A linear model of synaptic inputs suggests that the rotational gain of an afferent is related to the sensitivity of its spike encoder and the number of endings it makes with the two kinds of hair cells. The synaptic input to each calyx ending is estimated to be approximately two to three times larger than that to each bouton ending. Quantitative electron microscopy demonstrates that there are 10-15 times as many afferent (ribbon) synapses on individual calyx, as compared with individual bouton, endings, It would thus appear that the afferent synapses on calyx endings are less effective than those on bouton endings. 8. Type II hair cells make synapses with the outer faces of calyx endings. Outer-face synapses are plentiful in the central zone of the chinchilla crista but are rare in the monkey crista. C units have similar discharge properties in the two species, suggesting that the presence of outer-face synapses does not qualitatively alter the physiology of these afferents in the chinchilla.