The vestibular nerve of the chinchilla. V. Relation between afferent discharge properties and peripheral innervation patterns in the utricular macula.

1. The relation between the discharge properties of utricular afferents and their peripheral innervation patterns was studied in the chinchilla by the use of intra-axonal labeling techniques. Fifty-three physiologically characterized units were injected with horseradish peroxidase (HRP) or lucifer yellow CH (LY) and their labeled processes were traced to the utricular macula. For most labeled neurons, the discharge regularity, background discharge, and sensitivity to externally applied galvanic currents were determined, as were the gain (g2 Hz) and phase (phi 2 Hz) of the response to 2-Hz sinusoidal linear forces. Terminal fields were reconstructed and fibers were classified as calyx (n = 13) or dimorphic units (n = 40). No bouton units were recovered. Calyx units were confined to the striola. Dimorphic units were located in the striola (n = 8), the juxtastriola (n = 7), or the peripheral extrastriola (n = 25). 2. To determine whether the intra-axonal sample was representative, the physiological properties of labeled utricular units were compared with those of a larger sample of extracellularly recorded units. A comparison was also made between the morphology of intra-axonally labeled units and those labeled by the extracellular injection of HRP into the vestibular nerve. Most of the discrepancies between the intra-axonal and either extracellular sample can be explained by assuming that small-diameter fibers are underrepresented in the former sample. Dimorphic fibers labeled intra-axonally had more bouton endings and larger terminal trees than did those labeled extracellularly. The latter differences may reflect a sampling bias in the extracellular material. 3. Calyx units were irregularly discharging. The discharge regularity of dimorphic units was related to their macular locations. Only 1/8 dimorphic units in the striola was regularly discharging. The ratio increases to 3/7 in the juxtastriola and to 23/25 in the peripheral extrastriola. Among dimorphic units, there is a tendency for irregularly discharging afferents to have fewer bouton endings. The trend is far from perfect because it is possible to pick a subsample of dimorphic units that have similar numbers of boutons and, yet, have discharge patterns that range from regular to irregular. 4. Published morphological polarization maps can be used to predict the excitatory tilt directions of a unit from its macular location. Predictions were confirmed in 39/41 labeled afferents. 5. The galvanic sensitivity (beta *) of an afferent, irrespective of its peripheral innervation pattern or its epithelial location, was strongly correlated with a normalized coefficient of variation (CV*).(ABSTRACT TRUNCATED AT 400 WORDS)