Physiological and Anatomical Characteristics of Primary Vestibular Afferent Neurons in the Bullfrog

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Abstract
Intracellular recordings were made in the VIIIth nerve of the bullfrog (R. catesbeiana) to measure the membrane characteristics and obtain records of spontaneous and evoked spike activity of primary semicircular canal afferents. Physiological stimulation of the canals was achieved by rotating the preparation on a servomotor driven turntable with the animal''s head centered in the rotational axis. The responses of each neuron to sinusoidal rotations at frequencies of 0.05 Hz, 0.5 Hz and for impulsive accelerations of 400 deg/s2 were obtained. Membrane characteristics measured included the cell resting and action potential amplitude, and spike-activation threshold for applied currents. Physiologically characterized neurons were injected with horseradish peroxidase [HRP] by applying pneumatic pressure and/or iontophoretic currents to the micropipettes containing 5% HRP in 1 M KCl. Following survival times of 12-48 h, the VIIIth nerve and attached vestibular end organ was removed for histochemical processing using a diaminobenzidine procedure to visualize the HRP reaction product. Light microscopy was used to discern the anatomical features of the neurons and to trace their peripheral dendritic trajectories from the ganglion to their termination(s) in the crista. The bullfrog''s primary vestibular afferents are characterized by a broad range of soma and axon diameters which correspond to an equally broad range of spontaneous and evoked activity characteristics. The largest neurons had more irregular spontaneous firing rates and consistently exhibited the greatest gain and smallest phase shifts with respect to head acceleration. These neurons consistently terminated at or near the central region of the crista. The smallest neurons were characterized by having the most regular spontaneous discharge patterns, the lowest gains and greatest phase shifts with respect to head acceleration. The anatomical features of the primary vestibular neurons are apparently important in determining the neuron''s physiological characteristics. In terms of response dynamics the receptors in the frog''s crista ampullaris are heterogeneous and differentially sensitive to a wide range of stimulus frequencies.