Response of cat semicircular canal afferents to sinusoidal polarizing currents: implications for input-output properties of second-order neurons.

1. We studied the response of cat vestibular afferents, most likely innervating the semicircular canals, to sinusoidal polarizing currents applied to an electrode implanted near the horizontal ampulla. 2. Electrode implantation abolished responses to natural stimulation and reduced the level of resting activity compared to a population of afferents from unimplanted animals. The distribution of coefficients of variation of resting activity was, however, similar to that seen when the labyrinth is intact. 3. Many fibers were modulated sinusoidally by polarizing currents in the frequency range 0.175-4 Hz. Phase was mainly constant and typically led stimulus negativity by approximately 14 degrees, although about half the regular fibers had a phase lead that increased with frequency. Mean sensitivity (spikes X s-1 X microA-1) of regular and irregular fibers increased by a factor of about 1.5 over the frequency studied. Absolute sensitivity was about 7 times higher for irregular than for regular fibers. The overall behavior of the afferents could be well described by a transfer function in the form, sk, with 0 less than k less than 1. 4. We compared the response of afferent fibers to sinusoidal current with the response of second-order neurons studied under similar conditions in earlier experiments (15, 23). While the slopes of the sensitivities were similar, second-order neurons developed a phase advance over afferents at frequencies around 1 Hz. This difference in dynamics can be described by a transfer function in the form tau S + 1, with tau = 12 ms. This predicts that second-order neurons can develop a phase lead of about 25 degrees with respect to afferents at 6 Hz, a frequency still in the physiological range. It remains to be determined whether this applies to a particular subset of second-order neurons contributing to vestibulocollic reflexes.