NEURONAL ENCODING OF SOUND DIRECTION IN THE AUDITORY MIDBRAIN OF THE RAINBOW-TROUT

Acoustical stimulation causes displacement of the sensory hair cells r elative to the otoliths of the fish inner ear. The swimbladder, transf orming the acoustical pressure component into displacement, also contr ibutes to the displacement of the hair cells. Together, this (generall y) yields elliptical displacement orbits. Alternative mechanisms of fi sh directional hearing are proposed by the phase model, which requires a temporal neuronal code, and by the orbit model, which requires a sp ike density code. We investigated whether the directional selective re sponse of auditory neurons in the midbrain torus semicircularis (TS; h omologous to the inferior colliculus) is based on spike density and/or temporal encoding. Rainbow trout were mounted on top of a vibrating t able that was ddven in the horizontal plane to simulate sound source d irection. Rectilinear and elliptical (or circular) motion was applied at 172 Hz. Generally, responses to rectilinear and elliptical/circular stimuli (irrespective of direction of revolution) were the same. The response of auditory neurons was either directionally selective (DS un its, n = 85) or not (non-DS units, n = 106). The average spontaneous d ischarge rate of DS units was less than that of non-DS units. Most DS units (70%) had spontaneous activities <1 spike per second. Response l atencies (mode at 18 ms) were similar for both types of units. The res ponse of DS units is transient ( 19%), sustained (34%), or mixed (47%) . The response of 75% of the DS units synchronized to stimulus frequen cy, whereas just 23% of the non-DS responses did. Synchronized respons es were measured at stimulus amplitudes as low as 0.5 nm (at 172 Hz), which is much lower than for auditory neurons in the medulla of the tr out, suggesting strong convergence of VIIIth nerve input. The instant of firing of 42% of the units was independent of stimulus direction (s hift <15 degrees), but for the other units, a direction dependent phas e shift was observed. in the medial TS spatial tuning of DS units is i n the rostrocaudal direction, whereas in the lateral TS all preferred directions are present. On average, medial DS units have a broader dir ectional selectivity range, are less often synchronized, and show a sm aller shift of the instant of firing as a function of stimulus directi on than lateral DS units. DS response characteristics are discussed in relation to different hypotheses. We conclude that the results are mo re in favor of the phase model.