Encoding of acoustic stimulus intensity by inferior collicular neurons of the big brown bat, Eptesicus fuscus.

Using bats as a model system, we studied the isointensity and isofrequency discharge rate functions of inferior collicular (IC) neurons under free field stimulation conditions in order to understand how the midbrain auditory neurons encode stimulus intensity. For each encountered IC neuron, the best frequency (BF), minimum threshold (MT), tuning curve and intensity rate function for the BF were first determined. Then at a fixed stimulus intensity, the number of impulses was measured for several frequencies which were incrementally chosen across the entire range of the neuron's tuning curve. Such an isointensity discharge rate function was determined for at least three different intensities above each neuron's MT. A series of isofrequency discharge rate functions were also obtained by determining the intensity rate function for each of several frequencies chosen. Among 110 intensity rate functions measured at the BF of each IC neuron, 98 (89%) were non-monotonic and 12 (11%) were monotonic. The profiles of the intensity rate functions measured at several chosen frequencies for each neuron varied greatly. Thus, within the same series of isofrequency intensity rate functions, a neuron showed both monotonic and non-monotonic functions when measured at different frequencies. Similarly, the profile of each intensity rate curve within a series of isointensity rate functions might also vary with stimulus intensity. The isointensity discharge rate functions of most IC neurons (62 neurons, 61%) was triangular shaped reaching a peak value when stimulated with BF. The remaining (39 neurons, 39%) IC neurons had isointensity functions in which different curves peaked at different stimulus frequencies. In some extreme cases, some curves had two peaks or fluctuated within a moderate range of discharge rate throughout the whole range of stimulus frequency. Our studies suggest that encoding of a wide range of acoustic stimulus intensity in the IC involves more than the discharge rate of any one individual IC neuron. Different populations of IC neurons with different BFs will have to work coordinately in order to overcome the limitation of the dynamic range of individual neurons and to solve the ambiguity created by the same discharge rate of each individual neuron to different combinations of frequency and intensity within its auditory response area.