Binaural inhibition is important in shaping the free-field frequency selectivity of single neurons in the inferior colliculus.

Abstract

1. We have shown previously that under free-field stimulation in the frontal field, frequency selectivity of the majority of inferior colliculus (IC) neurons became sharper when the loudspeaker was shifted to ipsilateral azimuths. These results indicated that binaural inhibition may be responsible for the direction-dependent sharpening of frequency selectivity. To test the above hypothesis directly, we investigated the frequency selectivity of IC neurons under several conditions: monaural stimulation using a semiclosed acoustical stimulation system, binaural stimulation dichotically also using a semiclosed system, free-field stimulation from different azimuths, and free-field stimulation when the ipsilateral ear was occluded monaurally (coated with a thick layer of petroleum jelly, which effectively attenuated acoustic input to this ear). 2. The binaural interaction pattern of 98 IC neurons of northern leopard frogs (Rana pipiens pipiens) were evaluated; of these neurons, there were 34 EE and 64 EO neurons. The majority of IC neurons (92 of 98) showed some degree of binaural inhibition (i.e., showing diminished response when the ipsilateral and contralateral ears were stimulated simultaneously) whether they were designated as EE or EO; these IC neurons thus were classified as EE-I or EO-I. Neurons were classified as exhibiting strong inhibition if the ILD function showed a pronounced response decrement, i.e., a decrease of > or = 50% of the response to monaural stimulation of the contralateral ear. Those neurons that showed smaller response decrements (decrease was > or = 25% but < 50%) were designated as showing weak inhibition. Most of these EE-I and EO-I neurons (n = 68) showed strong binaural inhibition. 3. In agreement with results from our earlier studies, frequency threshold curves (FTCs) of IC neurons were altered by sound azimuth. Independent of binaural interaction pattern, most IC neurons (59 of 98) showed a narrowing of the FTC as sound direction was changed from contralateral 90 deg (c90 degrees) to ipsilateral 90 deg (i90 degrees). IC neurons that exhibited the largest direction-dependent changes in frequency selectivity were typically those that displayed stronger binaural inhibition. Occlusion of the ipsilateral ear, which reduced the strength of binaural inhibition by this ear, abolished direction-dependent frequency selectivity. 4. FTCs of IC neurons that exhibited little to moderate direction-dependent effects on frequency selectivity were associated typically with neurons that displayed weak binaural inhibition. Associated with this weak binaural inhibition, central neural responses under monaural occlusion also displayed only small effects; the FTCs were only slightly broader than those derived in the intact condition, and as before, the experimental manipulation resulted in abolishment of direction-dependent frequency selectivity. 5. In contrast to most IC neurons, which showed direction-dependent narrowing of the FTC, about one-third (34 of 98) of IC neurons studied showed a broadening of the FTC when sound direction was shifted to ipsilateral azimuths. Interestingly, for 90% of these 34 neurons, monaural occlusion resulted in narrowing of the bandwidth at each azimuth instead of broadening of the FTC bandwidth. We have evidence to suggest that this direction-dependent broadening is actually a consequence of a truncation or loss of the tip of the FTC derived at c90 degrees, which results from strong binaural inhibition. 6. To compare the frequency threshold tuning in response to monaural stimulation of each ear with free-field FTCs, we measured FTCs for each of the 34 EE neurons to independent contralateral and ipsilateral stimulation. FTCs derived from ipsilateral monaural stimulation were significantly narrower than those resulting from contralateral monaural stimulation, independent of a neuron's direction-dependent changes in frequency selectivity.