BINAURAL INHIBITION IS IMPORTANT IN SHAPING THE FREE-FIELD FREQUENCY-SELECTIVITY OF SINGLE NEURONS IN THE INFERIOR COLLICULUS

1. We have shown previously that under free-field stimulation in the f rontal field, frequency selectivity of the majority of inferior collic ulus (IC) neurons became sharper when the loudspeaker was shifted to i psilateral 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 t he frequency selectivity of IC neurons under several conditions: monau ral stimulation using a semiclosed acoustical stimulation system, bina ural stimulation dichotically also using a semiclosed system, free-fie ld stimulation from different azimuths, and free-field stimulation whe n the ipsilateral ear was occluded monaurally (coated with a thick lay er of petroleum jelly, which effectively attenuated acoustic input to this ear). 2. The binaural interaction pattern of 98 IC neurons of nor thern leopard frogs (Rana pipiens pipiens) were evaluated; of these ne urons, 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 di minished response when the ipsilateral and contralateral ears were sti mulated simultaneously) whether they were designated as EE or EO; thes e IC neurons thus were classified as EE-I or EO-I. Neurons were classi fied as exhibiting strong inhibition if the ILD function showed a pron ounced response decrement, i.e., a decrease of greater than or equal t o 50% of the response to monaural stimulation of the contralateral ear . Those neurons that showed smaller response decrements (decrease was greater than or equal to 25% but <50%) were designated as showing weak inhibition. Most of these EE-I and EO-I neurons (n = 68) showed stron g binaural inhibition. 3. In agreement with results from our earlier s tudies, frequency threshold curves (FTCs) of IC neurons were altered b y sound azimuth. Independent of binaural interaction pattern, most IC neurons (59 of 98) showed a narrowing of the FTC as sound direction wa s changed from contralateral 90 deg (c90 degrees) to ipsilateral 90 de g (i90 degrees). IC neurons that exhibited the largest direction-depen dent changes in frequency selectivity were typically those that displa yed stronger binaural inhibition. Occlusion of the ipsilateral ear, wh ich 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 wea k 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 na rrowing of the FTC, about one-third (34 of 98) of IC neurons studied s howed a broadening of the FTC when sound direction was shifted to ipsi lateral azimuths. Interestingly, for 90% of these 34 neurons, monaural occlusion resulted in narrowing of the bandwidth at each azimuth inst ead of broadening of the FTC bandwidth. We have evidence to suggest th at 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 ind ependent contralateral and ipsilateral stimulation. FTCs derived from ipsilateral monaural stimulation were significantly narrower than thos e resulting from contralateral monaural stimulation, independent of a neuron's direction-dependent changes in frequency selectivity. These r esults demonstrated that the narrower excitatory FTCs to ipsilateral m onaural stimulation cannot be the primary contributor to the sharpenin g of FTCs in some EE cells, and broadening in other EE cells, in respo nse to stimulation from ipsilateral azimuths in the free field. 7. The se results support our hypothesis that binaural interactions, particul arly binaural inhibition, play a role in the sharpening of frequency s electivity in the frog IC.