Reduced influence of the ipsilateral ear on spatial tuning of auditory neurons in the albino superior colliculus: a knock-on effect of anomalies of the acoustic chiasm?

Abstract

Auditory brainstem abnormalities affecting decussation patterns and nuclei involved in the acoustic chiasm exist in a variety of albino mammals, suggesting that binaural processes underlying spatial hearing may be disrupted in these mutants. To evaluate this we have compared the contribution of the two ears in albino and normally pigmented guinea pigs to the spatial tuning of auditory neurons in the deep layers of the superior colliculus (SC). Broadband noise stimuli at threshold and at suprathreshold intensities were presented from different azimuthal loudspeaker locations under free-field anechoic conditions, and auditory receptive fields were plotted before, during and after occluding the ipsilateral ear. We show that the deep layers of the albino SC contain a map of contralateral auditory azimuth along its anteroposterior axis, which is aligned with the visual map in the superficial layers above, just as in normal animals. We also show that threshold spatial responses are elicited only via the contralateral ear and at similar stimulus intensities (mean approximately 30 dB SPL) in the two pigmentation phenotypes. The mechanisms that maintain spatial tuning at sound intensities of 10-40 dB above threshold, however, differ markedly in these animals. Plugging the ipsilateral ear in normal guinea pigs caused significant expansions of their auditory receptive fields and loss of directional tuning, but in the albinos occlusion had little effect on these spatial properties. The results suggest that while spatial selectivity for relatively loud sounds among SC neurons is normally maintained via the binaural combination of contralateral excitatory drive and ipsilateral inhibition, it is achieved in albinos almost exclusively by monaural input from the contralateral ear. This finding is consistent with an excessive contralateral ear dominance of higher levels of the albino auditory system caused by anomalies of their acoustic chiasm, analogous to the monocular dominance of the visual system that results from excessive axon crossing at the optic chiasm in these animals.