Adaptive adjustment of connectivity in the inferior colliculus revealed byfocal pharmacological inactivation

In the midbrain sound localization pathway of the barn owl, a map of audito ry space is synthesized in the external nucleus of the inferior colliculus (ICX) and transmitted to the optic tectum. Early auditory experience shapes these maps of auditory space in part by modifying the tuning of the consti tuent neurons for interaural time difference (ITD), a primary cue for sound -source azimuth. Here we show that these adaptive modifications in ITD tuni ng correspond to changes in the pattern of connectivity within the inferior colliculus. We raised owls with an acoustic filtering device in one ear th at caused frequency-dependent changes in sound timing and level. As reporte d previously, device rearing shifted the representation of ITD in the ICX a nd tectum but not in the primary source of input to the ICX, the central nu cleus of the inferior colliculus (ICC). We applied the local anesthetic lid ocaine (QX-314) iontophoretically in the ICC to inactivate small population s of neurons that represented particular values of frequency and ITD. We me asured the effect of this inactivation in the optic tecta of a normal owl a nd owls raised with the device. In the normal owl, inactivation at a critic al site in the ICC eliminated responses in the tectum to the frequency-spec ific ITD value represented at the site of inactivation in the ICC. The loca tion of this site was consistent with the known pattern of ICC-ICX-tectum c onnectivity. In the device-reared owls, adaptive changes in the representat ion of ITD in the tectum corresponded to dramatic and predictable changes i n the locations of the critical sites of inactivation in the ICC. Given tha t the abnormal representation of ITD in the tectum depended on frequency an d was likely conveyed directly from the ICX, these results suggest that exp erience causes large-scale, frequency-specific adjustments in the pattern o f connectivity between the ICC and the ICX.