Aberrant projection induced by otocyst removal maintains normal tonotopic organization in the chick cochlear nucleus

Abstract

Nucleus magnocellularis (NM), a second-order nucleus in the chick auditory system, is topographically and tonotopically organized. The basilar papilla (cochlea) projects onto the ipsilateral NM via the auditory nerve. The anteromedial region of NM is innervated by the proximal end of the basilar papilla and responds to high-frequency sounds; more posterolateral regions receive input from more distal locations along the papilla and respond to progressively lower frequencies. NM projects exclusively to the third-order neurons of nucleus laminaris (NL). Otocyst removal prevents the formation of the ipsilateral cochlea and cochlear nerve and results in the development of an aberrant functional projection from the contralateral NM to the "deafferented" NM on the operated side of the brain (Jackson and Parks, 1988). In the present experiment, the otocyst was removed unilaterally and the tonotopic organization of the deafferented NM was physiologically mapped at 17-18 d of embryonic age (E17-E18). Quantitative analyses revealed that the frequency organization of the deafferented NM is almost identical to that in normal embryos. Progressively higher characteristic frequencies were recorded at successively more anterior and more medial locations in the nucleus, and the orientation of the tonotopic axis was indistinguishable from normal. Furthermore, the correlation between characteristic frequency and anatomical location is comparable in the deafferented (r = 0.91) and normal (r = 0.87) NM. The only noticeable discrepancy is that characteristic frequencies in NM on both sides of the brain of operated embryos are higher than the frequencies observed previously at comparable regions of the nucleus in unoperated controls. This discrepancy most probably reflects a difference in developmental age between operated embryos (E17-E18) and the normal embryos to which they were compared (E16-E17) and is unrelated to the aberrant projection. The observation that the induced NM-to-NM projection maintains a normal tonotopic organization in the deafferented NM implies that the projection is topographically organized. These findings also support the idea that NM is not a passive receiver of incoming afferents and that the ori-entation of the tonotopic axis in NM is determined by cues intrinsic to the nucleus. It is likely that the cues for orientation are similar in NM and NL, and that the induced NM branches are reading cues comparable to those which their parent axons normally encounter in their innervation of NL.