The morphological development of the cochlea begins in the base or midbasal region and spreads toward the apex. In adults, the base responds maximally to high-frequency sounds and lower frequencies are represented progressively toward the apex. This predicts that responses to sound should occur initially to high frequencies and gradually change to include lower frequencies. Paradoxically, animals respond first to relatively low frequencies and last to high frequencies. We have previously proposed that this discrepancy results from an ontogenetic change in spatial coding of frequency along the cochlea (Rubel et al., '76). According to this model, only the basal end of the cochlea transduces sound early in development but it responds to low frequencies. During maturation the representation of low and midrange frequencies shifts apically and the base becomes responsive to high frequencies. This hypothesis predicts that the tonotopic organization within the central nervous system should change during development; neurons at any given location within an auditory nucleus should become maximally responsive to successively higher frequency sounds during development. In the present study this prediction was tested by using microelectrode recording procedures to map the tonotopic organization of nucleus magnocellullaris (NM) and nucleus laminaris (NL), first- and second-order auditory nuclei, in chickens at three ages: embryonic day 17, 1 day posthatch, and 2-4 weeks posthatch. The characteristic frequencies of neurons having the same anatomical location were quantitatively compared across ages. The tonotopic order in NM and NL was similar at all ages; responses to high-frequency sounds were recorded anteromedially and lower frequencies were located progressively more caudolaterally. However, there was a striking quantitative change in tonotopic organization. Neurons at a given location in both nuclei became maximally responsive to progressively higher frequencies during development. The characteristic frequencies of neurons in embryos and newly hatched chicks averaged, respectively, 1.00 (+/- 0.06, S.E.M.) and 0.34 (+/- 0.04) octaves lower than their predicted adult values. All regions in both nuclei showed a statistically significant increase in characteristic frequency during development except the most posterolateral (low-frequency) sector. Too few neurons were recorded from this region to be able to reliably estimate characteristic frequency. These results support the hypothesis that the spatial coding of frequency along the cochlea shifts during development.(ABSTRACT TRUNCATED AT 400 WORDS)