Ontogenesis of tonotopy in inferior colliculus of a hipposiderid bat reveals postnatal shift in frequency-place code

Abstract

The postnatal development of midbrain tonotopy was investigated in the inferior colliculus (IC) of the south Indian CF-FM bat Hipposideros speoris. The developmental progress of the three-dimensional frequency representation was determined by systematic stereotaxic recordings of multiunit clusters from the 1st up to the 7th postnatal week. Additional developmental measures included the tuning characteristics of single units (Figs. 3f; 4f; 5f), the analysis of the vocalised pulse repertoire (Figs. 3e, 4e, 5e), and morphometric reconstructions of the brains of all experimental animals (Fig. 1). The maturation of auditory processing could be divided into two distinct, possibly overlapping developmental periods: First, up to the 5th week, the orderly tonotopy in the IC developed, beginning with the low frequency representation and progressively adding the high frequency representation. With regard to the topology of isofrequency sheets within the IC, maturation progresses from dorsolateral to ventromedial (Figs. 3c, 4c). At the end of this phase the entire IC becomes specialised for narrowly tuned and sensitive frequency processing. This includes the establishment of the 'auditory fovea', i.e. the extensive spatial representation of a narrow band of behaviorally relevant frequencies in the ventromedial part of the IC. In the 5th postnatal week the auditory fovea is concerned with frequencies from 100-118 kHz (Fig. 4c, d). During subsequent development, the frequency tuning of the auditory fovea increases by 20-25 kHz and finally attains the adult range of ca. 125-140 kHz. During this process, neither the bandwidth of the auditory fovea (15-20 kHz) nor the absolute sensitivity of its units (ca. 50 dB SPL) were changed. Further maturation occurred at the single unit level : the sharpness of frequency tuning increased from the 5th to the 7th postnatal weeks (Q-₁₀-dB-values up to 30-60), and upper thresholds emerged (Figs. 4f, 5f). Although in the adult the frequency of the auditory fovea matches that of the vocalised pulses, none of the juvenile bats tested from the 5th to the 7th weeks showed such a frequency match between vocalisation and audition (Figs. 4e, 5e). The results show that postnatal maturation of audition in hipposiderid bats cannot be described by a model based on a single developmental parameter.