Development of Inhibitory Mechanisms Underlying Selectivity for the Rate and Direction of Frequency-Modulated Sweeps in the Auditory Cortex

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Abstract
Although it is known that neural selectivity for species-specific vocalizations changes during development, the mechanisms underlying such changes are not known. This study followed the development of mechanisms underlying selectivity for the direction and rate of frequency-modulated (FM) sweeps in the auditory cortex of the pallid bat, a species that uses downward FM sweeps to echolocate. In the adult cortex, direction and rate selectivity arise as a result of different spectral and temporal properties of low-frequency inhibition (LFI) and high-frequency inhibition (HFI). A narrow band of delayed HFI shapes rate selectivity for downward FM sweeps. A broader band of early LFI shapes direction selectivity. Here we asked whether these differences in LFI and HFI are present at the onset of hearing in the echolocation range or whether the differences develop slowly. We also studied how the development of properties of inhibitory frequencies influences FM rate and direction selectivity. We found that adult-like FM rate selectivity is present at 2 weeks after birth, whereas direction selectivity matures 12 weeks after birth. The different developmental time course for direction and rate selectivity is attributable to the differences in the development of LFI and HFI. Arrival time and bandwidth of HFI are adult-like at 2 weeks. Average arrival time of LFI gradually becomes faster and bandwidth becomes broader between 2 and 12 weeks. Thus, two properties of FM sweeps that are important for vocalization selectivity follow different developmental time courses attributable to the differences in the development of underlying inhibitory mechanisms.