Neural Mechanisms Underlying Selectivity for the Rate and Direction of Frequency-Modulated Sweeps in the Inferior Colliculus of the Pallid Bat

Abstract

This study describes mechanisms that underlie neuronal selectivity for the direction and rate of frequency-modulated sweeps in the central nucleus of the inferior colliculus (ICC) of the pallid bat (Antrozous pallidus). This ICC contains a high percentage of neurons (66%) that respond selectively to the downward sweep direction of the bat's echolocation pulse. Some (19%) are specialists that respond only to downward sweeps. Most neurons (83%) are also tuned to sweep rates. A two-tone inhibition paradigm was used to describe inhibitory mechanisms that shape selectivity for sweep direction and rate. Two different mechanisms can create similar rate tuning. The first is an early on-best frequency inhibition that shapes duration tuning, which in turn determines rate tuning. In most neurons that are not duration tuned, a delayed high-frequency inhibition creates rate tuning. These neurons respond to fast sweep rates, but are inhibited as rate slows, and delayed inhibition overlaps excitation. In these neurons, starting a downward sweep within the excitatory tuning curve eliminates rate tuning. However, if rate tuning is shaped by duration tuning, this manipulation has no effect. Selectivity for the downward sweep direction is created by an early low-frequency inhibition that prevents responses to upward sweeps. In addition to this asymmetry in arrival times of low- and high-frequency inhibitions, the bandwidth of the low-frequency sideband was broader. Bandwidth influences the arrival time of inhibition during an FM sweep because a broader sideband will be encountered sooner. These findings show that similar spectrotemporal filters can be created by different mechanisms.