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.

Frequency modulated (FM) sweeps are common components of vocalizations, including human speech. How developmental experience shapes neuronal selectivity for these important signals is not well understood. Here, we show that altered developmental experience with FM sweeps used in echolocation by the pallid bat leads to either a loss of sideband inhibition or millisecond delays in the timing of inhibitory inputs, both of which lead to a reduction in rate and direction selectivity in auditory cortex. FM rate selectivity develops in an experience-independent manner, but requires experience for subsequent maintenance. Direction selectivity depends on experience for both development and maintenance. Rate and direction selectivity are affected by experience over different time periods during development. Altered inhibition may be a general mechanism of experience-dependent plasticity of selectivity for vocalizations.development ͉ response selectivity N eural selectivity for species-specific vocalizations is present in several vertebrate groups (1-8). In songbirds, experience shapes the development of vocalization selectivity (9-11). How experience modifies the receptive fields (RFs) underlying such selectivity has not been characterized. This report focuses on the mechanisms through which developmental experience shapes selectivity of auditory cortex neurons for the rate and direction of FM sweeps present in the echolocation calls of the pallid bat.The pallid bat brings several advantages to the study of experience-dependent plasticity of vocalization selectivity. First, the ontogeny of hearing and vocalization (echolocation) behavior is known (12). Second, nearly 70% of adult auditory cortical neurons tuned in the echolocation range are selective for the sweep rates and the downward sweep direction used in echolocation (13, 14), providing a model system for examining the development of this selectivity. Third, the mechanisms that shape FM sweep selectivity in the adult cortex and the developmental time course of these mechanisms are known (14, 15). FM rate selectivity and the underlying RF properties are adultlike from postnatal day (P) 14, at the onset of adult-like hearing in the echolocation range. This suggests that rate selectivity develops in an experience-independent manner. Direction selectivity and the underlying RF properties become adult-like between P60 and P90, well after the bat has begun to use echolocation, suggesting that experience plays a role in its development. The primary goal of this study was to determine the effects of altering experience with the echolocation call on the development of mechanisms that shape FM rate and direction selectivity. ResultsWe compared FM rate and direction selectivity in four groups of bats: experimental (EXP), control (CTRL), normal, and adults. The EXP pups were isolated from other bats and received laryngeal muscle Botox injections (n ϭ 7 pups) or laryngeal muscle lesions (n ϭ 3 pups). The muscle manipulation was done before the onset of high-frequency hearing (be...