Leading Inhibition to Neural Oscillation Is Important for Time-Domain Processing in the Auditory Midbrain

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Abstract
A number of central auditory neurons exhibit paradoxical latency shift (PLS), a response characterized by longer response latencies at higher sound levels. PLS neurons are known to play a role in target ranging for echolocating bats that emit frequency-modulated sounds. We recently reported that early inhibition of unit’s oscillatory discharges is critical for PLS in the inferior colliculus (IC) of little brown bats. The goal of this study was to determine in echolocating bats and in nonecholocating animals (frogs): 1) the detailed characteristics of PLS and whether PLS was dependent on sound level, frequency, and duration; 2) the time course of inhibition underlying PLS using a paired-pulse paradigm. We found that 22% of IC neurons in bats and 15% in frogs exhibited periodic discharge patterns in response to tone pulses at high sound levels. The firing periodicity was unit specific and independent of sound level and duration. Other IC neurons (28% in bats; 14% in frogs) exhibited PLS. These PLS neurons shared several response characteristics: 1) PLS was largely independent of sound frequency and 2) the magnitude of shift in first-spike latency was either duration dependent or duration tolerant. For PLS neurons, application of bicuculline abolished PLS and unmasked the unit’s periodical firing pattern that served as the building block for PLS. In response to paired sound pulses, PLS neurons exhibited delay-dependent response suppression, confirming that high-threshold leading inhibition was responsible for PLS. Results also revealed the timing of excitatory and inhibitory inputs underlying PLS and its role in time-domain processing.