ON-OFF units in the mustached bat inferior colliculus are selective for transients resembling ?acoustic glint? from fluttering insect targets

Abstract

Of 311 single units studied in the central nucleus of the inferior colliculus (ICC) in 18 mustached bats (Pteronotus parnelli), a small but significant population (13%) of cells with on-off discharge patterns to tone bursts at best frequency (BF) was found in the dorsoposterior division. In contrast to units with the same BF's but other discharge patterns, the majority of ON-OFF units were unresponsive to sinusoidally amplitude-modulated tone bursts (SAM). To define the contribution of linear and nonlinear components to the responses of ICC neurons to amplitude modulation, we tested some of these neurons with a long, seamlessly repeating pseudorandom sequence of ternary amplitude-modulated tones at BF. Wiener-like kernels were subsequently derived from cross-correlation of spikes with acoustic events in the sequence. These kernels provided estimates of neural impulse responses that proved unusual in SAM-unresponsive ON-OFF units. First, their estimated impulse response had no linear component. Second, the predicted second-order impulse responses to both increments and decrements in stimulus intensity were long (about 20 ms) and nearly identical in shape: triphasic, with the positive phase bounded by leading and trailing negative periods. The similar shape of responses to increments and decrements in these neurons suggests a full-wave rectifier. The triphasic, initially negative second-order prediction of the impulse response accounted for an unusual result in experiments measuring the recovery cycle of ON-OFF units using a pair of identical stimulus pulses separated by various time delays. This recovery cycle can be related to their response to amplitude modulation. As the delay between two brief, near-threshold BF tone bursts decreased, the response to the first tone diminished, rather than to the second. The second-order prediction of this experiment derived from impulse responses obtained with pseudorandom noise suggests that, at short interpulse intervals, the initial negative phase of the response to the later stimulus cancels the positive phase of the response to the first. Such cancellation at short interpulse intervals may help explain why the majority of ON-OFF units are unresponsive to SAM. The unusual properties of these ON-OFF units make them ideally suited to respond selectively to infrequent acoustic transients superimposed on an ongoing background of modulation. Such patterns are commonly encountered by mustached bats foraging in cluttered habitats for small, fluttering insects, which generate "acoustic glints" upon a background of modulated echoes from the surroundings (Schnitzler et al. 1983; Henson et al. 1987).