A Neural Mechanism for Time-Window Separation Resolves Ambiguity of Adaptive Coding

The senses of animals are confronted with changing environments and different contexts. Neural adaptation is one important tool to adjust sensitivity to varying intensity ranges. For instance, in a quiet night outdoors, our hearing is more sensitive than when we are confronted with the plurality of sounds in a large city during the day. However, adaptation also removes available information on absolute sound levels and may thus cause ambiguity. Experimental data on the trade-off between benefits and loss through adaptation is scarce and very few mechanisms have been proposed to resolve it. We present an example where adaptation is beneficial for one task—namely, the reliable encoding of the pattern of an acoustic signal—but detrimental for another—the localization of the same acoustic stimulus. With a combination of neurophysiological data, modeling, and behavioral tests, we show that adaptation in the periphery of the auditory pathway of grasshoppers enables intensity-invariant coding of amplitude modulations, but at the same time, degrades information available for sound localization. We demonstrate how focusing the response of localization neurons to the onset of relevant signals separates processing of localization and pattern information temporally. In this way, the ambiguity of adaptive coding can be circumvented and both absolute and relative levels can be processed using the same set of peripheral neurons.