Response recovery in the locust auditory pathway

Temporal resolution and the time courses of recovery from acute adaptation of neurons in the auditory pathway of the grasshopper Locusta migratoria were investigated with a response recovery paradigm. We stimulated with a series of single click and click pair stimuli while performing intracellular recordings from neurons at three processing stages: receptors and first and second order interneurons. The response to the second click was expressed relative to the single click response. This allowed the uncovering of the basic temporal resolution in these neurons. The effect of adaptation increased with processing layer. While neurons in the auditory periphery displayed a steady response recovery after a short initial adaptation, many interneurons showed nonlinear effects: most prominent a long-lasting suppression of the response to the second click in a pair, as well as a gain in response if a click was preceded by a click a few milliseconds before. Our results reveal a distributed temporal filtering of input at an early auditory processing stage. This set of specified filters is very likely homologous across grasshopper species and thus forms the neurophysiological basis for extracting relevant information from a variety of different temporal signals. Interestingly, in terms of spike timing precision neurons at all three processing layers recovered very fast, within 20 ms. Spike waveform analysis of several neuron types did not sufficiently explain the response recovery profiles implemented in these neurons, indicating that temporal resolution in neurons located at several processing layers of the auditory pathway is not necessarily limited by the spike duration and refractory period.