Gollisch, Tim; Schütze, Hartmut; Benda, Jan; Herz, Andreas V. M.
Energy integration describes sound-intensity coding in an insect auditory system.
In: The journal of neuroscience, Vol. 22, No. 23: pp. 10434-10448
We investigate the transduction of sound stimuli into neural responses and focus on locust auditory receptor cells. As in other mechanosensory model systems, these neurons integrate acoustic inputs over a fairly broad frequency range. To test three alternative hypotheses about the nature of this spectral integration (amplitude, energy, pressure), we perform intracellular recordings while stimulating with superpositions of pure tones. On the basis of online data analysis and automatic feedback to the stimulus generator, we systematically explore regions in stimulus space that lead to the same level of neural activity. Focusing on such iso-firing-rate regions allows for a rigorous quantitative comparison of the electrophysiological data with predictions from the three hypotheses that is independent of nonlinearities induced by the spike dynamics. We find that the dependence of the firing rates of the receptors on the composition of the frequency spectrum can be well described by an energy-integrator model. This result holds at stimulus onset as well as for the steady-state response, including the case in which adaptation effects depend on the stimulus spectrum. Predictions of the model for the responses to bandpass-filtered noise stimuli are verified accurately. Together, our data suggest that the sound-intensity coding of the receptors can be understood as a three-step process, composed of a linear filter, a summation of the energy contributions in the frequency domain, and a firing-rate encoding of the resulting effective sound intensity. These findings set quantitative constraints for future biophysical models.