The Journal of Neuroscience, December 1, 2002, 22(23):10434-10448
Energy Integration Describes Sound-Intensity Coding in an
Insect Auditory System
Tim
Gollisch,
Hartmut
Schütze,
Jan
Benda, and
Andreas V. M.
Herz
Institute for Theoretical Biology, Department of Biology, Humboldt
University, 10115 Berlin, Germany
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.
Key words:
mechanosensory transduction; spectral integration; auditory receptor; hearing; sound intensity; energy; model; locust
Copyright © 2002 Society for Neuroscience 0270-6474/02/222310434-15$05.00/0
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