Despite their simple auditory systems, some insect species recognize certai
n temporal aspects of acoustic stimuli with an acuity equal to that of vert
ebrates; however, the underlying neural mechanisms and coding schemes are o
nly partially understood. In this study, we analyze the response characteri
stics of the peripheral auditory system of grasshoppers with special emphas
is on the representation of species-specific communication signals. We use
both natural calling songs and artificial random stimuli designed to focus
on two low-order statistical properties of the songs: their typical time sc
ales and the distribution of their modulation amplitudes.
Based on stimulus reconstruction techniques and quantified within an inform
ation-theoretic framework, our data show that artificial stimuli with typic
al time scales of >40 msec can be read from single spike trains with high a
ccuracy. Faster stimulus variations can be reconstructed only for behaviora
lly relevant amplitude distributions. The highest rates of information tran
smission (180 bits/sec) and the highest coding efficiencies (40%) are obtai
ned for stimuli that capture both the time scales and amplitude distributio
ns of natural songs.
Use of multiple spike trains significantly improves the reconstruction of s
timuli that vary on time scales <40 msec or feature amplitude distributions
as occur when several grasshopper songs overlap. Signal-to-noise ratios ob
tained from the reconstructions of natural songs do not exceed those obtain
ed from artificial stimuli with the same low-order statistical properties.
We conclude that auditory receptor neurons are optimized to extract both th
e time scales and the amplitude distribution of natural songs. They are not
optimized, however, to extract higher-order statistical properties of the
song-specific rhythmic patterns.