Neural mechanism of experience-dependent sensory gain control in c. elegans

Animals' sensory systems adjust their responsiveness to environmental
stimuli that vary greatly in their intensity. Here we report the neural
mechanism of experience-dependent sensory adjustment, especially gain
control, in the ASH nociceptive neurons in Caenorhabditis elegans. Using
calcium imaging under gradual changes in stimulus intensity, we find that
the ASH neurons of naive animals respond to concentration increases in a
repulsive odor 2-nonanone regardless of the magnitude of the concentration
increase. However, after preexposure to the odor, the ASH neurons exhibit
significantly weak responses to a small gradual increase in odor
concentration while their responses to a large gradual increase remain
strong. Thus, preexposure changes the slope of stimulus-response
relationships (i.e., gain control). Behavioral analysis suggests that this
gain control contributes to the preexposure-dependent enhancement of odor
avoidance behavior. Mathematical analysis reveals that the ASH response
consists of fast and slow components, and that the fast component is
specifically suppressed by preexposure for the gain control. In addition,
genetic analysis suggests that G protein signaling is required for the
fast component. Thus, our integrative study demonstrates how prior
experience dynamically modulates stimulus-response relationships in
sensory neurons, eventually leading to adaptive modulation of behavior.