Abstract
Crickets carry wind-sensitive mechanoreceptors on their cerci, which, in response to the airflow produced by approaching predators, triggers escape reactions via ascending giant interneurons (GIs). Males also activate their cercal system by air currents generated due to the wing movements underlying sound production. Singing males still respond to external wind stimulation, but are not startled by the self-generated airflow. To investigate how the nervous system discriminates sensory responses to self-generated and external airflow, we intracellularly recorded wind-sensitive afferents and ventral GIs of the cercal escape pathway in fictively singing crickets, a situation lacking any self-stimulation. GI spiking was reduced whenever cercal wind stimulation coincided with singing motor activity. The axonal terminals of cercal afferents showed no indication of presynaptic inhibition during singing. In two ventral GIs, however, a corollary discharge inhibition occurred strictly in phase with the singing motor pattern. Paired intracellular recordings revealed that this inhibition was not mediated by the activity of the previously identified corollary discharge interneuron (CDI) that rhythmically inhibits the auditory pathway during singing. Cercal wind stimulation, however, reduced the spike activity of this CDI by postsynaptic inhibition. Our study reveals how precisely timed corollary discharge inhibition of ventral GIs can prevent self-generated airflow from triggering inadvertent escape responses in singing crickets. The results indicate that the responsiveness of the auditory and wind-sensitive pathway is modulated by distinct CDIs in singing crickets and that the corollary discharge inhibition in the auditory pathway can be attenuated by cercal wind stimulation.
Highlights
DISCRIMINATION OF SELF-GENERATED and external signals that occur simultaneously in the same sensory pathway during active behavior is a fundamental challenge for all animals (Cullen 2004; Sperry 1950; von Holst and Mittelstaedt 1950)
In the calling song of the Mediterranean field cricket Gryllus bimaculatus, chirps comprising 4 Ϯ 1 syllables are perseveringly repeated at a rate of 2–3 Hz, and the syllable repetition rate within the chirps is in a range of 25–30 Hz (Ferreira and Ferguson 2002; Schöneich and Hedwig 2012)
The dendrites of the cercal giant interneurons (GIs) are located within the cercal glomerulus of the terminal ganglion (Jacobs and Murphey 1987), where they receive monosynaptic excitatory inputs from wind-sensitive cercal afferents (Matsumoto and Murphey 1977; Shepherd et al 1988)
Summary
DISCRIMINATION OF SELF-GENERATED (reafferent) and external (exafferent) signals that occur simultaneously in the same sensory pathway during active behavior is a fundamental challenge for all animals (Cullen 2004; Sperry 1950; von Holst and Mittelstaedt 1950). Using corollary discharge or an “efference copy” of the motor commands to modulate or cancel the self-generated signals during sensory processing is an effective neuronal mechanism to prevent inappropriate behavioral responses and desensitization of the sensory pathway due to reafferent stimulation (Crapse and Sommer 2008; Poulet and Hedwig 2007). The periodic wing movements of a singing cricket produce notable airflow around the animal’s body (Kämper and Dambach 1985) These self-generated air currents seem not to play a significant role in communication (Pollack et al 1998), but do have particle velocities well above the threshold of the cercal mechanoreceptors to activate giant interneurons (GIs) of the wind-sensitive escape pathway in a resting cricket (Kämper and Dambach 1981; Kumagai et al 1998; Magal et al 2006). If neurons of the cercal escape pathway receive rhythmic inhibition during fictive singing, a situation without any self-induced sensory feedback, it must be www.jn.org
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