April 1, 2003 (Bethesda, MD) – How do we hear when some of us chatter all day? When we sing in the shower, why doesn’t the active voice smother the rest of our body’s sensory systems? The answer to these questions may be found in the simple male cricket (Gryllus bimaculatus), which sing for hours at over 100 decibels sound pressure levels (dB SPL) in order to attract females.
The “songs” of crickets (except the one from Disney’s famous character, “Jiminy Cricket, are generated by rhythmically rubbing the fore wings together resulting in a form of sound production called stridulation. As crickets’ ears are located on the forelegs, they are fully exposed to the self-generated sounds. Many animals reduce the responsiveness of their peripheral auditory system during sound production, but crickets do not. Despite this, behavioral experiments have shown that singing crickets can respond to external sounds.
A modulation in the sensitivity to reafferent (self-generated) stimulation by centrally generated neural signals has been identified in a variety of sensory systems, e.g., visual, electroreceptive, proprioceptive (perception at the subconscious level), and mechanoreceptive. A reduction in the responsiveness of auditory neurons in the brain has been recorded in humans and other vertebrates during vocalization, but the nature and source of the inhibition has never been characterized.
Crickets sing so loudly that reafferent sound could be confused with external sound and/or desensitize the cricket’s own auditory system. One solution to this problem could be to modulate the biophysical sensitivity of the ear during sound production. However, the tympanic membrane of the cricket remains fully responsive during stridulation.
A New Study
Researchers have examined how their central and simple auditory system copes with the intense reafferent stimulation through desensitizing effect of loud sounds on the responsiveness of ON1. Their research consisted of making intracellular recordings of auditory afferents and an identified auditory interneuron the Omega 1 neuron (ON1) during stridulation. The authors of “A Corollary Discharge Mechanism Modulates Central Auditory Processing in Singing Crickets,” are J.F.A. Poulet and B. Hedwig, from the Department of Zoology, University of Cambridge, Cambridge, United Kingdom. Their findings appear in the March 2003 edition of the Journal of Neurophysiology, one of 14 publications published monthly by the American Physiological Society.
All experiments were performed on adult male G. bimaculatus selected from a cricket colony maintained on a 12 hour light/12 hour dark cycle. Prior to dissection they were chilled at 4°C for 30 min. They were then fixed in a standing position on a holder that allowed free rotation of the animal. To allow for silent stridulation, the left wing of the crickets was removed. When recording false stridulation, the cricket was placed upside down in a Plasticene well and its ventral cuticle was removed to expose the abdominal and thoracic ganglia. The thoracic or thoracic and abdominal nerves were cut, except for prothoracic nerve #5, which contains the auditory afferents. Care was taken not to damage the main ventral trachea. To deafen crickets, the forelegs were removed just distal to the coxa. Other procedures performed include pharmacological stimulation, acoustic stimulation, as well as recordings on auditory neurons.
During sonorous stridulation, the auditory afferents and ON1 responded with bursts of spikes to the crickets’ own song. When the crickets were stridulating silently, after one wing had been removed, only a few spikes were recorded in the afferents and ON1. Primary afferent depolarizations (PADs) occurred in the terminals of the auditory afferents, and inhibitory postsynaptic potentials (IPSPs) were apparent in ON1. The PADs and IPSPs were composed of many summed, small-amplitude potentials that occurred at a rate of about 230 Hz. The PADs and the IPSPs started during the closing wing movement and peaked in amplitude during the subsequent opening wing movement. As a consequence, during silent stridulation, the ON1 response to acoustic stimuli was maximally inhibited during wing opening. Inhibition coincides with the time when ON1 would otherwise be most strongly excited by self-generated sounds in a sonorously stridulating cricket. The PADs and the IPSPs persisted in fictively stridulating crickets whose ventral nerve cord had been isolated from muscles and sense organs.
The findings demonstrate that the corollary discharge inhibition during the chirps will prevent desensitization in ON1 and allow the cricket to hear quieter, subsequent sounds in the chirp intervals. In a group of stridulating male G. bimaculatus, where individuals are spaced apart by two meters on average, the ability to hear during singing will be an advantage. It would allow males to defend their territory from rival singing males, to maintain a fixed distance from each other, and to hear noisy predators
This strongly suggests that the inhibition of the auditory pathway is the result of a corollary discharge from the stridulation motor network. Hyperpolarizing current injection into ON1 while it was responding to a 100 dB SPL sound pulse mimicked the central inhibition. This suppressed its spiking response to the acoustic stimulus and maintained its response to subsequent, quieter stimuli. The corollary discharge therefore prevents auditory desensitization in stridulating crickets and allows the animals to respond to external acoustic signals during the production of calling song.
Source: March 2003 edition of the Journal of Neurophysiology
The American Physiological Society (APS) was founded in 1887 to foster basic and applied science, much of it relating to human health. The Bethesda, MD-based Society has more than 10,000 members and publishes 3,800 articles in its 14 peer-reviewed journals every year.
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