Corollary discharge modulation of wind-sensitive interneurons in the singing cricket
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1
University of Cambridge, Department of Zoology, United Kingdom
A fundamental challenge for sensory systems is the processing of an animal’s self-generated (reafferent) sensory information and information from the environment (exafferent signals) that occurs simultaneously in the same pathway. One solution to this problem is a corollary discharge that is driven by the animal’s own motor commands and interferes with the ongoing sensory processing.
In singing field crickets, which expose their hearing system to their loud song when calling for females, an identified corollary discharge interneuron (CDI) provides central control of auditory processing. This CDI mediates rhythmic pre- and postsynaptic inhibition to auditory afferents and interneurons during singing (Poulet and Hedwig 2002 Nature 418:872-876). Each side of the cricket central nervous system houses one singing CDI with the cell body and dendrites in the mesothoracic ganglion and axonal branches stretching from the brain to the terminal ganglion (Poulet and Hedwig 2006 Science 311:518-522). Although axonal arborizations of the singing CDI are especially profuse in the auditory neuropile of the prothoracic ganglia, its overall morphology implies that this neuron modulates other sensory pathways as well.
Besides sound, the forewing movements of a singing cricket produce notable air currents. When similar air currents stimulate the highly wind-sensitive cercal mechanoreceptors in a resting cricket they reliably trigger fast escape reactions by activating ascending giant interneurons; a pathway involved in predator avoidance. Crickets usually sing continuously over several hours while external wind stimulation of their cerci reliably elicits either transient silencing or escape reactions. But how does the cricket nervous system manage to discriminate between the self-generated and external wind stimulation?
To investigate if a corollary discharge from the singing motor network also controls the activity in the wind-sensitive cercal escape pathway, we intracellularly recorded wind-sensing sensory afferents and interneurons in the terminal ganglion of fictively singing crickets. Singing was elicited by microinjection of Eserine into the brain. After severing all mesothoracic wing nerves the fictive singing motor pattern was monitored by extracellular motoneuron recording. Intracellular recordings from the terminal branches of wind-sensitive afferents in more than 20 singing crickets revealed that, in contrast to the auditory pathway, there are no primary afferent depolarizations in phase with the singing rhythm that would indicate a presynaptic inhibition at the first synapse of the wind-sensitive pathway. Intracellular recordings from the dendrites of the wind-sensitive ventral giant interneurons 8-1a and 8-1b, however, revealed rhythmic postsynaptic inhibition (IPSPs) occurring strictly in phase with the syllable rhythm of the singing pattern. In the fictively singing crickets, where no self-generated wind occurs, the corollary discharge inhibition in the giant interneurons was sufficient to suppress the spike responses towards external wind stimulation, when the stimulation coincided with the singing motor activity. Reduced responsiveness of the wind-sensitive giant interneurons by postsynaptic corollary discharge inhibition is a suitable mechanism to prevent inadvertent triggering of escape reactions by self-generated wind stimulation during singing while maintaining the sensitivity of the cercal predator avoidance pathway in the singing intervals. (This study was supported by the BBSRC and The Isaac Newton Trust)
Keywords:
corollary discharge,
cricket,
stridulation,
wind-sensitive interneurons
Conference:
Tenth International Congress of Neuroethology, College Park. Maryland USA, United States, 5 Aug - 10 Aug, 2012.
Presentation Type:
Poster (but consider for student poster award)
Topic:
Sensorimotor Integration
Citation:
Schöneich
S and
Hedwig
B
(2012). Corollary discharge modulation of wind-sensitive interneurons in the singing cricket.
Conference Abstract:
Tenth International Congress of Neuroethology.
doi: 10.3389/conf.fnbeh.2012.27.00074
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Received:
19 Mar 2012;
Published Online:
07 Jul 2012.
*
Correspondence:
Dr. Stefan Schöneich, University of Cambridge, Department of Zoology, Cambridge, CB2 33EJ, United Kingdom, stefan.schoeneich@uni-jena.de