Central projections of auditory receptor neurons of crickets

Abstract

We describe the central projections of physiologically characterized auditory receptor neurons of crickets as revealed by confocal microscopy. Receptors tuned to ultrasonic frequencies (similar to those produced by echolocating, insectivorous bats), to a mid-range of frequencies, and a subset of those tuned to low, cricket-like frequencies have similar projections, terminating medially within the auditory neuropile. Quantitative analysis shows that despite the general similarity of these projections they are tonotopic, with receptors tuned to lower frequencies terminating more medially. Another subset of cricket-song-tuned receptors projects more laterally and posteriorly than the other types. Double-fills of receptors and identified interneurons show that the three medially projecting receptor types are anatomically well positioned to provide monosynaptic input to interneurons that relay auditory information to the brain and to interneurons that modify this ascending information. The more laterally and posteriorly branching receptor type may not interact directly with this ascending pathway, but is well positioned to provide direct input to an interneuron that carries auditory information to more posterior ganglia. These results suggest that information about cricket song is segregated into functionally different pathways as early as the level of receptor neurons. Ultrasound-tuned and mid-frequency tuned receptors have approximately twice as many varicosities, which are sites of transmitter release, per receptor as either anatomical type of cricket-song-tuned receptor. This may compensate in part for the numerical under-representation of these receptor types.

Acoustic feature recognition in the dogbane tiger moth,Cycnia tenera

“…While moths may be tone-deaf, the Pacific field cricket, Teleogryllus oceanicus, categorically perceives sound frequencies representing diametrically opposed signals (mating versus bat sounds) (Wyttenbach et al, 1996) and could use spectral cues to identify an attacking bat. Crickets discriminate frequencies by using a range-fractionated auditory receptor array (Imaizumi and Pollack, 2005) that reserves approximately 25% of its cells for the ultrasonic calls of bats. The frequency non-fractionating, two-celled receptor organ of the noctuoid moth ear appears to preclude a similar ability for these insects.…”

Neurite‐specific Ca2+ dynamics underlying sound processing in an auditory interneurone

“…In other, closely related species, their axonal terminals project in a tonotopic fashion in the prothoracic auditory neuropile (Römer, 2003;Oldfield et al, 1986;Römer et al, 1988). In crickets, high frequency coding afferents terminate both medially and laterally, while lower frequency afferents project medially (Imaizumi and Pollack, 2005). The G. bimaculatus ON1 encodes a wider frequency range than individual afferents (Schildberger, 1988; personal observations), and extends its dendrite along the same projection area as the tonotopicity map of afferent terminals.…”

“…Its dendrites extend along the axonal projections of the auditory afferents in the auditory neuropile (Esch and Huber, 1980;Wohlers and Huber, 1982;Imaizumi and Pollack, 2005). We therefore tested for a tonotopic arrangement of auditory inputs along the dendritic branches (D1 and D2).…”

“…During sound processing, ON1 integrates ipsilateral excitatory inputs from auditory afferents (Imaizumi and Pollack, 2005) and inhibitory inputs from its contralateral counterpart. Presentation of a contralateral stimulus during ongoing ipsilateral stimulation demonstrated this integration not only in membrane potential but also in the Ca 2þ signals [ Fig.…”

“…ON1 receives inputs from ipsilateral auditory afferents originating from the ears in the front legs (Imaizumi and Pollack, 2005) and in turn forms inhibitory connections to its contralateral counterpart (Selverston et al, 1985) and the contralateral ascending auditory interneurones AN1 (Horseman and Huber, 1994;Faulkes and Pollack, 2000) and AN2 (Selverston et al, 1985), which transmit auditory information to the brain (Wohlers and Huber, 1982). The recurrent inhibitory network formed by the two ON1 has been implicated in enhancing bilateral auditory contrast supporting auditory orientation and temporal pattern processing (Wiese and Eilts, 1985;Nabatiyan et al, 2003).…”