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Phonotaxis in Crickets: From Auditory Processing to Motor Control

Berthold Hedwig

Department of Zoology, Cambridge, UK

The acoustic behaviour of crickets has captured the attention of scientists for more than a century. Females are attracted by the species-specific calling songs of the singing males and walk or fly towards them. This phonotactic behaviour of the females poses (at least) two central questions for neurobiologists interested in the neural basis of animal behaviour:

1. How do the animals recognise the species-specific song patterns?

2. How do they localize and steer towards the sound source?

We analysed the phonotactic behaviour of female crickets (G. bimaculatus) and underlying neural processing with a sensitive trackball system, high-speed video recordings, calcium imaging and intracellular recordings of auditory processing in key neurons.

Tethered females walk under open loop conditions on a sensitive trackball system while they remain stationary within the sound field. Under these conditions binaural intensity differences of 1-2 dB are sufficient to elicit reliable steering and the animals respond to changes in the speaker position of just 2 degree. Left-right auditory information processing can be demonstrated by imaging calcium levels in central auditory neurons, coupled by reciprocal inhibition.

When the animals are challenged with split song paradigms, presenting the pulses of the calling song from the left and right side in alternation, they rapidly steer towards individual sound pulses. Auditory steering is based on turning the prothorax and on front leg movements, with the tibia being extended into the direction of the acoustic stimulation. The tibial motoneurons involved do not receive any direct auditory inputs and rather seem to be activated by commands from descending brain neurons. During phonotaxis these commands are rapidly integrated into the walking motor pattern.

Once phonotaxis is activated females also do respond to artificial test pulses inserted into the calling song. The effect gradually starts at the beginning and wanes off at the end of phonotaxis. It indicates that pattern recognition modulates the gain of the auditory steering response.

The neural networks underlying pattern recognition are located in the brain. Intracellular recordings of brain neurons in walking crickets identified descending interneurons, which elicit walking and which may be involved in the control of phonotactic behaviour. Local interneurons tuned to the species-specific song pattern appear to forward auditory information from the ascending interneurons towards the descending premotor pathways. Thus a picture of auditory processing in the brain is gradually emerging.

Supported by the BBSRC and the Royal Society.