Gating of sensory responses of descending brain neurones during walking in crickets

Single descending brain neurones were recorded and stained intracellularly in the neck connectives of crickets while they walked upon a styrofoam ball under open-loop conditions. The animal's translational and rotational velocities were measured simultaneously, and various stimuli were used to investigate the neuronal response characteristics. Stimulation with a moving grating or an artificial calling song of 5 kHz induced optomotor behaviour and positive phonotaxis. An acoustic stimulus of 20 kHz elicited negative phonotaxis. We report the first clear evidence for behaviourally dependent gating of sensory responses of identified descending brain neurones. Most descending cells only responded to visual stimuli or to an artificial calling song of 5 kHz while the animal was walking, indicating that the responses to these stimuli were gated by the walking activity of the animal. In contrast to this, responses to stimuli that elicit negative phonotaxis, such as acoustic stimuli of 20 kHz, were not gated. This indicates that the gating of sensory responses in these cells depends on the behavioural context of the stimulus. From these findings, we conclude that significant information about the properties of sensory processing in higher-order neurones can only be gained from tests in behaviourally relevant paradigms. Important characteristics might otherwise be missed, thus leading to misinterpretations regarding their function.