Neuronal Organization of a Fast-Mediating Cephalothoracic Pathway for Antennal-Tactile Information in the Cricket (Gryllus bimaculatus DeGeer)

Crickets use their long antennae as tactile sensors. Confronted with obstacles, conspecifics, or predators, antennal contacts trigger short-latency motor responses. To reveal the neuronal pathway underlying these antennal-guided locomotory reactions we identified descending interneurons that rapidly transmit antennal-tactile information from the head to the thorax in the cricket Gryllus bimaculatus. Antennae were stimulated with forces approximating those of naturally occurring antennal contacts. Responding interneurons were individually identified by intracellular axon recordings in the pro-mesothoracic connective and subsequent tracer injection. Simultaneous with the intracellular recordings, the overall spike response in the neck connectives was recorded extracellularly to reveal the precise response-timing of each individual neuron within the collective multiunit response. Here we describe four descending brain neurons and two with the soma in the subesophageal ganglion. All antennal-touch elicited action potentials apparent in the neck connective recordings within 10 ms after antennal-contact are generated by these six interneurons. Their dendrites ramify in primary antennal-mechanosensory neuropils of the head ganglia. Each of them consistently generated action potentials in response to antennal touching and three of them responded also to different visual stimulation (light-off, movement). Their descending axons conduct action potentials with 3-5 m/s to the thoracic ganglia where they send off side branches in dorsal neuropils. Their physiological and anatomical properties qualify them as descending giant fibers in the cricket and suggest an involvement in evoking fast locomotory reactions. They form a fast-mediating cephalo-thoracic pathway for antennal-tactile information, whereas all other antennal-tactile interneurons had response latencies exceeding 40 ms. J. Comp. Neurol. 519:1677-1690, 2011. (c) 2011 Wiley-Liss, Inc.