Keeping track of the sensory signals generated by the world around us is challenging enough without having to disentangle the nerve signals generated by our own movements. But this is exactly what we would have to do if the neurons that control our every move didn't send simultaneous signals to our sensory systems, telling them to disregard confounding information generated by our own bodies. In addition, these so-called ‘corollary discharges’ may also contribute to other aspects of behaviour, such as providing stabilisation when senses may be overwhelmed by other inputs. However, unscrambling the impact of corollary signals on movements in the intricate nervous systems of multi-limbed animals is too complex, so Hans Straka and Boris Chagnaud from the Ludwig-Maximilians-University Munich, Germany, decided to focus on a much simpler animal: African clawed frog tadpoles. The nerve signals that control the tail beats of tadpoles and their associated corollary discharges are much simpler to interpret. Reasoning that a pair of touch-sensitive tentacles on the jaws of the tadpoles could be over-stimulated as the tiny swimmers wriggle through the water, Chagnaud, Straka, Sara Hänzi and Roberto Banchi began to investigate how corollary signals from spinal locomotor centres that control swimming might protect the tentacles from sensory overload.
Recording electrical signals from the nerves that indicated when the tadpole was swimming, the team saw that when the corollary signals were generated, the touch-sensitive tentacles swung back; and as soon as the animal stopped swimming, the tentacles moved forward again. Next, the team identified which nerve controlled the tentacles’ movements by painstakingly disconnecting different portions of the muscle that pulled the tentacle back, until they confirmed that the mandibular branch of the trigeminal nerve, which controls the tadpole’s jaw movements, controlled the swinging movement. Then, the team tested how many of the motoneurons in the trigeminal nerve triggered the tentacles’ movements by measuring changes in calcium ion concentration in the cell bodies of trigeminal motoneurons as the tadpole swam, and they found that the calcium signals harmonised with the animal’s swimming activity. Finally, the team compared the pattern of nerve signals generated in the spinal cord of the swimming tadpole with the nerve signals in the tentacle and found that the nerve discharge in the spinal ventral roots associated with swimming closely matched the discharge in the section of the trigeminal nerve that innervated the tentacle. And when the tadpoles swam hard, increasing the ventral root discharge, the tentacles retracted even further. ‘This corollary discharge encodes duration and strength of locomotor activity, thereby ensuring a reliable coupling between locomotion and tentacle motion’, the team says.
Having provided convincing evidence that corollary discharges from the spinal cord of swimming tadpoles control the movements of touch-sensitive tentacles either side of the tadpole’s mouth in coordination with swimming, the team is more confident that the tadpoles retract the tentacles to avoid over stimulation while swimming through sticky water. In addition, they suggest that folding the tentacles back could make the animals more streamlined to speed them on their way. Either way, the team has unravelled the mechanism uniting the tadpole's swimming wriggle with its swinging touch-sensitive tentacles.