Fine tuning of olfactory orientation behaviour by the interaction of oscillatory and single neuronal activity

We used a simple sensory and motor system to investigate the neuronal mechanisms of olfactory orientation behaviour. The main olfactory organs of terrestrial molluscs, the experimental animals used in this work, are located on the tips of their tentacles, which display complex movements when they explore a new environment. By reconstructing the trajectory of the tentacle tip ('nose') movements in three dimensions in freely moving snails, we showed that the protracted tentacles performed continuous scanning, both spontaneously and in response to odours. Odour applications elicited a brief startle-like quiver of the tentacle in a concentration-independent manner as well as a concentration-dependent contraction. Previous work showed that activation of an identified cerebral motoneuron, MtC3, produces tentacle contraction. Here we showed that in semi-intact preparations, MtC3 responded to odours in a concentration-dependent manner, similar to the tentacle contraction response to the same odours in intact animals. This observation suggests that MtC3 is involved in the central control of the scanning area by regulating the tentacle length. Using voltage-sensitive dyes and imaging, we demonstrated that during the hyperpolarizing phases of oscillations in the procerebral lobe, the main olfactory centre of the CNS of terrestrial molluscs, MtC3 spike frequency significantly decreased. We also showed that direct activation of the procerebral lobe resulted in the phasic inhibition of MtC3. This is therefore an example of an olfactory system in which the interaction of oscillatory and single neuronal activity plays an important role in the fine tuning of orientation behaviour to suit the particular odour environment.