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We studied the oscillatory properties and the olfactory responses of the procerebral (PC) lobe of the cerebral ganglion in the terrestrial mollusc Limax marginatus. The PC lobe, a central olfactory organ in Limax, is a highly interconnected network of local interneurons that receives olfactory inputs from the inferior and superior tentacular noses. We used an optical recording technique with a voltage-sensitive dye to record the activity of the PC lobe from either the posterior or the dorsal surface. The recordings revealed that almost all PC interneurons showed spontaneous oscillatory activities that had been entrained with each other. Upon presentation to the nose of odors to which the slugs had been aversively conditioned, the basal level of the oscillation changed biphasically. In the early phase of the response, depolarization in the basal level of the oscillation occurred in one or more belt-shaped regions parallel to the dorsoventral axis. In the late phase of the response, hyperpolarization of basal potential level of the PC lobe oscillations occurred in a wider area. Such spatial and temporal modulation was not observed when the unpaired control odors were presented to the preparation, whereas the same preparations responded to the aversively conditioned stimuli. Thus, it was considered that the spatial and temporal response in the basal level of oscillation was specific to the aversively conditioned odors. Furthermore, the spatial pattern of the depolarization modulation in the early phase was repeatable in multiple trials performed using the same odor, although different odors produced different spatial patterns of the modulation. From these results, we conclude that in the PC lobe learned odors are represented as spatial and temporal activity patterns of oscillators that constitute a coherent network.

Optical recording analysis of olfactory response of the procerebral lobe in the slug brain.