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

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.

[1]  D W Tank,et al.  Coherent network oscillations by olfactory interneurons: modulation by endogenous amines. , 1993, Journal of neurophysiology.

[2]  G. Laurent,et al.  Encoding of Olfactory Information with Oscillating Neural Assemblies , 1994, Science.

[3]  D. Kleinfeld,et al.  Dynamics of propagating waves in the olfactory network of a terrestrial mollusk: an electrical and optical study. , 1994, Journal of neurophysiology.

[4]  D. Tank,et al.  Odour-modulated collective network oscillations of olfactory interneurons in a terrestrial mollusc , 1990, Nature.

[5]  J S Kauer,et al.  Salamander olfactory bulb neuronal activity observed by video rate, voltage-sensitive dye imaging. III. Spatial and temporal properties of responses evoked by odorant stimulation. , 1995, Journal of neurophysiology.

[6]  Y Kirino,et al.  Behavioral modulation induced by food odor aversive conditioning and its influence on the olfactory responses of an oscillatory brain network in the slug Limax marginatus. , 1998, Learning & memory.

[7]  W. Singer,et al.  Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties , 1989, Nature.

[8]  T. Sekiguchi,et al.  Mapping of interneurons that contribute to food aversive conditioning in the slug brain. , 1998, Learning & memory.

[9]  D. Kleinfeld,et al.  Central and reflex neuronal responses elicited by odor in a terrestrial mollusk. , 1996, Journal of neurophysiology.

[10]  G. Laurent,et al.  Temporal Representations of Odors in an Olfactory Network , 1996, The Journal of Neuroscience.

[11]  G. Laurent,et al.  Odour encoding by temporal sequences of firing in oscillating neural assemblies , 1996, Nature.

[12]  G. Laurent,et al.  Odorant-induced oscillations in the mushroom bodies of the locust , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.