Optical recording of odor-evoked responses in the olfactory brain of the naïve and aversively trained terrestrial snails.

Regular spontaneous oscillations were recorded both electro- and optophysiologically using a voltage-sensitive absorption dye in the olfactory part of the brain (procerebral lobe of the cerebral ganglia) of the gastropod mollusk Helix lucorum. Odor application caused transient changes in procerebral oscillations, and an odor-evoked potential was recorded in the procerebrum (PC). The wave of evoked potential originated near the place of olfactory nerve entrance into the PC and propagated via the procerebral neuropile toward the cell body layer. The spread of the odor-evoked potential corresponded roughly to the neuropile area, whereas the spontaneous oscillations were recorded in the cell body layer of the PC and were not observed in the neuropile. Evoked potential did not produce additional events intercalated into the ongoing spontaneous oscillations. Changes in parameters of spontaneous oscillations to the repeated presentations of the same odor were variable. To estimate the role of spontaneous oscillations in odor encoding, we trained the snail to avoid cineole, using paired presentations of cineole and electric shock. Elaboration of conditioned aversion to cineole applications resulted in distinct pairing-specific changes in behavior of the snails and procerebral activity. Responses to odor (cineole) applications were not different in amplitude or frequency of spontaneous oscillations in control and trained snails, whereas ratio of amplitudes of the same oscillation wave in proximal and distal regions of the procerebrum was significantly different in control and aversively trained snails, reflecting changes in neural firing in certain areas of the olfactory lobe.

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

[2]  Kawahara,et al.  Morphological characterization of the bursting and nonbursting neurones in the olfactory centre of the terrestrial slug limax marginatus , 1998, The Journal of experimental biology.

[3]  R. Chase,et al.  Tracing neural pathways in snail olfaction: From the tip of the tentacles to the brain and beyond , 1993, Microscopy research and technique.

[4]  D. Kleinfeld,et al.  Waves and stimulus-modulated dynamics in an oscillating olfactory network. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[5]  R S Nowakowski,et al.  Postembryonic neurogenesis in the procerebrum of the terrestrial snail, Helix lucorum L. , 1998, Journal of neurobiology.

[6]  R. Sandeman,et al.  Characterization of Oscillatory Olfactory Interneurones in the Protocerebrum of the Crayfish , 1992 .

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

[8]  T Teyke,et al.  Olfactory oscillations augment odor discrimination not odor identification by Limax CNS. , 1999, Neuroreport.

[9]  A. Gelperin,et al.  Lateralized memory storage and crossed inhibition during odor processing by Limax , 2000, Journal of Comparative Physiology A.

[10]  J. Kauer,et al.  Responses of olfactory bulb neurones to odour stimulation of small nasal areas in the salamander , 1974, The Journal of physiology.

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

[12]  B Ermentrout,et al.  Minimal model of oscillations and waves in the Limax olfactory lobe with tests of the model's predictive power. , 1998, Journal of neurophysiology.

[13]  A. Gelperin,et al.  One-trial associative learning modifies food odor preferences of a terrestrial mollusc. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[14]  S Kawahara,et al.  Optical recording analysis of olfactory response of the procerebral lobe in the slug brain. , 1998, Learning & memory.

[15]  Effect of 5,7-dihydroxytryptamine on the food-aversive conditioning in the snailHelix lucorum L , 1987, Brain Research.

[16]  Stéphanie Ratté,et al.  Morphology of interneurons in the procerebrum of the snail Helix aspersa , 1997, The Journal of comparative neurology.

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

[18]  R. Chase,et al.  Responses to odors mapped in snail tentacle and brain by [14C]-2- deoxyglucose autoradiography , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  E. Niebur,et al.  Growth patterns in the developing brain detected by using continuum mechanical tensor maps , 2022 .

[20]  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.

[21]  P. Balaban.  Behavioral neurobiology of learning in terrestrial snails , 1993, Progress in Neurobiology.

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

[23]  L. Cohen.  More light on brains , 1988, Nature.

[24]  T. Teyke,et al.  Identification of stimuli and input pathways mediating food-attraction conditioning in the snail, Helix , 1998, Journal of Comparative Physiology A.

[25]  I. Zs.-Nagy,et al.  The fine structure of the procerebrum of pulmonate molluscs, Helix and Limax. , 1970, Tissue & cell.

[26]  D. Tank,et al.  Cultured olfactory interneurons from Limax maximus: optical and electrophysiological studies of transmitter-evoked responses. , 1993, Journal of neurophysiology.

[27]  Kawahara,et al.  Comparative study on neural oscillation in the procerebrum of the terrestrial slugs Incilaria bilineata and , 1997, The Journal of experimental biology.