Spatiotemporal Neural Activity Changes in the Molluscan Olfactory Center Specifically Induced by Innately Aversive and <i>In Vitro</i> Aversively Conditioned Odors
- 1 Department of Correlative Study in Physics and Chemistry, Graduate School of Integrated Basic Sciences, Nihon University, Tokyo, Japan
- 2 Department of Correlative Study in Physics and Chemistry, Graduate School of Integrated Basic Sciences, Nihon University, Tokyo, Japan
- 3 Department of Physics, College of Science and Technology, Nihon University, Tokyo, Japan
- 4 Department of Physics, College of Science and Technology, Nihon University, Tokyo, Japan
- 5 Department of Ultrastructural Research, National Institute of Neuroscience, National Center of Neurology and Psychiatry, Tokyo, Japan
- 6 Department of Correlative Study in Physics and Chemistry, Graduate School of Integrated Basic Sciences, Nihon University, Tokyo, Japan
Abstract
In the procerebrum (PC), the olfactory center, of the land slug Limax, an oscillation of local field potential (LFP) with 0.5 - 1 Hz is observed by electrophysiological extracellular recording. The oscillation has a phase delay along the distal-proximal axis, resulting in the propagation of waves from the distal to proximal region. One important advantage of nervous systems of mollusks such as Limax is that their nervous systems in vitro retain several types of computational properties found in vivo (e.g. learning and memory). A previous study showed that the LFP frequency in the PC of Limax increased specifically in response to innately aversive and in vitro aversively conditioned odors. In the present study, we examined spatiotemporal neural activity changes induced in the PC by those odors using the fluorescent voltage imaging technique. The results showed that innately aversive (onion and hexanol) and in vitro aversively conditioned (carrot, which is innately attractive) odors specifically induced an increase in propagation speed of the neural activity in the PC, while innately attractive odors did not induce it. The results also suggested that the avoidance behavior by those odors might be induced by the increase of propagation speed and the following increases in the discharges of the partial nerve that transmits the motor output.
- Kimura, T., Suzuki, H., Kono, E. and Sekiguchi, T. (1998) Mapping of Interneurons That Contribute to Food Aversive Conditioning in the Slug Brain. Learning & Memory, 4, 376-388. https://doi.org/10.1101/lm.4.5.376
- Teyke, T. and Gelperin, A. (1999) Olfactory Oscillation Augment Odor Discrimination Not Odor Identification by Limax CNS. NeuroReport, 10, 1061-1068. https://doi.org/10.1097/00001756-199904060-00030
- Gelperin A. and Tank, D.W. (1990) Odour-Modulated Collective Network Oscillations of Olfactory Interneurons in a Terrestrial Mollusk. Nature, 345, 437-440. https://doi.org/10.1038/345437a0
- Kleinfeld, D., Delaney, K.R., Fee, M.S., Flores, J.A., Tank, D.W. and Gelperin, A. (1994) Dynamics of Propagating Waves in the Olfactory Network of a Terrestrial Mollusk: An Electrical and Optical Study. Journal of Neurophysiology, 72, 1402-1419. https://doi.org/10.1152/jn.1994.72.3.1402
- Watanabe, S., Kawahara, S. and Kirino, Y. (1998) Morphological Characterization of the Bursting and Nonbursting Neurons in the Olfactory Centre of the Terrestrial Slug Limax marginatus. Journal of Experimental Biology, 201, 925-930.
- Watanabe, S. and Kirino, Y. (2007) Selective Calcium Imaging of Olfactory Interneurons in a Land Mollusk. Neuroscience Letters, 417, 246-249. https://doi.org/10.1016/j.neulet.2007.02.083
- Delaney, K.R., Gelperin, A., Fee, M.S., Flores, A., Gervais, R., Tank, D.W. and Kleinfeld, D. (1994) Waves and Stimulus-Modulated Dynamics in an Oscillating Olfactory Network. Proceedings of National Academy of Sciences of USA, 91, 669-673. https://doi.org/10.1073/pnas.91.2.669
- Inoue, S., Kawahara, S., Toda, S., Watanabe, S. and Kirino, Y. (1998) Selective Optical Recording of the Neural Activity in the Olfactory Center of the Land Slug Using a Calcium Indicator Dye. Bioimages, 6, 59-67.
- Hamasaki, Y., Hosoi, M., Nakada, S., Shimokawa T. and Saito, M. (2013) Fluorescent Voltage Imaging Technique for the Measurement of Molluscan Neural Activities. Open Journal of Biophysics, 3, 54-58. https://doi.org/10.4236/ojbiphy.2013.31A007
- Watanabe, S., Takanashi, F., Ishida, K., Kobayashi, S., Kitamura, Y., Hamasaki, Y. and Saito, M. (2015) Nitric Oxide-Mediated Modulation of Central Network Dynamics during Olfactory Perception. PLoS One, 10, e0136846. https://doi.org/10.1371/journal.pone.0136846
- Lukowiak, K. and Sahley, C. (1981) The In Vitro Classical Conditioning of a Gill Withdrawal Reflex in Aplysia: Neural Correlates and Possible Neural Mechanism. Science, 212, 1516-1518. https://doi.org/10.1126/science.212.4502.1516