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Organization of the procerebrum in terrestrial pulmonates (Helix, Limax) reconsidered: cell mass layer synaptology and its serotonergic input system

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Abstract

The synaptology of the cell body layer of the olfactory center, procerebrum, was investigated in two prominent terrestrial pulmonate gastropod species, Helix pomatia and Limax valentianus. In addition, the analysis of the 5-HT-immunoreactive innervation, including ultrastructural level, was performed at high resolution in H. pomatia. A highly complex system of synaptic and non-synaptic connections was found in the procerebrum of both species connected to local neuropil areas of different size. The procerebral (globuli) cell perikarya were richly innervated by varicosities meanwhile the axon profiles also established contacts with each other. Synaptic configurations including convergence, divergence and presynaptic modulation were also revealed. The frequent occurrence of unspecialized but close axo-somatic and axo-axonic membrane contacts referring to the modulatory forms of transmitter release were also accompanied by membrane configurations indicative of active exocytosis. In H. pomatia, the cell mass layer was shown to receive a rich 5-HT-immunoreactive innervation, forming a dense network around the cell bodies. At ultrastructural level, 5-HT-immunoreactive varicosities contacted both cell bodies and different unlabeled axon profiles. Our results suggest that the local neuropil regions in the cell body layer are site of local circuits, which may play a decisive role in olfactory integrative processes bound to the procerebrum. The pattern and form of the 5-HT-immunoreactive innervation of extrinsic origin suggest an overall modulatory role in the cell body layer. The results may serve a basis for considering the role of local intercellular events, connected to microcircuits, within the procerebrum cell body layer involved in oscillation activities.

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Acknowledgments

Authors’ thanks are due to the skillful technical assistance of Ms. Zsuzsanna N. Fekete and Mr. Boldizsár Balázs. We are grateful to Dr. Anna Kiss, Dr. József Kiss (both at the Semmelweis University Medical School, Budapest), and Professor László Seress (University of Pécs Medical School, Pécs) providing the possibility to use the Hitachi H-7650 and the JEOL 1200 EXII electron microscopes, respectively. This work was supported by a Grant from the Hungarian Scientific Research Fund (OTKA, No. 78224 to K.E.), and Grants-in-Aid for KAKENHI from the Japan Society for the Promotion of Science (No. 21657022 to E.I., and No. 23570099 to S.K.).

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Authors and Affiliations

  1. Department of Experimental Zoology, Balaton Limnological Institute, Centre for Ecological Research, Hungarian Academy of Sciences, Tihany, Hungary

    Károly Elekes & Izabella Battonyai

  2. Laboratory of Functional Biology, Kagawa School of Pharmaceutical Sciences, Tokushima Bunri University, Sanuki, Japan

    Suguru Kobayashi & Etsuro Ito

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  1. Károly Elekes
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  2. Izabella Battonyai
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  3. Suguru Kobayashi
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  4. Etsuro Ito
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Correspondence to Károly Elekes.

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Elekes, K., Battonyai, I., Kobayashi, S. et al. Organization of the procerebrum in terrestrial pulmonates (Helix, Limax) reconsidered: cell mass layer synaptology and its serotonergic input system. Brain Struct Funct 218, 477–490 (2013). https://doi.org/10.1007/s00429-012-0409-2

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