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VGLUT3-immunoreactive afferents of the lateral septum: ultrastructural evidence for a modulatory role of glutamate

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Abstract

Through its extensive connections with various brain regions, the lateral septum (LS) participates in the processing of cognitive, emotional and autonomic information. It is decisively involved in the generation of behavioral responses according to environmental demands. Modulatory afferents reaching the LS from the brain stem (e.g. dopaminergic, serotonergic) play a role in the adjustment of these behavioral responses. Recently, a population of vesicular glutamate transporter 3-immunoreactive (VGLUT3-ir) fibers forming prominent pericellular basket-like structures (PBLS) was described in the rat LS. These VGLUT3-ir PBLS are distributed in a layer-like pattern, which is very typical for modulatory afferents of the LS. There is meanwhile broad evidence that glutamate can act as a modulatory or co-transmitter and that those neurons, which make use of this transmission mode, primarily express VGLUT3. Thus, the VGLUT3-ir fibers within the LS could also display features typical for non-canonical glutamatergic transmission. Employing pre-embedding electron microscopy for VGLUT3 in rats, we show now that the VGLUT3-ir fibers outlining LS neurons represent axonal terminals, which primarily form symmetric synapses with somata and proximal dendrites of their target neurons. Occasionally, we also found VGLUT3-ir terminals that make canonical asymmetric synapses on distal dendrites and spines. Thus, VGLUT3-ir boutons in the LS form two different, disproportionate, populations of synaptic contacts with their target neurons. The larger one of them is indicative of employing glutamate as a modulatory transmitter.

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Acknowledgments

The study was supported by the German Academic Exchange Service (DAAD, project 313-PPP-SF.09-lk, AR), Paulo Foundation and Jalmari and Rauha Aaltonen Foundation, Finland (RM) and by the German Science Foundation (SFB-TRR 31 and SFB 779, EB). The authors thank Mmes. Anja Gürke, Karla Klingenberg and Virpi Miettinen for their excellent technical assistance.

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Department of Zoology/Developmental Neurobiology, Otto von Guericke University Magdeburg, Leipziger Str. 44, 39120, Magdeburg, Germany

    Anett Riedel

  2. Department Auditory Learning and Speech, Leibniz Institute for Neurobiology, Brenneckestr. 6, 39118, Magdeburg, Germany

    Anett Riedel, Franziska Stöber & Eike Budinger

  3. Institute of Biochemistry and Cell Biology, Otto von Guericke University Magdeburg, Leipziger Str. 44, 39120, Magdeburg, Germany

    Karin Richter & Klaus-Dieter Fischer

  4. Department of Neurology, Institute of Clinical Medicine, University of Eastern Finland, Yliopistonranta 1C, 70211, Kuopio, Finland

    Riitta Miettinen

  5. Department of Obstetrics, Gynecology, and Reproductive Sciences, Yale University School of Medicine, 333 Cedar Street, New Haven, CT, 06520, USA

    Riitta Miettinen

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  1. Anett Riedel
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  2. Franziska Stöber
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  3. Karin Richter
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  4. Klaus-Dieter Fischer
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  5. Riitta Miettinen
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  6. Eike Budinger
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Corresponding author

Correspondence to Anett Riedel.

Additional information

R. Miettinen and E. Budinger contributed equally to this work.

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Riedel, A., Stöber, F., Richter, K. et al. VGLUT3-immunoreactive afferents of the lateral septum: ultrastructural evidence for a modulatory role of glutamate. Brain Struct Funct 218, 295–301 (2013). https://doi.org/10.1007/s00429-012-0395-4

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  • DOI: https://doi.org/10.1007/s00429-012-0395-4

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