Advertisement

Brain Structure and Function

, Volume 218, Issue 1, pp 295–301 | Cite as

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

  • Anett RiedelEmail author
  • Franziska Stöber
  • Karin Richter
  • Klaus-Dieter Fischer
  • Riitta Miettinen
  • Eike Budinger
Short Communication

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.

Keywords

Basal forebrain Gray type I synapse Gray type II synapse Excitation Inhibition Gamma-aminobutyric acid 

Notes

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.

References

  1. Alonso JR, Frotscher M (1989) Organization of the septal region in the rat brain: a Golgi/EM study of lateral septal neurons. J Comp Neurol 286:472–287Google Scholar
  2. Amilhon B, Lepicard E, Renoir T, Mongeau R, Popa D, Poirel O, Miot S, Gras C, Gardier AM, Gallego J, Hamon M, Lanfumey L, Gasnier B, Giros B, El Mestikawy S (2010) VGLUT3 (vesicular glutamate transporter type 3) contribution to the regulation of serotonergic transmission and anxiety. J Neurosci 30:2198–2210PubMedCrossRefGoogle Scholar
  3. Aznar S, Qian ZX, Knudsen GM (2004) Non-serotonergic dorsal and median raphe projection onto parvalbumin- and calbindin-containing neurons in hippocampus and septum. Neuroscience 124:573–581PubMedCrossRefGoogle Scholar
  4. Bellone C, Lüscher C, Mameli M (2008) Mechanisms of synaptic depression triggered by metabotropic glutamate receptors. Cell Mol Life Sci 65:2913–2923PubMedCrossRefGoogle Scholar
  5. Cools, Roberts AC, Robbins TW (2008) Serotoninergic regulation of emotional and behavioural control processes. Trends Cogn Sci 12:31–40Google Scholar
  6. Dinopoulos A, Dori I, Parnavelas JG (1993) Serotonergic innervation of the mature and developing lateral septum of the rat: a light and electron microscopic immunocytochemical analysis. Neuroscience 55:209–222PubMedCrossRefGoogle Scholar
  7. El Mestikawy S, Wallén-Mackenzie A, Fortin GM, Descarries L, Trudeau LE (2011) From glutamate co-release to vesicular synergy: vesicular glutamate transporters. Nat Rev Neurosci 12:204–216PubMedCrossRefGoogle Scholar
  8. Fremeau RT Jr, Burman J, Qureshi T, Tran CH, Proctor J, Johnson J, Zhang H, Sulzer D, Copenhagen DR, Storm-Mathisen J, Reimer RJ, Chaudhry FA, Edwards RH (2002) The identification of vesicular glutamate transporter 3 suggests novel modes of signaling by glutamate. Proc Natl Acad Sci USA 99:14488–14493Google Scholar
  9. Fremeau RT Jr, Voglmaier S, Seal RP, Edwards RH (2004) VGLUTs define subsets of excitatory neurons and suggest novel roles for glutamate. Trends Neurosci 27:98–103PubMedCrossRefGoogle Scholar
  10. Fujiyama F, Furuta T, Kaneko T (2001) Immunocytochemical localization of candidates for vesicular glutamate transporters in the rat cerebral cortex. J Comp Neurol 435:379–387PubMedCrossRefGoogle Scholar
  11. Gabellec MM, Panzanelli P, Sassoe-Pognetto M, Lledo MP (2007) Synapse-specific localization of vesicular glutamate transporters in the rat olfactory bulb. Eur J Neurosci 25:1373–1383PubMedCrossRefGoogle Scholar
  12. Gallagher JP, Zheng F, Hasuo H, Shinnick-Gallagher P (1995) Activities of neurons within the rat dorsolateral septal nucleus (DLSN). Prog Neurobiol 45:373–395PubMedCrossRefGoogle Scholar
  13. Gras C, Herzog E, Bellenchi GC, Bernard V, Ravassard P, Pohl M, Gasnier B, Giros B, El Mestikawy S (2002) A third vesicular glutamate transporter expressed by cholinergic and serotonergic neurons. J Neurosci 22:5442–5451PubMedGoogle Scholar
  14. Herzog E, Bellenchi GC, Gras C, Bernard V, Ravassard P, Bedet C, Gasnier B, Giros B, El Mestikawy S (2001) The existence of a second vesicular glutamate transporter specifies subpopulations of glutamatergic neurons. J Neurosci 21:RC181Google Scholar
  15. Herzog E, Gilchrist J, Gras C, Muzerelle A, Ravassard P, Giros B, Gaspar P, El Mestikawy S (2004) Localization of VGLUT3, the vesicular glutamate transporter type 3, in the rat brain. Neuroscience 123:983–1002PubMedCrossRefGoogle Scholar
  16. Hioki H, Fujiyama F, Nakamura K, Wu SX, Matsuda W, Kaneko T (2004) Chemically specific circuit composed of vesicular glutamate transporter 3- and preprotachykinin B producing interneurons in the rat neocortex. Cereb Cortex 14:1266–1275PubMedCrossRefGoogle Scholar
  17. Hioki H, Nakamura H, Ma YF, Konno M, Hayakawa T, Nakamura KC, Fujiyama F, Kaneko T (2010) Vesicular glutamate transporter 3-expressing nonserotonergic projection neurons constitute a subregion in the rat midbrain raphe nuclei. J Comp Neurol 518:668–686PubMedCrossRefGoogle Scholar
  18. Jakab RL, Leranth C (1995) Septum. In: Paxinos G (ed) The rat nervous system, 2nd edn. Academic Press, New York, pp 405–442Google Scholar
  19. Kaneko T, Fujiyama F, Hioki H (2002) Immunohistochemical localization of candidates for vesicular glutamate transporters in the rat brain. J Comp Neurol 444(1):39–62Google Scholar
  20. Klemann CJ, Roubos EW (2011) The gray area between synapse structure and function-Gray’s synapse types I and II revisited. Synapse 65:1222–1230PubMedCrossRefGoogle Scholar
  21. Martin-Ibanez R, Jenstad M, Berghuis P, Edwards RH, Hioki H, Kaneko T, Mulder J, Canals JM, Ernfors P, Chaudhry FA, Harkany T (2006) Vesicular glutamate transporter 3 (VGLUT3) identifies spatially segregated excitatory terminals in the rat substantia nigra. Eur J Neurosci 23:1063–1070PubMedCrossRefGoogle Scholar
  22. Paxinos G, Watson W (1998) The rat brain in stereotaxic coordinates, 4th edn. Academic Press, New YorkGoogle Scholar
  23. Peters A, Palay SL, Webster H (1991) The fine structure of the nervous system, 3rd edn. University Press, OxfordGoogle Scholar
  24. Riedel A, Westerholz S, Braun K, Edwards RH, Arendt T, Härtig W (2008) Vesicular glutamate transporter 3-immunoreactive pericellular baskets ensheath a distinct population of neurons in the lateral septum. J Chem Neuroanat 36:177–190PubMedCrossRefGoogle Scholar
  25. Risold PY, Swanson LW (1997a) Chemoarchitecture of the rat lateral septal nucleus. Brain Res Brain Res Rev 24:91–113PubMedCrossRefGoogle Scholar
  26. Risold PY, Swanson LW (1997b) Connections of the rat lateral septal complex. Brain Res Brain Res Rev 24:115–195PubMedCrossRefGoogle Scholar
  27. Schultz W (2007) Behavioral dopamine signals. Trends Neurosci 30:203–210PubMedCrossRefGoogle Scholar
  28. Sheehan TP, Chambers RA, Russell DS (2004) Regulation of affect by the lateral septum: implications for neuropsychiatry. Brain Res Brain Res Rev 46:71–117PubMedCrossRefGoogle Scholar
  29. Shigemoto R, Nakanishi S, Mizuno N (1992) Distribution of the mRNA for a metabotropic glutamate receptor (mGluR1) in the central nervous system: an in situ hybridization study in adult and developing rat. J Comp Neurol 322:121–135PubMedCrossRefGoogle Scholar
  30. Shigemoto R, Nomura S, Ohishi H, Sugihara H, Nakanishi S, Mizuno N (1993) Immunohistochemical localization of a metabotropic glutamate receptor, mGluR5, in the rat brain. Neurosci Lett 163:53–57PubMedCrossRefGoogle Scholar
  31. Stornetta RL, Rosin DL, Simmons JR, Mc Quiston TJ, Vujovic N, Weston MC, Guyenet PG (2005) Coexpression of vesicular glutamate transporter-3 and γ-aminobutyric acidergic markers in rat rostral medullary raphe and intermediolateral cell column. J Comp Neurol 49:477–494CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Anett Riedel
    • 1
    • 2
    Email author
  • Franziska Stöber
    • 2
  • Karin Richter
    • 3
  • Klaus-Dieter Fischer
    • 3
  • Riitta Miettinen
    • 4
    • 5
  • Eike Budinger
    • 2
  1. 1.Department of Zoology/Developmental NeurobiologyOtto von Guericke University MagdeburgMagdeburgGermany
  2. 2.Department Auditory Learning and SpeechLeibniz Institute for NeurobiologyMagdeburgGermany
  3. 3.Institute of Biochemistry and Cell BiologyOtto von Guericke University MagdeburgMagdeburgGermany
  4. 4.Department of Neurology, Institute of Clinical MedicineUniversity of Eastern FinlandKuopioFinland
  5. 5.Department of Obstetrics, Gynecology, and Reproductive SciencesYale University School of MedicineNew HavenUSA

Personalised recommendations