Abstract
The granule cells (GC) of the dentate gyrus (DG) are very exciting cells, although it seems that they can also be very inhibiting cells. They contain and release the excitatory amino acid glutamate, the metal Zn++, the peptides Y, and dynorphin, brain derived neurotrophic factor (BDNF), and it has recently been well established that they also have the necessary machinery to synthesize, vesiculate and release the inhibitory amino acid GABA.6, 12 Among all these chemical messengers, glutamate is the only one with fast-acting excitatory actions. There is no doubt on the excitatory nature of the GC, but when they fire at high frequencies, peptides Y14 and dynorphin35 are released to produce inhibition and glutamate reaches an extracellular concentration that, by spilling over, activates presynaptic mGlu and kainate receptors21, 28 to inhibit further release. To complicate things further, GABA can be released from the mossy fibers (MF) under certain conditions.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
5. References
L. Acsády, A. Kamondi, A., A. Sik, T. Freund, and G. Buzsáki, GABAergic cells are the major postsynaptic targets of mossy fibers in the hippocampus, J. Neurosci. 18, 3386–3403 (1998).
B. Adams, M. Lee, M. Fahnestock, and R.J. Racine, Long-term potentiation trains induce mossy fiber sprouting, Brain Res. 775, 193–197 (1997).
L. Bergersen, A. Ruiz, J.G. Bjaalie, D.M. Kullmann, V. Gundersen, GABA and GABAA receptors at hippocampal mossy fibre synapses, Eur. J. Neurosci. 18, 931–941 (2003).
I.L. Crawford and J.D. Connor, Localization and release of glutamic acid in relation to the hippocampal mossy fibre pathway, Nature 244, 442–443 (1973).
G. Gómez-Lira, E. Trillo, M. Ramírez, M. Asai, M. Sitges, R. Gutiérrez, Expression of GABAergic transmission in the mossy fiber synapse coincides with the seizure-induced expression of GABA in mossy fiber synaptosomes, Exp. Neurol. 177, 276–283 (2002).
R. Gutierrez, Seizures induce simultaneous GABAergic and glutamatergic neurotransmission in the dentate gyrus-CA3 system, J. Neurophysiol. 84, 3088–3090 (2000).
R. Gutierrez, Activity-dependent expression of simultaneous glutamatergic and GABAergic neurotransmission from the mossy fibers in vitro, J. Neurophysiol. 87, 2562–2570 (2002).
R. Gutiérrez, The GABAergic phenotype of the “glutamatergic” granule cells of the dentate gyrus, Prog. Neurobiol. 71, 337–358 (2003).
R. Gutiérrez and U. Heinemann, Simultaneous release of glutamate and GABA might be induced in mossy fibers after kindling, Neurosci. Lett. 48, S23 (1997).
R. Gutiérrez and U. Heìnemann, Kindling induces transient fast inhibition in the dentate gyrus-CA3 projection, Eur. J. Neurosci. 13, 1371–1379 (2001).
R. Gutiérrez, H. Romo-Parra, J. Maqueda, C. Vivar, M. Ramirez, M.A. Morales and M. Lamas, Plasticity of the GABAergic phenotype of the “glutamatergic” granule cells of the rat dentate gyrus, J. Neurosci. 23, 5594–5598 (2003).
D.A. Henze, N.N. Urban and G. Barrionuevo, The multifarious hippocampal mossy fiber pathway: a review, Neuroscience 98, 407–427 (2000).
A.M. Kasyanov, V.F. Safiulina, L.L. Voronin and E. Cherubini, GABA-mediated giant depolarizing potentials as coincidence detectors for enhancing synaptic efficacy in the developing hippocampus, Proc. Natl. Acad. Sci. USA 101, 3967–3972 (2004).
G.J. Klapstein and W.F. Colmers, On the sites of presynaptic inhibition by neuropeptide Y in rat hippocampus in vitro, Hippocampus 3, 103–111 (1993).
M. Lamas, G. Gómez-Lira and R. Gutiérrez, Vesicular GABA transporter mRNA expression in the dentate gyrus and in mossy fiber synaptosomes, Mol. Brain Res. 93, 209–214 (2001).
H. Lehmann, U. Ebert and W. Löscher, Immunocytochemical localization of GABA immunoreactivity in dentate granule cells of normal and kindled rats, Neurosci. Lett. 212, 41–44 (1996).
X. Leinekugel, I. Medina, I. Khalilov, Y. Ben-Ari, R. Khazipov, Ca2+ oscillations mediated by the synergistic excitatory actions of GABA(A) and NMDA receptors in the neonatal hippocampus, Neuron 18, 243–255 (1997).
A.A. Lie, A. Becker, K. Behle, H. Beck, B. Malitschek, P.J. Conn, R. Kuhn, R. Nitsch, M. Plaschke, J. Schramm, C.E. Elger, O.D. Wiestler, I. Blumcke, Up-regulation of the metabotropic glutamate receptor mGluR4 in hippocampal neurons with reduced seizure vulnerability, Ann. Neurol. 47, 26–35 (2000).
Y. Makiura, F. Suzuki, E. Chevalier and B. Onténiente, Excitatory granule cells of the dentate gyrus exhibit a double inhibitory neurochemical content after intrahippocampal administration of kainate in adult mice, Exp. Neurol. 159, 73–83 (1999).
J. Maqueda, M. Ramírez, M. Lamas and R. Gutiéirez R., Glutamic acid decarboxylase (GAD)67, but not GAD65, is constitutively expressed during development and transiently overexpressed by activity in the granule cells of the rat, Neurosci. Lett. 353, 69–71 (2003).
M.Y. Min, D.A. Rusakov and D.M. Kullmann, Activation of AMPA, kainate, and metabotropic receptors at hippocampal mossy fiber synapses: role of glutamate diffusion, Neuron 21, 561–570 (1998).
H. Ohishi, C. Akazawa, R. Shigemoto, S. Nakanishi and N. Mizuno, Distributions of the mRNAs for L-2-amino-4-phosphonobutyrate-sensitive metabotropic glutamate receptors, mGluR4 and mGluR7, in the rat brain, J. Comp. Neurol. 360, 555–570 (1995).
V. Ramirez-Amaya, M.L. Escobar, V. Chao and F. Bermudez-Rattoni, Synaptogenesis of mossy fibers induced by spatial water maze overtraining, Hippocampus 9, 631–636 (1999).
M. Ramírez and R. Gutiérrez, Activity-dependent expression of GAD67 in the granule cells of the rat hippocampus, Brain Res. 917, 139–146 (2001).
H. Romo-Parra, C. Vivar, J. Maqueda, M.A. Morales and R. Gutiérrez R. Activity-dependent induction of multitransmitter signaling onto pyramidal cells and interneurons of area CA3 of the rat hippocampus, J. Neurophysiol. 89, 3155–3167 (2003).
A. Ruiz, R. Fabian-Fine, R. Scott, M.C. Walker, D.A. Rusakov and D.M. Kullmann, GABAA receptors at hippocampal mossy fibers, Neuron 39, 961–973 (2003).
R. Sandier and A.D. Smith, Coexistence of GABA and glutamate in mossy fiber terminals of the primate hippocampus: an ultrastructural study, J. Comp. Neurol. 303, 177–192 (1991).
D. Schmitz, J. Mellor, M. Frerking and R.A. Nicoll, Presynaptic kainate receptors at hippocampal mossy fiber synapses, Proc. Natl. Acad. Sci. USA 98, 11003–11008 (2001).
C. Schwarzer and G. Sperk, Hippocampal granule cells express glutamic acid decarboxylase-67 after limbic seizures in the rat, Neuroscience 69, 705–709 (1995).
R. Shigemoto, A. Kinoshita, E. Wada, S. Nomura, H. Ohishi, M. Takada, P.J. Flor, A. Neki, T. Abe, S. Nakanishi and N. Mizuno, Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus, J. Neurosci. 17, 7503–7522 (1997).
R.S. Sloviter, M.A. Dichter, T.L. Rachinsky, E. Dean, J.H. Goodman, A.L. Sollas and D.L. Martin, Basal expression and induction of glutamate decarboxylase and GABA in excitatory granule cells of the rat and monkey hippocampal dentate gyrus, J. Comp. Neurol. 373, 593–618 (1996).
M. Treviño, H. Romo-Parra and R. Gutiérrez, GABAA-receptor-mediated field potentials in CA3 reflect massive GABAergic transmission in the mossy fiber synapse, Submitted.
O. Vindrola, R. Briones, M. Asai and A. Fernandez-Guardiola, Amygdaloid kindling enhances the enkephalin content in the rat brain, Neurosci Lett. 21, 39–43 (1981).
M.C. Walker, A. Ruiz and D.M. Kullmann, Monosynaptic GABAergic signaling from dentate to CA3 with a pharmacological and physiological profile typical of mossy fiber synapses, Neuron 29, 703–715 (2001).
M.G. Weisskopf, R.A. Zalutsky and R.A. Nicoll, The opioid peptide dynorphin mediates heterosynaptic depression of hippocampal mossy fibre synapses and modulates long-term potentiation, Nature 365, 188 (1993).
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2005 Springer Science+Business Media, Inc.
About this paper
Cite this paper
Gutiérrez, R. et al. (2005). Kindling the GABAergic Phenotype of the Glutamatergic Granule Cells. In: Corcoran, M.E., Moshé, S.L. (eds) Kindling 6. Advances in Behavioral Biology, vol 55. Springer, Boston, MA. https://doi.org/10.1007/0-387-26144-3_8
Download citation
DOI: https://doi.org/10.1007/0-387-26144-3_8
Publisher Name: Springer, Boston, MA
Print ISBN: 978-0-387-24380-1
Online ISBN: 978-0-387-26144-7
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)