GABAergic Signaling at Mossy Fiber Synapses in Neonatal Rat Hippocampus

Safiulina, Victoria F.; Fattorini, Giorgia; Conti, Fiorenzo; Cherubini, Enrico

doi:10.1523/jneurosci.4493-05.2006

Cited by 82 publications

(156 citation statements)

References 61 publications

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“…Previous studies have suggested that DG granule cells express GABAergic phenotypes (Walker et al, 2001;Gutiérrez, 2003;Safiulina et al, 2006), which are gradually decreased with development, and eventually disappear at around P24, and the time course of the change in GABAergic phenotypes is similar to that of the fiber volley facilitation discovered in the present study (Figs. 3,4 F).…”

Section: Discussionsupporting

confidence: 89%

“…Previous studies have shown that the granule cells in the DG express GABAergic phenotypes (Gutiérrez, 2003), and glutamate and GABA are coreleased from the mossy fiber terminal during the first 3 weeks after birth (Walker et al, 2001;Safiulina et al, 2006). Thus, the source of GABA responsible for the fiber volley facilitation may be not only GABAergic interneurons but also the mossy fiber terminal itself.…”

Section: Gabaergic Interneurons Contribute To the Fiber Volley Facilimentioning

confidence: 99%

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GABAergic Interneurons Facilitate Mossy Fiber Excitability in the Developing Hippocampus

Nakamura¹,

Sekino²,

Manabe³

2007

J. Neurosci.

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Profound activity-dependent synaptic facilitation at hippocampal mossy fiber synapses is a unique and functionally important property. Although presynaptic ionotropic receptors, such as kainate receptors, contribute partially to the facilitation in the hippocampus, the precise mechanisms of presynaptic regulation by endogenous neurotransmitters remain unclear. In this study, we report that axonal GABA A receptors on mossy fibers are involved in the activity-dependent facilitation during development. In immature mouse hippocampal slices, short-train stimulation (five pulses at 25 Hz) caused frequency-dependent facilitation of not only postsynaptic responses but also presynaptic fiber volleys that represent presynaptic activities. This fiber volley facilitation was inhibited by selective GABA A receptor antagonists, or by enkephalin that selectively suppresses excitability of interneurons. Furthermore, we directly demonstrated that this facilitation resulted from depolarization of mossy fibers in imaging experiments using a voltage-sensitive dye. This increased mossy fiber excitability caused by depolarizing action of GABA gradually decreased with development and eventually disappeared at around postnatal day 30. These results suggested that GABA released from interneurons acted on axonal GABA A receptors on mossy fibers and contributed at least partially to the activity-and age-dependent facilitation in the hippocampus.

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Section: Discussionsupporting

confidence: 89%

Section: Gabaergic Interneurons Contribute To the Fiber Volley Facilimentioning

confidence: 99%

GABAergic Interneurons Facilitate Mossy Fiber Excitability in the Developing Hippocampus

Nakamura¹,

Sekino²,

Manabe³

2007

J. Neurosci.

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“…Dual glutamate/GABA transmission at MF synapses is supported by the following evidence: (1) GAD and VIAAT are expressed in MFTs (Sloviter et al, 1996;Gutiérrez et al, 2003;Zander et al, 2010), (2) GABA is released from isolated MF synaptosomes (Gó mez-Lira et al, 2002), (3) GABAA receptors are expressed in the postsynaptic density facing GAD-immunopositive MFTs (Bergersen et al, 2003), and (4) IPSCs are detected upon extracellular stimulation in st. granulosum (Walker et al, 2001;Gutiérrez et al, 2003;Safiulina et al, 2006; but see Mori et al, 2004;Uchigashima et al, 2007;Toni et al, 2008). Our results appear consistent with some of these observations but do not support the conclusion that postsynaptic GABAA receptors are activated by GABA release at MFTs upon phasic activity.…”

Section: Discussioncontrasting

confidence: 69%

“…1), together with the presence of local interneurons in the granule cell layer and hilus (Lübke et al, 1998;Houser, 2007) complicates the interpretation of postsynaptic responses evoked by extracellular electrical stimulation (Walker et al, 2001;Safiulina et al, 2006;Uchigashima et al, 2007). We examined the postsynaptic responses evoked by photostimulation of individual, visually identified GCs using local photolysis of MNI-glutamate in hippocampal organotypic slices from G42 mice.…”

Section: Resultsmentioning

confidence: 99%

“…In addition to glutamate, mossy fiber terminals (MFTs) have been shown to contain GABA (Sandler and Smith, 1991), the GABAsynthesizing enzyme glutamate decarboxylase (GAD; Sloviter et al, 1996), and the vesicular transporter VIAAT (vesicular inhibitory amino acid transporter; Zander et al, 2010). Mixed (glutamatergic and GABAergic), apparently monosynaptic responses are recorded in CA3 pyramidal neurons upon stimulation of the granule cell layer, suggesting the two neurotransmitters might be coreleased from MFTs (Walker et al, 2001;Safiulina et al, 2006). This was observed both in juvenile [ϽP24 (postnatal day 24)] animals (Gutiérrez et al, 2003) and under pathological conditions in adults (Sloviter et al, 1996), suggesting MFs may be endowed with a developmental and activity-dependent switch of neurotransmitter modality.…”

Section: Introductionmentioning

confidence: 99%

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Presynaptic But Not Postsynaptic GABA Signaling at Unitary Mossy Fiber Synapses

Cabezas

Irinopoulou²,

Gauvain³

et al. 2012

J. Neurosci.

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Dentate gyrus granule cells have been suggested to corelease GABA and glutamate both in juvenile animals and under pathological conditions in adults. Although mossy fiber terminals (MFTs) are known to express glutamic acid decarboxylase (GAD) in early postnatal development, the functional role of GABA synthesis in MFTs remains controversial, and direct evidence for synaptic GABA release from MFTs is missing. Here, using GAD67-GFP transgenic mice, we show that GAD67 is expressed only in a population of immature granule cells in juvenile animals. We demonstrate that GABA can be released from these cells and modulate mossy fiber excitability through activation of GABAB autoreceptors. However, unitary postsynaptic currents generated by individual, GAD67-expressing granule cells are purely glutamatergic in all postsynaptic cell types tested. Thus GAD67 expression does not endow dentate gyrus granule cells with a full GABAergic phenotype and GABA primarily instructs the pre-rather than the postsynaptic element.

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Postnatal cellular contributions of the hippocampus subventricular zone to the dentate gyrus, corpus callosum, fimbria, and cerebral cortex

et al. 2006

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The rodent dentate gyrus (DG) is formed in the embryo when progenitor cells migrate from the dentate neuroepithelium to establish a germinal zone in the hilus and a secondary germinal matrix, near the fimbria, called the hippocampal subventricular zone (HSVZ). The developmental plasticity of progenitors within the HSVZ is not well understood. To delineate the migratory routes and fates of progenitors within this zone, we injected a replication-incompetent retrovirus, encoding the enhanced green fluorescent protein (EGFP), into the HSVZ of postnatal day 5 (P5) mice. Between P6 and P45, retrovirally-infected EGFP(+) of progenitors migrated into the DG, established a reservoir of progenitor cells, and differentiated into neurons and glia. By P6-7, EGFP(+) cells were observed migrating into the DG. Subsets of these EGFP(+) cells expressed Sox2 and Musashi-1, characteristic of neural stem cells. By P10, EGFP(+) cells assumed positions within the DG and expressed immature neuronal markers. By P20, many EGFP(+) cells expressed the homeobox prospero-like protein Prox1, an early and specific granule cell marker in the CNS, and extended mossy fiber projections into the CA3. A subset of non-neuronal EGFP(+) cells in the dentate gyrus acquired the morphology of astrocytes. Another subset included EGFP(+)/RIP(+) oligodendrocytes that migrated into the fimbria, corpus callosum, and cerebral cortex. Retroviral injections on P15 labeled very few cells, suggesting depletion of HSVZ progenitors by this age. These findings suggest that the early postnatal HSVZ progenitors are multipotent and migratory, and contribute to both dentate gyrus neurogenesis as well as forebrain gliogenesis.

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GABAergic Signaling at Mossy Fiber Synapses in Neonatal Rat Hippocampus

Cited by 82 publications

References 61 publications

GABAergic Interneurons Facilitate Mossy Fiber Excitability in the Developing Hippocampus

GABAergic Interneurons Facilitate Mossy Fiber Excitability in the Developing Hippocampus

Presynaptic But Not Postsynaptic GABA Signaling at Unitary Mossy Fiber Synapses

Postnatal cellular contributions of the hippocampus subventricular zone to the dentate gyrus, corpus callosum, fimbria, and cerebral cortex

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