Monosynaptic GABAergic Signaling from Dentate to CA3 with a Pharmacological and Physiological Profile Typical of Mossy Fiber Synapses

Walker, Matthew C.; Ruiz, Arnaud; Kullmann, Dimitri M.

doi:10.1016/s0896-6273(01)00245-8

Cited by 181 publications

(207 citation statements)

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“…They also demonstrate that, at this developmental stage, GABA is the main neurotransmitter released from the MF (21,22). That granule cells from the DG may corelease GABA and glutamate early in postnatal life was already known (21).…”

Section: Discussionmentioning

confidence: 71%

“…This assumption has been verified on mossy fiber (MF)-CA3 connections that, during the first postnatal week, are still poorly developed, reaching a full maturation only toward the end of the second postnatal week (20). This pathway is of particular interest because it can release GABA in addition to glutamate (21). Moreover, it has been shown that, during postnatal development, granule cells of the dentate gyrus (DG), from which MF originate, transiently express a functional GABAergic phenotype (22).…”

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confidence: 94%

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GABA-mediated giant depolarizing potentials as coincidence detectors for enhancing synaptic efficacy in the developing hippocampus

Kasyanov

Safiulina

Voronin

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

159

171

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Spontaneously occurring neuronal oscillations constitute a hallmark of developmental networks. They have been observed in the retina, neocortex, hippocampus, thalamus, and spinal cord. In the immature hippocampus, the so-called ''giant depolarizing potentials'' (GDPs) are network-driven synaptic events generated by ␥-aminobutyric acid (GABA), which at this stage is depolarizing and excitatory. We have tested the hypothesis that during the first postnatal week, GDP-associated calcium signals may alter the properties of synaptic transmission at poorly developed mossy fiber (MF)-CA3 connections. We found that ''pairing'' GDPs with MF stimulation induced a persistent increase in synaptic efficacy at MF-CA3 synapses. When the interval between GDPs and MF stimulation was increased, the potentiating effect progressively declined and disappeared. The potentiation depended on activation of voltage-dependent calcium channels and calcium flux. This activity may contribute to the refinement of neuronal connectivity before the establishment of the adult neuronal circuit. mossy fibers ͉ synaptic plasticity ͉ GABA-mediated oscillatory events ͉ development ͉ synaptic pairing

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Section: Discussionmentioning

confidence: 71%

mentioning

confidence: 94%

GABA-mediated giant depolarizing potentials as coincidence detectors for enhancing synaptic efficacy in the developing hippocampus

Kasyanov

Safiulina

Voronin

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

159

171

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“…Both presynaptic and postsynaptic mechanisms contribute to the generation of this functional variety (Craig and Boudin, 2001;Atwood and Karunanithi, 2002). Electrophysiological studies on mossy fiber synapses indicate that the glutamatergic and GABAergic secretory components of a single cell behave as if they were packed in different secretory vesicles (Walker et al, 2001). Our evidence suggests that the functional diversity of synapses could also result from heterogeneity in SV composition dictated by the biogenesis pathway followed.…”

Section: Discussionmentioning

confidence: 76%

The Zinc Transporter ZnT3 Interacts with AP-3 and It Is Preferentially Targeted to a Distinct Synaptic Vesicle Subpopulation

Salazar

Love

Werner

et al. 2004

MBoC

112

178

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Synaptic vesicles (SV) are generated by two different mechanisms, one AP-2 dependent and one AP-3 dependent. It has been uncertain, however, whether these mechanisms generate SV that differ in molecular composition. We explored this hypothesis by analyzing the targeting of ZnT3 and synaptophysin both to PC12 synaptic-like microvesicles (SLMV) as well as SV isolated from wild-type and AP-3-deficient mocha brains. ZnT3 cytosolic tail interacted selectively with AP-3 in cell-free assays. Accordingly, pharmacological disruption of either AP-2-or AP-3-dependent SLMV biogenesis preferentially reduced synaptophysin or ZnT3 targeting, respectively; suggesting that these antigens were concentrated in different vesicles. As predicted, immuno-isolated SLMV revealed that ZnT3 and synaptophysin were enriched in different vesicle populations. Likewise, morphological and biochemical analyses in hippocampal neurons indicated that these two antigens were also present in distinct but overlapping domains. ZnT3 SV content was reduced in AP-3-deficient neurons, but synaptophysin was not altered in the AP-3 null background. Our evidence indicates that neuroendocrine cells assemble molecularly heterogeneous SV and suggests that this diversity could contribute to the functional variety of synapses. INTRODUCTIONThe molecular diversity in total brain synaptic vesicle (SV) composition is generally presumed to result from differential expression of synaptic vesicle membrane proteins in different brain regions. However, the possibility that synaptic vesicles differ in composition because of different biogenesis mechanisms has not been explored. Different vesiculation pathways could result in molecularly diverse synaptic vesicles. Vesiculation mechanisms are known to produce distinct cargo carriers from a population of donor membranes (Bonifacino and Dell'Angelica, 1999;Springer et al., 1999;Boehm and Bonifacino, 2001). This process is achieved by adaptor complexes that recognize and concentrate specific membrane proteins in the donor membranes (Bonifacino and Dell 'Angelica, 1999;Kirchhausen, 1999). PC12 cells have been shown to possess two such adaptor-dependent pathways for the assembly of synaptic vesicles, also known as synaptic-like microvesicles (SLMV) (Shi et al., 1998;de Wit et al., 1999;Jarousse and Kelly, 2001). In one pathway, SLMV are generated from the plasma membrane by a vesiculation mechanism that requires the adaptor AP-2, clathrin, and the GTPase dynamin (Shi et al., 1998). In the second pathway, SLMV are generated from endosomes by the adaptor complex AP-3 (Faundez et al., 1998;Blumstein et al., 2001) and the GTPase ARF1 (Faundez et al., 1997). In contrast to the plasma membrane pathway, the endosomederived mechanism is highly sensitive to brefeldin A (BFA) (Shi et al., 1998).Phenotypes observed in the AP-3-deficient mocha mouse are consistent with a role for the AP-3-dependent, endosome-derived pathway in neurons (Kantheti et al., 1998). The mocha mossy fibers are devoid of both the synaptic vesiclespecific zinc transpor...

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“…None of the studies described above have addressed whether new neurons can synthesize and release glutamate or to what extent their output properties may differ from those of mature DGCs (31,39,52). This information is particularly important considering that a small subpopulation of DGCs can release GABA (53), and it would be tempting to speculate that those GABAergic DGCs might originate during adulthood. Liu and collaborators (16) have recently demonstrated that the adult DG can generate not only functional DGCs but also GABAergic interneurons.…”

Section: Functional Neurogenesis In Tissue Culturementioning

confidence: 99%

A Hypothesis About the Role of Adult Neurogenesis in Hippocampal Function

Schinder

Gage

2004

Physiology

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The functional relevance of adult hippocampal neurogenesis has long been a matter of intense experimentation and debate, but the precise role of new neurons has not been sufficiently elaborated. Here we propose a hypothesis in which specific features of newly generated neurons contribute to hippocampal plasticity and function and discuss the most recent and relevant findings in the context of the proposed hypothesis.

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Monosynaptic GABAergic Signaling from Dentate to CA3 with a Pharmacological and Physiological Profile Typical of Mossy Fiber Synapses

Cited by 181 publications

References 53 publications

GABA-mediated giant depolarizing potentials as coincidence detectors for enhancing synaptic efficacy in the developing hippocampus

GABA-mediated giant depolarizing potentials as coincidence detectors for enhancing synaptic efficacy in the developing hippocampus

The Zinc Transporter ZnT3 Interacts with AP-3 and It Is Preferentially Targeted to a Distinct Synaptic Vesicle Subpopulation

A Hypothesis About the Role of Adult Neurogenesis in Hippocampal Function

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