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

Kasyanov, Alexander M.; Safiulina, Victoria F.; Voronin, L. L.; Cherubini, Enrico

doi:10.1073/pnas.0305974101

Cited by 159 publications

(185 citation statements)

References 50 publications

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“…In agreement with a previous study (13), we found that with this delay the pairing procedure failed to induce synaptic potentiation. Before and after pairing, the amplitude of the evoked responses was not significantly different (6.4 Ϯ 1.1 and 4.4 Ϯ 0.9 pA, respectively; P Ͼ 0.5).…”

supporting

confidence: 82%

“…Our findings suggest that ''pairing'' persistently enhances synaptic efficacy at these synapses, an effect that depends on the rise of calcium in the postsynaptic cell. In addition, compared with our previous work (13), in the present study, we identified the intracellular signaling pathway mediating pairinginduced potentiation, which involves the activation of BDNF and the ERK pathway.…”

mentioning

confidence: 76%

“…Experiments were performed on hippocampal slices from P2-P6 Wistar rats as previously described (13). Briefly, animals were decapitated after being anesthetized with an i.p.…”

Section: Methodsmentioning

confidence: 99%

“…GDPs are therefore ideal for allowing associative modifications of coincident signals. We previously demonstrated that at mossy fiber-CA3 connections, which during the first postnatal week are mainly GABAergic (12), pairing GDPs with afferent stimulation induced a persistent increase in synaptic efficacy, which is usually restricted to the activated synapse (13).…”

mentioning

confidence: 99%

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Correlated network activity enhances synaptic efficacy via BDNF and the ERK pathway at immature CA3–CA1 connections in the hippocampus

Mohajerani

Sivakumaran²,

Zacchi³

et al. 2007

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

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At early developmental stages, correlated neuronal activity is thought to exert a critical control on functional and structural refinement of synaptic connections. In the hippocampus, between postnatal day 2 (P2) and P6, network-driven giant depolarizing potentials (GDPs) are generated by the synergistic action of glutamate and GABA, which is depolarizing and excitatory. Here the rising phase of GDPs was used to trigger Schaffer collateral stimulation in such a way that synchronized network activity was coincident with presynaptic activation of afferent input. This procedure produced a persistent increase in spontaneous and evoked ␣-amino-3-hydroxy-5-methyl-4-isoxadepropionic acid-mediated glutamatergic currents, an effect that required calcium influx through postsynaptic L-type calcium channels. No potentiation was observed when a delay of 3 sec was introduced between GDPs and afferent stimulation. Pairing-induced potentiation was prevented by scavengers of endogenous BDNF or tropomyosin-related kinase receptor B (TrkB) receptor antagonists. Blocking TrkB receptors in the postsynaptic cell did not prevent the effects of pairing, suggesting that BDNF, possibly secreted from the postsynaptic cell during GDPs, acts on TrkB receptors localized on presynaptic neurons. Application of exogenous BDNF mimicked the effects of pairing on synaptic transmission. In addition, pairing-induced synaptic potentiation was blocked by ERK inhibitors, suggesting that BDNF activates the MAPK/ERK cascade, which may lead to transcriptional regulation and new protein synthesis in the postsynaptic neuron. These results support the hypothesis that, during a critical period of postnatal development, GABA A-mediated GDPs are instrumental in tuning excitatory synaptic connections and provide insights into the molecular mechanisms involved in this process.development ͉ giant depolarizing potential ͉ excitatory postsynaptic current ͉ synaptic pairing ͉ TrkB receptors S pontaneously occurring neuronal oscillations constitute a hallmark of developmental networks (1). In the immature hippocampus, giant depolarizing potentials (GDPs) represent a primordial form of synchrony between neurons, which precedes more organized forms of activity, such as the theta and gamma rhythms (2). These events, which are characterized by recurrent membrane depolarization with superimposed fast-action potentials separated by long and variable intervals of several seconds, are generated when the synaptic traffic and cell firing within the network increase to a threshold level (3). GDPs are synaptic in origin and involve the action of both glutamate and GABA, which, during a restricted period of postnatal development, is depolarizing and excitatory (4-6). The depolarizing action of GABA during GDPs results in the activation of voltagedependent calcium channels and N-methyl-D-aspartate receptors (7). GDPs also can be recorded in vivo in rat pups, in which they occur during immobility periods, sleep, and feeding (8). GDP-associated calcium waves are thought to be crucial...

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supporting

confidence: 82%

mentioning

confidence: 76%

“…Experiments were performed on hippocampal slices from P2-P6 Wistar rats as previously described (13). Briefly, animals were decapitated after being anesthetized with an i.p.…”

Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 99%

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Correlated network activity enhances synaptic efficacy via BDNF and the ERK pathway at immature CA3–CA1 connections in the hippocampus

Mohajerani

Sivakumaran²,

Zacchi³

et al. 2007

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

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“…This may be partially attributable to the depolarizing and excitatory action of GABA (Cherubini et al, 1991), which produces giant depolarizing potentials (GDPs) (Ben-Ari et al, 1989; Sipila et al, 2005). GDPs ensure calcium entry through NMDA and voltage-dependent calcium channels (Garaschuck et al, 1998) and act as coincidence detectors and thereby persistently enhance synaptic activity at MF-CA3 synapses (Kasyanov et al, 2004).…”

Section: Introductionmentioning

confidence: 99%

GABAergic Signaling at Mossy Fiber Synapses in Neonatal Rat Hippocampus

Safiulina¹,

Fattorini²,

Conti³

et al. 2006

J. Neurosci.

139

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In the adult rat hippocampus, granule cell mossy fibers (MFs) form excitatory glutamatergic synapses with CA3 principal cells and local inhibitory interneurons. However, evidence has been provided that, in young animals and after seizures, the same fibers can release in addition to glutamate GABA. Here we show that, during the first postnatal week, stimulation of granule cells in the dentate gyrus gave rise to monosynaptic GABA A -mediated responses in principal cells and in interneurons. These synapses were indeed made by MFs because they exhibited strong paired-pulse facilitation, high sensitivity to the metabotropic glutamate receptor agonist L-AP-4, and short-term frequency-dependent facilitation.

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Characterization of NPY Y2 receptor protein expression in the mouse brain. II. Coexistence with NPY, the Y1 receptor, and other neurotransmitter‐related molecules

Stanić

Mulder

Watanabe

et al. 2011

J of Comparative Neurology

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Neuropeptide Y (NPY) is widely expressed in the brain and its biological effects are mediated through a variety of receptors. We examined, using immunohistochemistry, expression of the Y2 receptor (R) protein in the adult mouse brain and its association with NPY and the Y1R, as well as a range of additional neurotransmitters and signaling-related molecules, which previously have not been defined. Our main focus was on the hippocampal formation (HiFo), amygdaloid complex, and hypothalamus, considering the known functions of NPY and the wide expression of NPY, Y1R, and Y2R in these regions. Y2R-like immunoreactivity (-LI) was distributed in nerve fibers/terminal endings throughout the brain axis, without apparent colocalization with NPY or the Y1R. Occasional coexistence between NPY- and Y1R-LI was found in the HiFo. Following colchicine treatment, Y2R-LI accumulated in cell bodies that coexpressed γ-aminobutyric acid (GABA) in a population of cells in the amygdaloid complex and lateral septal nucleus, but not in the HiFo. Instead, Y2R-positive nerve terminals appeared to surround GABA-immunoreactive (ir) cells in the HiFo and other neuronal populations, e.g., NPY-ir cells in HiFo and tyrosine hydroxylase-ir cells in the hypothalamus. In the HiFo, Y2R-ir mossy fibers coexpressed GABA, glutamic acid decarboxylase 67 and calbindin, and Y2R-LI was found in the same fibers that contained the presynaptic metabotropic glutamate receptor 2, but not together with any of the three vesicular glutamate transporters. Our findings provide further support that Y2R is mostly presynaptic, and that Y2Rs thus have a modulatory role in mediating presynaptic neurotransmitter release.

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

Cited by 159 publications

References 50 publications

Correlated network activity enhances synaptic efficacy via BDNF and the ERK pathway at immature CA3–CA1 connections in the hippocampus

Correlated network activity enhances synaptic efficacy via BDNF and the ERK pathway at immature CA3–CA1 connections in the hippocampus

GABAergic Signaling at Mossy Fiber Synapses in Neonatal Rat Hippocampus

Characterization of NPY Y2 receptor protein expression in the mouse brain. II. Coexistence with NPY, the Y1 receptor, and other neurotransmitter‐related molecules

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