Multiple forms of LTP in hippocampal CA3 neurons use a common postsynaptic mechanism

Yeckel, Mark F.; Kapur, Arvinder; Johnston, Daniel

doi:10.1038/10180

Cited by 291 publications

(296 citation statements)

References 49 publications

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“…In older animals, induction of LTP at MF synapses was shown to be independent of postsynaptic activation (41,42). However, like in the present experiments, under certain conditions, MF-LTP may involve a rise of calcium in the postsynaptic cell (43)(44)(45). This suggests that, at MF synapse, different forms of LTP may coexist.…”

Section: Discussionsupporting

confidence: 55%

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: Discussionsupporting

confidence: 55%

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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“…5). Although there are arguments for and against a requirement for a postsynaptic induction locus (Yeckel et al, 1999;Nicoll and Schmitz, 2005) almost all camps agree that expression of mossy fiber-pyramidal cell LTP proceeds as an increase in initial release probability of transmitter glutamate release. In marked contrast, the same high-frequency induction protocol that causes LTP at principal cell synapses induces two distinct forms of long-term depression (LTD) at mossy fiber-interneuron synapses (Figs.…”

Section: Mossy Fiber-inhibitory Interneuron Plasticitymentioning

confidence: 99%

Chapter 13 Differential mechanisms of transmission and plasticity at mossy fiber synapses

McBain

2008

Progress in Brain Research

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The last few decades have seen the hippocampal formation at front and center in the field of synaptic transmission. However, much of what we know about hippocampal short-and long-term plasticity has been obtained from research at one particular synapse; the Schaffer collateral input onto principal cells of the CA1 subfield. A number of recent studies, however, have demonstrated that there is much to be learned about target-specific mechanisms of synaptic transmission by study of the lesser known synapse made between the granule cells of the dentate gyrus; the so-called mossy fiber synapse, and its targets both within the hilar region and the CA3 hippocampus proper. Indeed investigation of this synapse has provided an embarrassment of riches concerning mechanisms of transmission associated with feedforward excitatory and inhibitory control of the CA3 hippocampus. Importantly, work from a number of labs has revealed that mossy fiber synapses possess unique properties at both the level of their anatomy and physiology, and serve as an outstanding example of a synapse designed for target-specific compartmentalization of synaptic transmission. The purpose of the present review is to highlight several aspects of this synapse as they pertain to a novel mechanism of bidirectional control of synaptic plasticity at mossy fiber synapses made onto hippocampal stratum lucidum interneurons. It is not my intention to pour over all that is known regarding the mossy fiber synapse since many have explored this topic exhaustively in the past and interested readers are directed to other fine reviews (Henze et al., 2000;Urban et al., 2001;Lawrence et al., 2003;Bischofberger et al., 2006;Nicoll and Schmitz, 2005). Keywordshippocampus; local circuit inhibitory interneuron; long-term depression; glutamate receptors; plasticity; mossy fiber; mGluR7 Anatomy of the granule cell mossy fiber axonBefore discussing the physiological properties of the mossy fiber synapse, a short description of the granule cell anatomy and in particular the mossy fiber axon is warranted. The granule cell is the principal cell of the dentate gyrus and releases the neurotransmitter glutamate (Spruston and McBain, 2006). Granule cells typically possess small, ovoid cell bodies with a single apical, and conical dendritic tree, which extends into the molecular layer and terminates close to the hippocampal fissure. Compared to other principal cells of the hippocampal formation the granule cell is relatively small, possessing a somata approximately 10 μm in *Corresponding author. Tel.: +1 301 4024778; Fax: +1 301 4024777; E-mail: E-mail: mcbainc@mail.nih.gov. Uncited references: Castillo et al. (1994), Chicurel and Harris (1992), Henze et al. (2000), Lei and McBain (2002), Urban et al. (2001), Zucker and Regehr (2002). diameter and about 18 μm along its long axis. The number of dendritic branches is highly variable but the total dendritic length is significantly shorter than their CA1 and CA3 pyramidal neuron counterparts. The axon of the granule cell emerges ...

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“…Finally, marked differences in plasticity were observed. In CA3 pyramidal neurons, highfrequency stimulation (HFS) leads to a large posttetanic potentiation (∼800%) and long-term potentiation (∼200%; [36,68,71,88,89]). In contrast, in stratum lucidum interneurons HFS induces synaptic depression rather than potentiation [50,67].…”

Section: Differential Synaptic Transmission At Mossy Fiber-pyramidal mentioning

confidence: 99%

Timing and efficacy of transmitter release at mossy fiber synapses in the hippocampal network

Bischofberger

Engel

Frotscher

et al. 2006

Pflugers Arch - Eur J Physiol

115

110

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It is widely accepted that the hippocampus plays a major role in learning and memory. The mossy fiber synapse between granule cells in the dentate gyrus and pyramidal neurons in the CA3 region is a key component of the hippocampal trisynaptic circuit. Recent work, partially based on direct presynaptic patch-clamp recordings from hippocampal mossy fiber boutons, sheds light on the mechanisms of synaptic transmission and plasticity at mossy fiber synapses. A high Na + channel density in mossy fiber boutons leads to a large amplitude of the presynaptic action potential. Together with the fast gating of presynaptic Ca 2+ channels, this generates a large and brief presynaptic Ca 2+ influx, which can trigger transmitter release with high efficiency and temporal precision. The large number of release sites, the large size of the releasable pool of vesicles, and the huge extent of presynaptic plasticity confer unique strength to this synapse, suggesting a large impact onto the CA3 pyramidal cell network under specific behavioral conditions. The characteristic properties of the hippocampal mossy fiber synapse may be important for pattern separation and information storage in the dentate gyrus-CA3 cell network.Keywords Presynaptic recording . Mossy fiber boutons . Mossy fiber synapses . Hippocampus . Autoassociative networks . Episodic memory . Synaptic efficacyThe mossy fiber synapse: a key connection in the hippocampal networkThe hippocampal formation consists of three types of principal neurons: granule cells in the dentate gyrus, CA3 pyramidal cells, and CA1 pyramidal neurons. These cells are interconnected by glutamatergic synapses, forming the classical trisynaptic circuit (Fig. 1a,b). Dentate gyrus granule cells receive excitatory glutamatergic input from layer 2 pyramidal cells of the entorhinal cortex and project to CA3 pyramidal cells. CA3 pyramidal cells project to CA1 cells, which in turn project to the subiculum and back to the entorhinal cortex [4]. In addition to this trisynaptic circuit, there is also a direct input from the entorhinal cortex to both CA3 and CA1 pyramidal cells. Furthermore, CA3 pyramidal neurons are extensively connected to each other via recurrent collateral synapses.The nonmyelinated axons of the granule cells, the socalled mossy fibers, show several structural properties that distinguish them from the other synaptic pathways [39]. They project to the CA3 region, mainly traveling within a narrow band termed "stratum lucidum." Several (∼15) large "giant" boutons (∼3-5-μm diameter) emerge from a single mossy fiber axon, either arranged in an en passant manner or attached to the main axon via a short perpendicular axonal branch [1,8,29,31] (Fig. 1c,d). A large mossy fiber bouton typically contacts only a single CA3 pyramidal neuron [21], and a mossy fiber axon contacts a given CA3 pyramidal neuron only once, as boutons are ∼150 μm apart. As the rat hippocampus contains ∼1 million granule cells

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Multiple forms of LTP in hippocampal CA3 neurons use a common postsynaptic mechanism

Cited by 291 publications

References 49 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

Chapter 13 Differential mechanisms of transmission and plasticity at mossy fiber synapses

Timing and efficacy of transmitter release at mossy fiber synapses in the hippocampal network

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