Presynaptic GABAA receptors facilitate spontaneous glutamate release from presynaptic terminals on mechanically dissociated rat CA3 pyramidal neurons

Jang, Il‐Sung; Nakamura, Michiko; Ito, Yushi; Akaike, Norio

doi:10.1016/j.neuroscience.2005.11.001

Cited by 85 publications

(106 citation statements)

References 51 publications

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“…In addition to these direct contributions of the intraterminal Ca 2ϩ , presynaptic ionotropic receptors are also associated with the activity-dependent synaptic facilitation via the regulation of presynaptic Ca 2ϩ concentrations (Nicoll and Schmitz, 2005); for example, presynaptic kainate receptors at mossy fiber synapses are also involved in the frequency facilitation of mossy fiber synaptic transmission (Schmitz et al, 2001;Kamiya et al, 2002). Furthermore, previous studies have implied that GABA A receptor-mediated fiber volley facilitation might result from presynaptic depolarization of mossy fibers (Ruiz et al, 2003;Jang et al, 2006). In the present study, synaptically released GABA acts only on axonal GABA A receptors, and there seem to be no functional GABA A receptors at synaptic terminals (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…We next examined possible involvement of GABA, another candidate for a mediator of the fiber volley facilitation, because activation of presynaptic GABA A receptors has been suggested previously to depolarize mossy fiber axons and/or terminals (Ruiz et al, 2003;Jang et al, 2006) and synaptically released GABA may act on mossy fiber terminals (Vogt and Nicoll, 1999). To examine the action of GABA in the absence of excitatory synaptic transmission, slices were first treated with the non-NMDA receptor antagonist CNQX (10 M).…”

Section: Figurementioning

confidence: 99%

“…Previously, it has been suggested that activation of presynaptic GABA A receptors may also depolarize mossy fiber axons and/or terminals, which might regulate glutamate release from the mossy fiber terminal (Ruiz et al, 2003;Jang et al, 2006). It has also been reported that synaptically released GABA may activate GABA A receptors on mossy fibers (Jang et al, 2006), and GABA released from the mossy fiber terminal (Walker et al, 2001;Gutiérrez, 2003) is a candidate that activates presynaptic GABA A receptors, although it has not yet been determined how the presynaptic GABA A receptor is activated. Thus, although the mossy fiber synapse plays a principal role as an excitatory synapse, it exceptionally shows a characteristic as an inhibitory synapse as well and its function may be regulated presynaptically by GABA A receptors, but the exact role of GABA A receptors on the mossy fiber is still unknown.…”

Section: Introductionmentioning

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: Discussionmentioning

confidence: 99%

Section: Figurementioning

confidence: 99%

Section: Introductionmentioning

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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“…Although the inhibitory effect of GABA mediated through the GABA A receptor is commonly considered to be postsynaptic, the presynaptically expressed GABA A receptors were also described in the variety of neurons in the CNS; however, the pharmacological properties of those receptors are relatively poorly understood. Mossy fibers in the hippocampus representing the axons of granule cells constitute one of the sites of the presynaptic expression of GABA receptors (Jang et al, 2006). Activation of these receptors induces neuron depolarization and facilitates spontaneous glutamate release (Jang et al, 2006).…”

Section: Gaba a Signalingmentioning

confidence: 99%

“…Mossy fibers in the hippocampus representing the axons of granule cells constitute one of the sites of the presynaptic expression of GABA receptors (Jang et al, 2006). Activation of these receptors induces neuron depolarization and facilitates spontaneous glutamate release (Jang et al, 2006). The standard anxiolytic drug, diazepam, was shown to induce an increase in the frequency of EPSPs and the potentiation of muscimol-induced glutamate release (Han et al, 2009).…”

Section: Gaba a Signalingmentioning

confidence: 99%

The Loss of Glutamate-GABA Harmony in Anxiety Disorders

Wierońska¹,

Stachowicz²,

Nowak³

et al. 2011

Anxiety Disorders

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Glucose and hippocampal neuronal excitability: Role of ATP‐sensitive potassium channels

Huang

Cheng

et al. 2007

J of Neuroscience Research

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Hyperglycemia-related neuronal excitability and epileptic seizures are not uncommon in clinical practice. However, their underlying mechanism remains elusive. ATP-sensitive K(+) (K(ATP)) channels are found in many excitable cells, including cardiac myocytes, pancreatic beta cells, and neurons. These channels provide a link between the electrical activity of cell membranes and cellular metabolism. We investigated the effects of higher extracellular glucose on hippocampal K(ATP) channel activities and neuronal excitability. The cell-attached patch-clamp configuration on cultured hippocampal cells and a novel multielectrode recording system on hippocampal slices were employed. In addition, a simulation modeling hippocampal CA3 pyramidal neurons (Pinsky-Rinzel model) was analyzed to investigate the role of K(ATP) channels in the firing of simulated action potentials. We found that incremental extracellular glucose could attenuate the activities of hippocampal K(ATP) channels. The effect was concentration dependent and involved mainly in open probabilities, not single-channel conductance. Additionally, higher levels of extracellular glucose could enhance neuropropagation; this could be attenuated by diazoxide, a K(ATP) channel agonist. In simulations, high levels of intracellular ATP, used to mimic increased extracellular glucose or reduced conductance of K(ATP) channels, enhanced the firing of action potentials in model neurons. The stochastic increases in intracellular ATP levels also demonstrated an irregular and clustered neuronal firing pattern. This phenomenon of K(ATP) channel attenuation could be one of the underlying mechanisms of glucose-related neuronal hyperexcitability and propagation.

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Presynaptic GABAA receptors facilitate spontaneous glutamate release from presynaptic terminals on mechanically dissociated rat CA3 pyramidal neurons

Cited by 85 publications

References 51 publications

GABAergic Interneurons Facilitate Mossy Fiber Excitability in the Developing Hippocampus

GABAergic Interneurons Facilitate Mossy Fiber Excitability in the Developing Hippocampus

The Loss of Glutamate-GABA Harmony in Anxiety Disorders

Glucose and hippocampal neuronal excitability: Role of ATP‐sensitive potassium channels

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