Long-Lasting Modulation of Synaptic Transmission by Metabotropic Glutamate Receptors

Gallagher, Joel P.; Zheng, Fang; Shinnick‐Gallagher, Patricia

doi:10.1007/978-1-4757-2298-7_7

Cited by 9 publications

(4 citation statements)

References 68 publications

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“…The metabotropic glutamate receptors, modulating both glutamate and GABA signaling in the NTS, provide an additional target for plasticity (20,22,64). Studies in other networks have demonstrated that activating presynaptic and postsynaptic metabotropic glutamate receptors not only acutely modulates neurotransmission, but also induces Hebbian plasticity: longterm potentiation (60) and long-term depression (8,35,40,49,66). To the extent that plasticity of metabotropic glutamate receptors on neurons in the lung and airway reflex pathway in the NTS can occur, the data could provide new insights into how the transmission of airway-related information is modified to evoke long-term changes in reflex outputs.…”

Section: Neurotransmitters and Neuromodulatorsmentioning

confidence: 99%

Plasticity in the nucleus tractus solitarius and its influence on lung and airway reflexes

Bonham¹,

Chen²,

Sekizawa³

et al. 2006

Journal of Applied Physiology

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The nucleus tractus solitarius (NTS) is the first central nervous system (CNS) site for synaptic contact of the primary afferent fibers from the lungs and airways. The signal processing at these synapses will determine the output of the sensory information from the lungs and airways to all downstream synapses in the reflex pathways. The second-order NTS neurons bring to bear their own intrinsic and synaptic properties to temporally and spatially integrate the sensory information with inputs from local networks, higher brain regions, and circulating mediators, to orchestrate a coherent reflex output. There is growing evidence that NTS neurons share the rich repertoire of forms of plasticity demonstrated throughout the CNS. This review focuses on existing evidence for plasticity in the NTS, potential targets for plasticity in the NTS, and the impact of this plasticity on lung and airway reflexes.

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Section: Neurotransmitters and Neuromodulatorsmentioning

confidence: 99%

Plasticity in the nucleus tractus solitarius and its influence on lung and airway reflexes

Bonham¹,

Chen²,

Sekizawa³

et al. 2006

Journal of Applied Physiology

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“…Multiple physiological roles for mGluRs have been identified, including neuronal excitation (increase of cell excitability, potentiation of glutamate release, coinduction, or facilitation of LTP) as well as neuronal inhibition (hyperpolarization, presynaptic inhibition of glutamate and GABA release, coinduction, or facilitation of LTD), and a possible implication in glutamate-induced neurotoxicity (for review, see Schoepp and Conn, 1993;Gallagher et al, 1994;Ben-Ari and Aniksztejn, 1995;Pin and Duvoisin, 1995). The mGluRs are coupled to a large variety of second messenger systems [including activation of phospholipase C (PLC) and inhibition of adenylyl cyclase] and modulate several ligand-gated ionic channels (for review, see Schoepp and Conn, 1993;Pin and Duvoisin, 1995).…”

Section: ϩ -Activated Nonselective Cationic Current; Slow Synaptic Imentioning

confidence: 99%

A Long-Lasting Calcium-Activated Nonselective Cationic Current Is Generated by Synaptic Stimulation or Exogenous Activation of Group I Metabotropic Glutamate Receptors in CA1 Pyramidal Neurons

et al. 1997

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We have shown previously that a selective metabotropic glutamate receptor (mGluR) agonist, 1S,3R-1-aminocyclopentane-1,3-dicarboxylate (1S,3R-ACPD), evokes an inward current in CA1 pyramidal neurons of rat hippocampal slices in the presence of K ϩ channel blockers (Cré pel et al., 1994). This current has been characterized as a Ca 2ϩ -activated nonselective cationic (CAN) current. Using whole-cell patch-clamp recordings and intracellular dialysis, we now have identified the mGluR subtype and the mechanisms underlying the CAN current (I CAN ) and report for the first time the presence of a synaptic I CAN in the mammalian CNS. First, we have shown pharmacologically that activation of I CAN by 1S,3R-ACPD involves the group I mGluRs (and not the groups II and III) and a G-protein-dependent process. We also report that I CAN is modulated by the divalent cations (Mg 2ϩ , Cd 2ϩ , and Zn 2ϩ ). Second, we have isolated a slow synaptic inward current evoked by a high-frequency stimulation in the presence of K ϩ channel blockers, ionotropic glutamate, and GABA A receptor antagonists. This current shows similar properties to the exogenously evoked I CAN : its reversal potential is close to the reversal potential of the 1S,3R-ACPD-evoked I CAN , and it is G-protein-and Ca 2ϩ -dependent. Because the amplitude and duration of I CAN increased in the presence of a glutamate uptake blocker, we suggest that this synaptic current is generated via the activation of mGluRs. We propose that the synaptic I CAN , activated by a brief tetanic stimulation and leading to a long-lasting inward current, may be involved in neuronal plasticity and synchronized network-driven oscillations.

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“…Key words: metabotropic glutamate receptors; group-I subtype; group-II; group-III; synaptic transmission; presynaptic; postsynaptic; excitability; potassium channels; brainstem; spinal cord; phrenic motoneurons; respiration Metabotropic glutamate receptors (mGluRs) modulate neuronal function via affecting excitability and altering synaptic transmission (Schoepp and Conn, 1993;Gallagher et al, 1994;Pin and Duvoisin, 1995). The diversity of mGluR actions can be primarily attributed to different receptor subtypes [mGluR1-8 (Pin and Bockaert, 1995)] and their cellular localizations.…”

mentioning

confidence: 99%

Distinct Subtypes of Metabotropic Glutamate Receptors Mediate Differential Actions on Excitability of Spinal Respiratory Motoneurons

Dong

Feldman

1999

J. Neurosci.

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Metabotropic glutamate receptors (mGluRs) modulate neuronal function by affecting excitability and altering synaptic transmission. We have shown that the mGluR agonist (1S,3R)-1-amino-1, 3-cyclopentanedicarboxylic acid (1S,3R-ACPD) has multiple actions on phrenic motoneurons (PMNs), including reduction of inspiratory-modulated synaptic currents and an increase of neuronal excitability. We hypothesized that these actions were mediated by different mGluR subtypes. We have now identified the involvement of mGluR subtypes and their roles in modulating the excitability of PMNs and the consequent inspiratory motor output in an in vitro neonatal rat brainstem-spinal cord preparation. Activation of postsynaptic group-I mGluRs increases PMN excitability, associated with the production of an inward current and a decrease in membrane conductance, whereas activation of group-II or group-III mGluRs decreases PMN inspiratory-modulated synaptic current, probably via a presynaptic mechanism. To confirm further the distinction and the involvement of group-I and group-II/-III receptor subtypes affecting PMN excitability, we used the membrane permeable cAMP analog 8-bromo-cAMP (8-Br-cAMP) to elevate intracellular cAMP concentration to mask or occlude any effects mediated via the cAMP cascade. 8-Br-cAMP attenuated the reduction of the inspiratory-modulated activity of PMNs by both (S)-4-carboxy-3-hydroxyphenylglycine (4C3HPG) and L-(+)-2-amino-4-phosphonobutyric acid (L-AP4), agonists for group-II and group-III mGluRs, respectively, but did not affect the actions of 3,5-dihydroxyphenylglycine (DHPG), an agonist for group-I mGluRs. These three groups of mGluRs are all endogenously activated during the inspiratory phase. We conclude that three groups of mGluRs are functionally expressed in the phrenic nucleus and that their activation modulates PMN excitability via distinct mechanisms, with group-I acting at postsynaptic sites and group-II and group-III acting at presynaptic sites.

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Long-Lasting Modulation of Synaptic Transmission by Metabotropic Glutamate Receptors

Cited by 9 publications

References 68 publications

Plasticity in the nucleus tractus solitarius and its influence on lung and airway reflexes

Plasticity in the nucleus tractus solitarius and its influence on lung and airway reflexes

A Long-Lasting Calcium-Activated Nonselective Cationic Current Is Generated by Synaptic Stimulation or Exogenous Activation of Group I Metabotropic Glutamate Receptors in CA1 Pyramidal Neurons

Distinct Subtypes of Metabotropic Glutamate Receptors Mediate Differential Actions on Excitability of Spinal Respiratory Motoneurons

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