γ-Aminobutyric acid type A receptors modulate cAMP-mediated long-term potentiation and long-term depression at monosynaptic CA3–CA1 synapses

Yu, Tzu-Ping; McKinney, Sheri; Lester, Henry A.; Davidson, Norman

doi:10.1073/pnas.091093998

Cited by 32 publications

(24 citation statements)

References 40 publications

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“…The slow increase in presynaptic function during compound LTP was reminiscent of chemically induced, PKA-dependent LTP that can be induced at CA3-CA1 synapses by increasing the intracellular level of cAMP (Frey et al, 1993;Bolshakov et al, 1997;Yu et al, 2001;Otmakhov et al, 2004). To define the role of PKA in the presynaptic and postsynaptic components of compound LTP, we monitored changes in the fEPSP slope and spHp in the presence and absence of the cell-permeable, PKA-specific inhibitor PKI 14 -22 amide (1 M).…”

Section: Ltp Induced By 50 Hz Tetanization Consists Only Of the Fast mentioning

confidence: 99%

Slow Presynaptic and Fast Postsynaptic Components of Compound Long-Term Potentiation

Bayazitov¹,

Richardson²,

Fricke³

et al. 2007

J. Neurosci.

143

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Long-term potentiation (LTP) mediates learning and memory in the mammalian hippocampus. Whether a presynaptic or postsynaptic neuron principally enhances synaptic transmission during LTP remains controversial. Acute hippocampal slices were made from transgenic mouse strains that express synaptopHluorin in neurons. SynaptopHluorin is an indicator of synaptic vesicle recycling; thus, we monitored functional changes in presynaptic boutons of CA3 pyramidal cells by measuring changes in synaptopHluorin fluorescence. Simultaneously, we recorded field excitatory postsynaptic potentials to monitor changes in the strength of excitatory synapses between CA3 and CA1 pyramidal neurons. We found that LTP consists of two components, a slow presynaptic component and a fast postsynaptic component. The presynaptic mechanisms contribute mostly to the late phase of compound LTP, whereas the postsynaptic mechanisms are crucial during the early phase of LTP. We also found that protein kinase A (PKA) and L-type voltage-gated calcium channels are crucial for the expression of the presynaptic component of compound LTP, and NMDA channels are essential for that of the postsynaptic component of LTP. These data are the first direct evidence that presynaptic and postsynaptic components of LTP are temporally and mechanistically distinct.

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Section: Ltp Induced By 50 Hz Tetanization Consists Only Of the Fast mentioning

confidence: 99%

Slow Presynaptic and Fast Postsynaptic Components of Compound Long-Term Potentiation

Bayazitov¹,

Richardson²,

Fricke³

et al. 2007

J. Neurosci.

143

View full text Add to dashboard Cite

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“…The disruption of working memory by ⌬ 9 -THC was reversed in the wild-type mice by the GABA A receptor antagonist bicuculline (Varvel et al 2004), implicating both the GABAergic system and CB1Rs in the memory-disruptive effects of this drug. It has also been established that GABAergic function plays a critical role in determining the direction of hippocampal synaptic plasticity (Yu et al 2001), and that hippocampal interneuron activity is necessary to drive rhythmic cellular networks at or ␥ frequencies, which are permissive to memory formation and the expression of LTP (Traub et al 1998). Moreover, these intrinsic hippocampal rhythms can be disrupted by cannabinoids acting on CB1Rs on GABAergic terminals (Hajos et al 2000).…”

mentioning

confidence: 99%

Opposing actions of chronic Δ⁹-tetrahydrocannabinol and cannabinoid antagonists on hippocampal long-term potentiation

Hoffman¹,

Öz²,

Yang³

et al. 2007

Learn. Mem.

129

119

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Memory deficits produced by marijuana arise partly via interaction of the psychoactive component, ⌬ 9 -tetrahydrocannabinol (⌬ 9 -THC), with cannabinoid receptors in the hippocampus. Although cannabinoids acutely reduce glutamate release and block hippocampal long-term potentiation (LTP), a potential substrate for learning and memory, the consequences of prolonged exposure to ⌬ 9 -THC for hippocampal function are poorly understood. Rats were injected with ⌬ 9 -THC (10 mg/kg, i.p., q.d.) for 1, 3, or 7 d, and electrophysiological recordings were performed in hippocampal slices 1d after the final injection. At this time, ⌬ 9 -THC was undetectable in hippocampus using liquid chromatography-mass spectrometry (LC-MS). Hippocampal LTP generated using high-frequency (HFS) or theta burst stimulation was not observed in brain slices from the 7-d ⌬ -THC also produced tolerance to the inhibition of synaptic GABA, but not glutamate release by the agonist WIN55,212-2. These data define consequences of repeated ⌬ 9 -THC exposure for synaptic plasticity in the hippocampus that may help explain memory impairments in humans following chronic marijuana use.

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“…While postsynaptic infusion of PKA inhibitors has been found to block latephase LTP (Duffy and Nguyen 2003), the application of the nonhydrolyzable cAMP analog, Sp-cAMPs, elicits a persistent increase in transmission that involves increased presynaptic activity (Bolshakov et al 1997;Ma et al 1999;Yu et al 2001). Here too, NO has been proposed to act as a retrograde messenger that elicits presynaptic changes involved in Schaffer collateral LTP (Zhuo et al 1994;Arancio et al 1995;Lu et al 1999).…”

Section: Discussionmentioning

confidence: 99%

Gα_i2 inhibition of adenylate cyclase regulates presynaptic activity and unmasks cGMP-dependent long-term depression at Schaffer collateral-CA1 hippocampal synapses

Bailey

Nicholls²,

Zhang³

et al. 2008

Learn. Mem.

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Cyclic AMP signaling plays a central role in regulating activity at a number of synapses in the brain. We showed previously that pairing activation of receptors that inhibit adenylate cyclase (AC) and reduce the concentration of cyclic AMP, with elevation of the concentration of cyclic GMP is sufficient to elicit a presynaptically expressed form of LTD at Schaffer collateral-CA1 synapses in the hippocampus. To directly test the role of AC inhibition and G-protein signaling in LTD at these synapses, we utilized transgenic mice that express a mutant, constitutively active inhibitory G protein, G␣ i2 , in principal neurons of the forebrain. Transgene expression of G␣ i2 markedly enhanced LTD and impaired late-phase LTP at Schaffer collateral synapses, with no associated differences in input/output relations, paired-pulse facilitation, or NMDA receptor-gated conductances. When paired with application of a type V phosphodiesterase inhibitor to elevate the concentration of intracellular cyclic GMP, constitutively active G␣ i2 expression converted the transient depression normally caused by this treatment to an LTD that persisted after the drug was washed out. Moreover, this effect could be mimicked in control slices by pairing type V phosphodiesterase inhibitor application with application of a PKA inhibitor. Electrophysiological recordings of spontaneous excitatory postsynaptic currents and two-photon visualization of vesicular release using FM1-43 revealed that constitutively active G␣ i2 tonically reduced basal release probability from the rapidly recycling vesicle pool of Schaffer collateral terminals. Our findings support the hypothesis that inhibitory G-protein signaling acts presynaptically to regulate release, and, when paired with elevations in the concentration of cyclic GMP, converts a transient cyclic GMP-induced depression into a long-lasting decrease in release.Long-term potentiation (LTP) and long-term depression (LTD) of synaptic strength are reciprocal, activity-dependent mechanisms that are thought to mediate synaptic competition during development and store information in mature networks. cAMP and its major effector kinase, cyclic AMP-dependent protein kinase (PKA), play key roles in the induction of LTP (Frey et al. 1993;Impey et al. 1996;Nguyen and Kandel 1997;Otmakhova et al. 2000;Matsushita et al. 2001). Evidence also suggests that inhibition of adenylate cyclase (AC) and reduced PKA activity promote the induction of LTD. Inhibiting PKA enhances the induction of LTD at Schaffer collateral-CA1 synapses (Santschi et al. 1999(Santschi et al. , 2006, and simultaneous elevation of the concentration of intracellular cGMP and inhibition of PKA is sufficient to elicit LTD at these synapses in the absence of afferent stimulation (Santschi et al. 1999;Stanton et al. 2001). This chemically induced form of LTD (CLTD) is presynaptically expressed and occludes stimulusevoked LTD (SLTD), suggesting convergence of key mechanisms between CLTD and SLTD (Santschi et al. 1999;Stanton et al. 2001Stanton et al. , 200...

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γ-Aminobutyric acid type A receptors modulate cAMP-mediated long-term potentiation and long-term depression at monosynaptic CA3–CA1 synapses

Cited by 32 publications

References 40 publications

Slow Presynaptic and Fast Postsynaptic Components of Compound Long-Term Potentiation

Slow Presynaptic and Fast Postsynaptic Components of Compound Long-Term Potentiation

Opposing actions of chronic Δ⁹-tetrahydrocannabinol and cannabinoid antagonists on hippocampal long-term potentiation

Gα_i2 inhibition of adenylate cyclase regulates presynaptic activity and unmasks cGMP-dependent long-term depression at Schaffer collateral-CA1 hippocampal synapses

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γ-Aminobutyric acid type A receptors modulate cAMP-mediated long-term potentiation and long-term depression at monosynaptic CA3–CA1 synapses

Cited by 32 publications

References 40 publications

Slow Presynaptic and Fast Postsynaptic Components of Compound Long-Term Potentiation

Slow Presynaptic and Fast Postsynaptic Components of Compound Long-Term Potentiation

Opposing actions of chronic Δ9-tetrahydrocannabinol and cannabinoid antagonists on hippocampal long-term potentiation

Gαi2 inhibition of adenylate cyclase regulates presynaptic activity and unmasks cGMP-dependent long-term depression at Schaffer collateral-CA1 hippocampal synapses

Contact Info

Product

Resources

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Opposing actions of chronic Δ⁹-tetrahydrocannabinol and cannabinoid antagonists on hippocampal long-term potentiation

Gα_i2 inhibition of adenylate cyclase regulates presynaptic activity and unmasks cGMP-dependent long-term depression at Schaffer collateral-CA1 hippocampal synapses