Kappa opioids inhibit induction of long-term potentiation in the dentate gyrus of the guinea pig hippocampus

Terman, GW; Wagner, John J.; Chavkin, Charles

doi:10.1523/jneurosci.14-08-04740.1994

Cited by 74 publications

(46 citation statements)

References 41 publications

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“…It is conceivable that released enkephalins may act at 6 receptors on interneurons to hyperpolarize their dendrites, which reduces calcium influx through NMDA channels and hence inhibits induction of LTI? Different opioid receptor subtypes are known to play distinct roles in modulating LTP of excitatory synaptic signals in the hippocampus (Bramham et al, 199la;Xie and Lewis, 1991;Wagner et al, 1993;Weisskopf et al, 1993;Terman et al, 1994). Our data suggest that this is also the case for opioid regulation of LTP in inhibitory circuits.…”

Section: Discussionsupporting

confidence: 59%

Endogenous opioids regulate long-term potentiation of synaptic inhibition in the dentate gyrus of rat hippocampus

Xie

Lewis

1995

J. Neurosci.

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Long-term potentiation (LTP) of excitatory transmission in the hippocampus has been extensively studied as a synaptic model of learning and memory. Here we report a new form of LTP in which inhibitory synaptic signals are potentiated following tetanic stimulation of an opioid-containing excitatory pathway in the presence of opioid antagonists. The lateral perforant path (LPP) was stimulated at the dentate outer molecular layer of hippocampal slices. Evoked synaptic currents were recorded from dentate granule cells using whole- cell voltage-clamp techniques. A high-frequency stimulus train (100 Hz, 1 sec) delivered to the LPP in the presence of naloxone (1 microM) was found to induce a long-lasting potentiation (20 min to 2 hr) in the amplitude of gamma-aminobutyric acidA (GABAA) receptor-mediated inhibitory postsynaptic currents (IPSCs) of granule cells. Such a potentiation was not observed when tetanizing the LPP in control medium. Naloxone-revealed LTP of LPP-evoked IPSCs did not depend upon the presence of granule cell discharge, and was not accompanied by potentiation of mossy fiber-evoked IPSCs, indicating that feedforward, but not feedback, inhibitory circuits were involved. Induction of this LTP could be completely blocked by the N-methyl-D-aspartate (NMDA) receptor antagonist D-2-amino-5-phosphonopentanoic acid (D-APV). However, it was not significantly affected by hyperpolarization of granule cells. These results suggest that LTP may occur at the excitatory synapses between LPP terminals and GABAergic interneurons, rather than at the inhibitory synapses between interneurons and granule cells. Further examination using selective opioid antagonists demonstrated that blocking delta, but not mu and kappa, receptors is critical for inducing LTP of IPSCs in granule cells.

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Section: Discussionsupporting

confidence: 59%

Endogenous opioids regulate long-term potentiation of synaptic inhibition in the dentate gyrus of rat hippocampus

Xie

Lewis

1995

J. Neurosci.

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“…The hippocampus is enriched with glucocorticoid receptors and is crucially involved in regulating stress effects on synaptic plasticity and learning and memory (Shors et al, 1989;Oitzl and de Kloet, 1992;Pavlides et al, 1996;Xu et al, 1997;de Quervain et al, 1998;McEwen, 1999;Kim and Diamond, 2002). On the other hand, both synaptic plasticity (Terman et al, 1994;Little and Teyler, 1996;Mansouri et al, 1999;Pu et al, 2002) and behavioral studies (Fan et al, 1999;Lu et al, 2000;Mitchell et al, 2000) support the view that the hippocampus is involved in opiate addiction, and in other drugs addiction as suggested recently (White, 1996;Berke and Hyman, 2000;Hyman and Malenka, 2001;Nestler, 2001a;Vorel et al, 2001). …”

Section: Reinforcing Effect and Associative Learningmentioning

confidence: 77%

“…Previous studies have shown that stress or glucocorticoids block or facilitate memory and affect LTP and long-term depression (LTD) in the hippocampus (Shors et al, 1989;McEwen, 1994;Diamond et al, 1996;Kim et al, 1996;Xu et al, 1997Xu et al, , 1998ade Quervain et al, 1998;Conrad et al, 1999;Mizoguchi et al, 2000). Similarly, opiates affect cognitive function (Beatty, 1983;Classen and Mondadori, 1984;Guerra et al, 1987;Li et al, 2001) facilitate (Mansouri et al, 1999) or inhibit (Terman et al, 1994;Pu et al, 2002) LTP, and facilitate LTD (Wagner et al, 2001) in the hippocampus. Furthermore, stress modifies morphine responses in behavior (Olley et al, 1990;Deroche et al, 1992), and morphine influences the effect of stress on synaptic plasticity and behavior (Fratta et al, 1977;Shors et al, 1990;Scheggi et al, 2000).…”

Section: Introductionmentioning

confidence: 99%

Stress Enables Synaptic Depression in CA1 Synapses by Acute and Chronic Morphine: Possible Mechanisms for Corticosterone on Opiate Addiction

Yang¹,

Zheng²,

Wang³

et al. 2004

J. Neurosci.

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The hippocampus, being sensitive to stress and glucocorticoids, plays significant roles in certain types of learning and memory. Therefore, the hippocampus is probably involved in the increasing drug use, drug seeking, and relapse caused by stress. We have studied the effect of stress with morphine on synaptic plasticity in the CA1 region of the hippocampus in vivo and on a delayed-escape paradigm of the Morris water maze. Our results reveal that acute stress enables long-term depression (LTD) induction by low-frequency stimulation (LFS) but acute morphine causes synaptic potentiation. Remarkably, exposure to an acute stressor reverses the effect of morphine from synaptic potentiation (ϳ20%) to synaptic depression (ϳ40%), precluding further LTD induction by LFS. The synaptic depression caused by stress with morphine is blocked either by the glucocorticoid receptor antagonist RU38486 or by the NMDA-receptor antagonist D-APV. Chronic morphine attenuates the ability of acute morphine to cause synaptic potentiation, and stress to enable LTD induction, but not the ability of stress in tandem with morphine to cause synaptic depression. Furthermore, corticosterone with morphine during the initial phase of drug use promotes later delayed-escape behavior, as indicated by the morphine-reinforced longer latencies to escape, leading to persistent morphine-seeking after withdrawal. These results suggest that hippocampal synaptic plasticity may play a significant role in the effects of stress or glucocorticoids on opiate addiction.

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“…These released dynorphins were found to selectively bind to kappa opioid receptors after release (Wagner et al, 1991). Focal stimulation of dynorphin-containing pathways caused presynaptic inhibition of excitatory synaptic transmission in hippocampus that could be selectively blocked by kappa receptor antagonism (Wagner et al, 1993;Weisskopf et al, 1993;Drake et al, 1994;Terman et al, 1994). These studies are summarized in more complete reviews (Castillo et al, 1996;Simmons and Chavkin, 1996) and diagrammed in Fig.…”

Section: Neurotransmitter Properties Of Dynorphinmentioning

confidence: 99%

Dynorphin–Still an Extraordinarily Potent Opioid Peptide

Chavkin

2012

Mol Pharmacol

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This issue of Molecular Pharmacology is dedicated to Dr. Avram Goldstein, the journal's founding editor and one of the leaders in the development of modern pharmacology. This article focuses on his contributions to the discovery of the dynorphins and evidence that members of this family of opioid peptides are endogenous agonists for the kappa opioid receptor. In his original publication describing the purification and sequencing of dynorphin A, Avram described this peptide as "extraordinarily potent" ("dyn" from the Greek, dynamis 5 power and "orphin" for endogenous morphine peptide). The name originally referred to its high affinity and great potency in the bioassay that was used to follow its activity during purification, but the name has come to have a second meaning: studies of its physiologic function in brain continue to provide powerful insights to the molecular mechanisms controlling mood disorders and drug addiction. During the 30 years since its discovery, we have learned that the dynorphin peptides are released in brain during stress exposure. After they are released, they activate kappa opioid receptors distributed throughout the brain and spinal cord, where they trigger cellular responses resulting in different stress responses: analgesia, dysphoria-like behaviors, anxietylike responses, and increased addiction behaviors in experimental animals. Avram predicted that a detailed molecular analysis of opiate drug actions would someday lead to better treatments for drug addiction, and he would be gratified to know that subsequent studies enabled by his discovery of the dynorphins resulted in insights that hold great promise for new treatments for addiction and depressive disorders.

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Kappa opioids inhibit induction of long-term potentiation in the dentate gyrus of the guinea pig hippocampus

Cited by 74 publications

References 41 publications

Endogenous opioids regulate long-term potentiation of synaptic inhibition in the dentate gyrus of rat hippocampus

Endogenous opioids regulate long-term potentiation of synaptic inhibition in the dentate gyrus of rat hippocampus

Stress Enables Synaptic Depression in CA1 Synapses by Acute and Chronic Morphine: Possible Mechanisms for Corticosterone on Opiate Addiction

Dynorphin–Still an Extraordinarily Potent Opioid Peptide

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