Cyclic adenosine‐3′,5′‐monophosphate potentiates the synaptic potential mediated by NMDA receptors in the amygdala

C. C. Huang, Po-Wu Gean

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10 Citations (Scopus)

Abstract

An in vitro slice preparation of rat amygdala was used to study the actions of forskolin and cyclic adenosine‐3′,5′‐monophosphate (cAMP) analogues on the N‐methyl‐D‐aspartate (NMDA) receptor‐mediated synaptic potential (EPSPNMDA). Intracellular recordings were made from basolateral amygdala neurons in the presence of 6‐cyano‐7‐nitroquinoxaline‐2,3‐dione (CNQX, 10μM) and picrotoxin (50 μM) to pharmacologically isolate the EPSPNMDA. Application of forskolin (25 μM) markedly and persistently potentiated the EPSPNMDA In contrast, the inactive forskolin analogue, 1,9‐dideoxy‐forskolin, failed to affect the EPSPNMDA significantly. Superfusion of dibutyryl‐cAMP (dbcAMP, 200 μM) for 15 min caused a transient depression of the amplitude of EPSPNMDA. The EPSPNMDA amplitude was reduced to 68 ± 3% of control (n = 10) 15 min after the application, restored to its control value within 25 min, and followed by a long‐term potentiation (LTP). Pretreating the slices with 8‐cyclopentyl‐1,3‐dipropylxanthine (DPCPX, 5 μM), a selective A1 receptor antagonist, blocked the transient depressive phase produced by dbcAMP. This result suggests that the transient depression induced by dbcAMP was likely due to the interaction of dbcAMP or its breakdown products with adenosine A1 receptors. To determine the site of action, we examined the effect of forskolin on the postsynaptic responses to exogenously applied NMDA. Forskolin potentiated the postsynaptic depolarization induced by NMDA, suggesting that the enhancement is mediated, at least in part, by a persistent upregulation of postsynaptic NMDA receptor‐operated conductances. Occlusion experiments were performed to examine whether the sustained enhancements of EPSPNMDA produced by tetanic stimulation (TS) and forskolin share a common mechanism. Three episodes of TS were delivered to saturate the LTP and, under this condition, forskolin still caused a further potentiation of the EPSPNMDA. Similarly, TS, delivered after the EPSPNMDA was enhanced by forskolin or dbcAMP, produced LTP. These results suggest that the long‐term enhancements of EPSPNMDA produced by TS and forskolin are different and thus do not support the hypothesis that activation of protein kinase A triggers LTP. © 1995 Wiley‐Liss, Inc.

Original languageEnglish
Pages (from-to)747-754
Number of pages8
JournalJournal of Neuroscience Research
Volume40
Issue number6
DOIs
Publication statusPublished - 1995

Fingerprint

Synaptic Potentials
Colforsin
Amygdala
6-Cyano-7-nitroquinoxaline-2,3-dione
Adenosine A1 Receptors
Picrotoxin
Cyclic AMP-Dependent Protein Kinases
Up-Regulation
Neurons

All Science Journal Classification (ASJC) codes

  • Cellular and Molecular Neuroscience

Cite this

@article{5da917687ce8417e9864a0ed8331daaf,
title = "Cyclic adenosine‐3′,5′‐monophosphate potentiates the synaptic potential mediated by NMDA receptors in the amygdala",
abstract = "An in vitro slice preparation of rat amygdala was used to study the actions of forskolin and cyclic adenosine‐3′,5′‐monophosphate (cAMP) analogues on the N‐methyl‐D‐aspartate (NMDA) receptor‐mediated synaptic potential (EPSPNMDA). Intracellular recordings were made from basolateral amygdala neurons in the presence of 6‐cyano‐7‐nitroquinoxaline‐2,3‐dione (CNQX, 10μM) and picrotoxin (50 μM) to pharmacologically isolate the EPSPNMDA. Application of forskolin (25 μM) markedly and persistently potentiated the EPSPNMDA In contrast, the inactive forskolin analogue, 1,9‐dideoxy‐forskolin, failed to affect the EPSPNMDA significantly. Superfusion of dibutyryl‐cAMP (dbcAMP, 200 μM) for 15 min caused a transient depression of the amplitude of EPSPNMDA. The EPSPNMDA amplitude was reduced to 68 ± 3{\%} of control (n = 10) 15 min after the application, restored to its control value within 25 min, and followed by a long‐term potentiation (LTP). Pretreating the slices with 8‐cyclopentyl‐1,3‐dipropylxanthine (DPCPX, 5 μM), a selective A1 receptor antagonist, blocked the transient depressive phase produced by dbcAMP. This result suggests that the transient depression induced by dbcAMP was likely due to the interaction of dbcAMP or its breakdown products with adenosine A1 receptors. To determine the site of action, we examined the effect of forskolin on the postsynaptic responses to exogenously applied NMDA. Forskolin potentiated the postsynaptic depolarization induced by NMDA, suggesting that the enhancement is mediated, at least in part, by a persistent upregulation of postsynaptic NMDA receptor‐operated conductances. Occlusion experiments were performed to examine whether the sustained enhancements of EPSPNMDA produced by tetanic stimulation (TS) and forskolin share a common mechanism. Three episodes of TS were delivered to saturate the LTP and, under this condition, forskolin still caused a further potentiation of the EPSPNMDA. Similarly, TS, delivered after the EPSPNMDA was enhanced by forskolin or dbcAMP, produced LTP. These results suggest that the long‐term enhancements of EPSPNMDA produced by TS and forskolin are different and thus do not support the hypothesis that activation of protein kinase A triggers LTP. {\circledC} 1995 Wiley‐Liss, Inc.",
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T1 - Cyclic adenosine‐3′,5′‐monophosphate potentiates the synaptic potential mediated by NMDA receptors in the amygdala

AU - Huang, C. C.

AU - Gean, Po-Wu

PY - 1995

Y1 - 1995

N2 - An in vitro slice preparation of rat amygdala was used to study the actions of forskolin and cyclic adenosine‐3′,5′‐monophosphate (cAMP) analogues on the N‐methyl‐D‐aspartate (NMDA) receptor‐mediated synaptic potential (EPSPNMDA). Intracellular recordings were made from basolateral amygdala neurons in the presence of 6‐cyano‐7‐nitroquinoxaline‐2,3‐dione (CNQX, 10μM) and picrotoxin (50 μM) to pharmacologically isolate the EPSPNMDA. Application of forskolin (25 μM) markedly and persistently potentiated the EPSPNMDA In contrast, the inactive forskolin analogue, 1,9‐dideoxy‐forskolin, failed to affect the EPSPNMDA significantly. Superfusion of dibutyryl‐cAMP (dbcAMP, 200 μM) for 15 min caused a transient depression of the amplitude of EPSPNMDA. The EPSPNMDA amplitude was reduced to 68 ± 3% of control (n = 10) 15 min after the application, restored to its control value within 25 min, and followed by a long‐term potentiation (LTP). Pretreating the slices with 8‐cyclopentyl‐1,3‐dipropylxanthine (DPCPX, 5 μM), a selective A1 receptor antagonist, blocked the transient depressive phase produced by dbcAMP. This result suggests that the transient depression induced by dbcAMP was likely due to the interaction of dbcAMP or its breakdown products with adenosine A1 receptors. To determine the site of action, we examined the effect of forskolin on the postsynaptic responses to exogenously applied NMDA. Forskolin potentiated the postsynaptic depolarization induced by NMDA, suggesting that the enhancement is mediated, at least in part, by a persistent upregulation of postsynaptic NMDA receptor‐operated conductances. Occlusion experiments were performed to examine whether the sustained enhancements of EPSPNMDA produced by tetanic stimulation (TS) and forskolin share a common mechanism. Three episodes of TS were delivered to saturate the LTP and, under this condition, forskolin still caused a further potentiation of the EPSPNMDA. Similarly, TS, delivered after the EPSPNMDA was enhanced by forskolin or dbcAMP, produced LTP. These results suggest that the long‐term enhancements of EPSPNMDA produced by TS and forskolin are different and thus do not support the hypothesis that activation of protein kinase A triggers LTP. © 1995 Wiley‐Liss, Inc.

AB - An in vitro slice preparation of rat amygdala was used to study the actions of forskolin and cyclic adenosine‐3′,5′‐monophosphate (cAMP) analogues on the N‐methyl‐D‐aspartate (NMDA) receptor‐mediated synaptic potential (EPSPNMDA). Intracellular recordings were made from basolateral amygdala neurons in the presence of 6‐cyano‐7‐nitroquinoxaline‐2,3‐dione (CNQX, 10μM) and picrotoxin (50 μM) to pharmacologically isolate the EPSPNMDA. Application of forskolin (25 μM) markedly and persistently potentiated the EPSPNMDA In contrast, the inactive forskolin analogue, 1,9‐dideoxy‐forskolin, failed to affect the EPSPNMDA significantly. Superfusion of dibutyryl‐cAMP (dbcAMP, 200 μM) for 15 min caused a transient depression of the amplitude of EPSPNMDA. The EPSPNMDA amplitude was reduced to 68 ± 3% of control (n = 10) 15 min after the application, restored to its control value within 25 min, and followed by a long‐term potentiation (LTP). Pretreating the slices with 8‐cyclopentyl‐1,3‐dipropylxanthine (DPCPX, 5 μM), a selective A1 receptor antagonist, blocked the transient depressive phase produced by dbcAMP. This result suggests that the transient depression induced by dbcAMP was likely due to the interaction of dbcAMP or its breakdown products with adenosine A1 receptors. To determine the site of action, we examined the effect of forskolin on the postsynaptic responses to exogenously applied NMDA. Forskolin potentiated the postsynaptic depolarization induced by NMDA, suggesting that the enhancement is mediated, at least in part, by a persistent upregulation of postsynaptic NMDA receptor‐operated conductances. Occlusion experiments were performed to examine whether the sustained enhancements of EPSPNMDA produced by tetanic stimulation (TS) and forskolin share a common mechanism. Three episodes of TS were delivered to saturate the LTP and, under this condition, forskolin still caused a further potentiation of the EPSPNMDA. Similarly, TS, delivered after the EPSPNMDA was enhanced by forskolin or dbcAMP, produced LTP. These results suggest that the long‐term enhancements of EPSPNMDA produced by TS and forskolin are different and thus do not support the hypothesis that activation of protein kinase A triggers LTP. © 1995 Wiley‐Liss, Inc.

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