Inhibition of protein kinase activity enhances long-term potentiation of hippocampal IPSPs

Xie, Zheng; Sastry, B.R.

doi:10.1097/00001756-199107000-00009

Cited by 19 publications

(13 citation statements)

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“…In this scenario, after LTP induction, the interplay between a potentiated EPSP, which will facilitate pyramidal cell firing, and the consequent passive propagation of LTP onto a vertical OAI will result in a potentiation of a late IPSP component onto pyramidal neurons, which may act to prevent the occurrence of prolonged spike discharges. However, it has been shown previously that even when interneuron afferents demonstrate LTP, the IPSP onto pyramidal cells could be depressed postsynaptically (Morishita and Sastry, 1991;Xie and Sastry 1991;Stelzer et al, 1994), adding another level of complexity to the network effects of LTP induction.…”

Section: Ltp In Interneurons and Network Effectsmentioning

confidence: 99%

“…Therefore, the possibility of additional synaptic plasticity occurring in nonpyramidal cells would greatly increase both the power and the level of complexity of signal processing in the CA1 subfield. Indeed, several reports have shown that after tetanic stimulation, changes occur in (1) evoked nonpyramidal cell firing probability (Buzsaki and Eidelberg, 1982), (2) IPSP amplitudes recorded on pyramidal cells (Xie and Sastry, 1991;Morishita and Sastry, 1991), and (3) EPSP or EPSC amplitudes recorded in interneurons (Taube and Schwartzkroin, 1987;Stelzer et al, 1994;Ouardouz and Lacaille, 1995). In addition, however, synaptic depression occurring at the Schaffer collateral-pyramidal neuron synapses can "passively propagate" to interneurons of the st. oriens/alveus and influence the excitatory drive of these cells (Maccaferri and McBain, 1995).…”

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confidence: 99%

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Long-Term Potentiation in Distinct Subtypes of Hippocampal Nonpyramidal Neurons

1996

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We have investigated NMDA receptor-dependent long-term potentiation (LTP) in distinct subtypes of nonpyramidal neurons of the CA1 hippocampus using induction protocols that permitted the differentiation between a direct form of LTP and plasticity resulting simply from the "passive propagation" of LTP occurring on CA1 pyramidal neurons. Two types of stratum (st.) oriens/ alveus interneurons received passive propagation of synaptic potentiation via the recurrent collaterals of CA1 pyramidal cells, but neither subtype possessed direct plasticity. In st. radiatum, two distinct classes of cells were observed: st. radiatum interneurons that showed neither direct nor propagated forms of synaptic plasticity, and "giant cells" for which EPSPs were robustly potentiated after a pairing protocol. This potentiation is similar to the LTP described in pyramidal cells, and its induction requires NMDA receptor activation. Thus, a large heterogeneity of synaptic plasticity exists in morphologically distinct neurons and suggests that complex changes in the CA1 network properties will occur after the induction of LTP.Key words: hippocampus; interneurons; LTP; plasticity; GABAergic; CA1 Synaptic plasticity of the CA1 subfield of the rat hippocampus has been extensively studied and characterized in pyramidal cells (Bliss and Collingridge, 1993;Malenka and Nicoll, 1993;Lisman, 1994). Although many issues still are under debate (Kullmann and Siegelbaum, 1995), the mechanisms involved in the induction of long-term potentiation (LTP) and long-term depression (LTD) have been elucidated (Bliss and Collingridge, 1993;Malenka, 1994). Both forms of plasticity require the activation of postsynaptic NMDA receptors (NMDARs) and an elevation of intracellular calcium levels (Collingridge et al., 1983; Malenka et al., 1988, Dudek andBear, 1992;Mulkey and Malenka, 1992), which lead to phosphorylation or dephosphorylation processes (Malinow et al., 1988;Malenka et al., 1989;Mulkey at al, 1993;Lisman, 1994).At the level of the hippocampal network, the net flow of information in the CA1 region is strongly modulated by the action of the nonpyramidal neurons, the cell bodies of which are distributed throughout all layers of the hippocampus (Lacaille et al., 1987(Lacaille et al., , 1989 Lacaille and Schwartzkroin, 1988a,b;Buhl et al., 1994;Sik et al., 1994Sik et al., , 1995Cobb et al., 1995;Maccaferri and McBain, 1995) (for review, see Freund and Buzsaki, 1996). The vast majority (ϳ90%) of these cells have been shown to be glutamate decarboxylase (GAD)-positive inhibitory interneurons (Woodson et al., 1989), the axons of which target different domains of the pyramidal cell dendritic tree (Gulyás et al., 1993;Buhl et al., 1994;Sik et al., 1995). Therefore, the possibility of additional synaptic plasticity occurring in nonpyramidal cells would greatly increase both the power and the level of complexity of signal processing in the CA1 subfield. Indeed, several reports have shown that after tetanic stimulation, changes occur in (1) evoked nonpyramidal cell f...

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Section: Ltp In Interneurons and Network Effectsmentioning

confidence: 99%

mentioning

confidence: 99%

Long-Term Potentiation in Distinct Subtypes of Hippocampal Nonpyramidal Neurons

1996

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“…Inhibitory postsynaptic potentials (IPSPs) in pyramidal cells can be depressed (Haas and Rose, 1982) or enhanced (Abraham et al, 1987;Taube and Schwartzkroin, 1987;Perez and Lacaille, 1995;Grunze et al, 1996) by tetanization. The strengthened IPSPs may result in part from the potentiation of GABAergic synapses onto pyramidal cells (Xie and Sastry, 1991;Xie et al, 1995), but enhanced excitatory synaptic drive onto local inhibitory neurons may also contribute significantly. Excitatory postsynaptic responses in basket cells in the pyramidal layer (Stelzer et al, 1994;Taube and Schwartzkroin, 1987) and in cells located near the alveus in stratum oriens (Stelzer et al, 1994;Ouardouz and Lacaille, 1995) are enhanced by high-frequency stimulation in vitro.…”

Section: Introductionmentioning

confidence: 99%

Effects of GABAA inhibition on the expression of long-term potentiation in CA1 pyramidal cells are dependent on tetanization parameters

1998

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“…( Morishita and Sastry, 1991;Xie and Sastry, 1991) have described LTP of GABA,-and GABA,-mediated IPSPs in CA1 pyramidal cells. This LTP is enhanced, rather than reduced, by LTP of IPSCs was not prevented by hyperpolarizing granule cell chelation of intracellular calcium and blockade of protein kinase C, making it unlikely that it is NMDA receptor dependent.…”

Section: Discussionmentioning

confidence: 99%

“…, hippocampal CA1 neurons (Morishita and Sastry, 199 I ;Xie and Sastry, 1991) and cerebellar Purkinje cells (Kano et al, 1992) following tetanic stimulation of excitatory inputs to the same cells. It is unclear yet whether the LTP of inhibitory circuits is a common phenomenon inducible in other brain areas as well, and very little is known concerning the factors that modulate LTP induction in the inhibitory circuitry.…”

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confidence: 99%

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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Inhibition of protein kinase activity enhances long-term potentiation of hippocampal IPSPs

Cited by 19 publications

References 0 publications

Long-Term Potentiation in Distinct Subtypes of Hippocampal Nonpyramidal Neurons

Long-Term Potentiation in Distinct Subtypes of Hippocampal Nonpyramidal Neurons

Effects of GABAA inhibition on the expression of long-term potentiation in CA1 pyramidal cells are dependent on tetanization parameters

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

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