Mechanisms of selective long-term potentiation of excitatory synapses in stratum oriens/alveus interneurons of rat hippocampal slices

Ouardouz, Mohamed; Lacaille, Jean‐Claude

doi:10.1152/jn.1995.73.2.810

Cited by 86 publications

(80 citation statements)

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“…Alternatively, we would favor the lack of some of the necessary components required for LTP induction. Our results contrast to those reported by Ouardouz and Lacaille (1995), who reported LTP in an unidentified st. oriens cell type. In these studies, tetanic stimulation was used to induce LTP, which does not allow a clear distinction between direct plasticity and passive propagation.…”

Section: Discussion Ltp In Oaiscontrasting

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: Discussion Ltp In Oaiscontrasting

confidence: 99%

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confidence: 99%

Long-Term Potentiation in Distinct Subtypes of Hippocampal Nonpyramidal Neurons

1996

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“…To examine whether LTP was a property of excitatory synapses specific to certain types of interneurons, the paradigm of TBS paired with depolarization was applied to interneurons in R͞LM (12,14) and to pyramidal cells. In addition, this series of experiments was conducted in ACSF containing normal (2 mM) Ca 2ϩ ͞Mg 2ϩ levels to verify that LTP was not inducible solely in elevated extracellular Ca 2ϩ ͞Mg 2ϩ levels.…”

Section: Resultsmentioning

confidence: 99%

“…Modeling studies suggest that plasticity at interneuron synapses is important for learning and recall by hippocampal neuronal networks (9). However, experimental evidence of long-term synaptic plasticity at input and͞or output synapses of hippocampal interneurons has been controversial (10)(11)(12)(13)(14)(15)(16). This uncertainty has been due, in part, to the heterogeneity of interneuron types present in the hippocampus and to the complexity of the network (6,17,18).…”

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confidence: 99%

A hebbian form of long-term potentiation dependent on mGluR1a in hippocampal inhibitory interneurons

Perez

Lacaille²

2001

Proc. Natl. Acad. Sci. U.S.A.

183

268

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Hippocampal inhibitory interneurons play important roles in controlling the excitability and synchronization of pyramidal cells, but whether they express long-term synaptic plasticity that contributes to hippocampal network function remains uncertain. We found that pairing postsynaptic depolarization with -burst stimulation induced long-term potentiation (LTP) of putative singlefiber excitatory postsynaptic currents in interneurons. Either postsynaptic depolarization or -burst stimulation alone failed to induce LTP. LTP was expressed as a decrease in failure rates and an increase in excitatory postsynaptic current amplitude, independent of N-methyl-D-aspartate receptors, and dependent on metabotropic glutamate receptors subtype 1a. LTP was induced specifically in interneurons in stratum oriens and not in interneurons of stratum radiatum͞lacunosum-moleculare. Thus, excitatory synapses onto specific subtypes of inhibitory interneurons express a new form of hebbian LTP that will contribute to hippocampal network plasticity.L ong-term potentiation (LTP) is the enduring increase in strength of synaptic transmission observed after tetanization of afferents (1). This synaptic plasticity has been extensively studied at glutamate synapses onto CA1 pyramidal cells of the hippocampus, where multiple forms of LTP can be induced by activation of N-methyl-D-aspartate receptors (NMDARs) (1, 2), metabotropic glutamate receptors (mGluRs) (3), and voltagedependent Ca 2ϩ channels (4, 5).The hippocampal neuronal network is also composed of inhibitory interneurons, which control the excitability and synchronization of projection cells (6-8). Modeling studies suggest that plasticity at interneuron synapses is important for learning and recall by hippocampal neuronal networks (9). However, experimental evidence of long-term synaptic plasticity at input and͞or output synapses of hippocampal interneurons has been controversial (10-16). This uncertainty has been due, in part, to the heterogeneity of interneuron types present in the hippocampus and to the complexity of the network (6,17,18). An important confounding factor has been that LTP induced at pyramidal cell synapses by tetanic stimulation of Schaffer collaterals can passively propagate to interneurons through recurrent excitatory collaterals of pyramidal cells and can be confused with direct potentiation of excitatory inputs onto interneurons (19). In addition, the apparent absence in interneurons of Ca 2ϩ -calmodulin-dependent protein kinase II and calcineurin (20), two major components of the Ca 2ϩ -signaling cascades involved in the induction of NMDAR-dependent LTP and depression, has been argued to support the lack of synaptic plasticity in interneurons (19,20). Recently, however, long-term depression has been observed at excitatory synapses onto interneurons after trains of high-frequency stimulation, suggesting that synaptic plasticity can indeed occur directly in interneurons (13,15).In the present study, the issue of long-term synaptic plasticity at synapses directly on i...

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“…These properties depend on receptor subunit composition (particularly the relative absence of GluR-B in interneurones and perhaps on the relative presence of GluR_D) and are regulated by posttranslational alternative splicing and RNA editing (Bochet et al 1994;Geiger et al 1995). We suggest that the functional reliability of the e i connection (which can even allow unitary EPSPs to elicit action potentials (Knowles & Schwartzkroin, 1981;Lacaille et al 1987;Miles, 1990)) takes on biological meaning because of the role interneurones play in high-frequency cortical oscillations, with the apparent necessity for interneurone doublets to occur during long-range synchrony of firing, and that usedependent increases in efficacy of excitatory synapses on interneurones (Taube & Schwartzkroin, 1987;Ouardouz & Lacaille, 1995) may be important for the same reason.…”

Section: Ampa Receptors On Interneuronesmentioning

confidence: 94%

Spatiotemporal patterns of γ frequency oscillations tetanically induced in the rat hippocampal slice

Whittington

Stanford

Colling

et al. 1997

The Journal of Physiology

210

204

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We used transverse and longitudinal rat hippocampal slices to study the synchronization of γ frequency (> 20 Hz) oscillations, across distances of up to 4.5 mm. γ oscillations were evoked in the CA1 region by tetanic stimulation at one or two sites simultaneously, and were associated with population spikes. Tetanic stimuli that were strong enough to induce oscillations were associated with depolarization of both pyramidal cells and interneurones, largely produced by activation of metabotropic glutamate receptors. Computer simulations of γ oscillations were also performed in a model with pyramidal cells and interneurones, arranged in a chain of five cell groups. This model had suggested previously that interneurone networks alone could generate synchronous γ oscillations locally, but that pyramidal cell firing, by inducing spike doublets in interneurones, was necessary for the occurrence of highly correlated oscillations with small phase lag (< 2.5 ms), in a distributed network possessing long axon conduction delays. In both experiment and model, pyramidal cell spikes occurred in phase with local population spikes, as did the first spike of the interneurone doublet. The conductance of the interneurone α‐amino‐3‐hydroxy‐5‐methyl‐4‐isoxazole propionic acid (AMPA) receptor‐mediated conductance was manipulated in the model, while the relation between oscillations at opposite ends of the chain was examined. When the conductance was large enough for doublet firing to be synaptically induced in interneurones, oscillation phase lags were < 2.25 ms across the chain. As predicted, experimental blockade of AMPA receptors resulted in increased phase lags between two sites oscillating simultaneously, compared with control conditions. Both in model and in experiment, when stimuli to the two ends of the network were slightly different, cross‐network synchronization occurred with a shorter phase lag at high frequencies than at lower frequencies. These data suggest that, while interneurone networks alone can generate locally synchronized γ oscillations, firing of pyramidal cells, and the synaptically induced doublet firing in interneurones, contribute to the stability and tight synchrony of the oscillations in distributed networks.

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Mechanisms of selective long-term potentiation of excitatory synapses in stratum oriens/alveus interneurons of rat hippocampal slices

Cited by 86 publications

References 0 publications

Long-Term Potentiation in Distinct Subtypes of Hippocampal Nonpyramidal Neurons

Long-Term Potentiation in Distinct Subtypes of Hippocampal Nonpyramidal Neurons

A hebbian form of long-term potentiation dependent on mGluR1a in hippocampal inhibitory interneurons

Spatiotemporal patterns of γ frequency oscillations tetanically induced in the rat hippocampal slice

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