Evaluation of long-term potentiation of small compound and unitary EPSPs at the hippocampal CA3-CA1 synapse

Friedlander, M. J.; Sayer, RJ; Redman, S. J.

doi:10.1523/jneurosci.10-03-00814.1990

Cited by 38 publications

(16 citation statements)

References 52 publications

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“…LTP of unitary EPSPs could not be induced with high-frequency tetanization of a single CA3 cell in our experiments, consistent with results in ex vivo hippocampal slices (6). The failure of this pattern of presynaptic activity to induce potentiation cannot be attributed to an inability of these synapses to express LTP, as suggested previously (6), because synchronous pairing of the same synapses reliably induced a persistent increase in the unitary EPSP amplitude.…”

Section: Discussionsupporting

confidence: 92%

“…Potentiation of these compound EPSPs persisting >4 min was only obtained when the compound EPSP had an amplitude >4 mV. Previously reported data from ex vivo hippocampal slices are consistent with-this conclusion (4,6). Unitary Schaffer collateral EPSPs in hippocampal slice cultures have a mean amplitude of -1 mV (13).…”

Section: Discussionsupporting

confidence: 74%

“…The associative induction of LTP at connections between pairs of hippocampal CA3 and CAl neurons has been observed when low-frequency stimulation of the presynaptic neuron is paired with a maintained postsynaptic depolarization (5), but was not observed with high-frequency presynaptic tetani alone (6). The failure to observe tetanus-induced LTP in the latter study could result either because unitary inputs are simply too weak to engage the biochemical machinery responsible for potentiation or because of something intrinsic to the individual synapses studied, such as an inherent nonplasticity.…”

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confidence: 99%

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Cooperative interactions in the induction of long-term potentiation and depression of synaptic excitation between hippocampal CA3-CA1 cell pairs in vitro.

Debanne

Gähwiler

Thompson

1996

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

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The requirement for cooperative interactions between multiple synaptic inputs in the induction of long-term potentiation (LTP) and long-term depression (LTD) has been tested at Schaffer collateral synapses with paired recordings from monosynaptically coupled CA3-CA1 cell pairs in rat hippocampal slice cultures. Tetanization of single presynaptic neurons at 50 Hz (repeated 5-7 times for 300-500 ms each) induced only a transient potentiation (<3 min) of excitatory postsynaptic potentials (EPSPs). Persistent potentiation (>15 min) was induced only when single presynaptic action potentials were synchronously paired with directly induced postsynaptic depolarizing pulses (repeated 50-100 times). Tetanus- Persistent changes in the strength of the synaptic connections between cells are likely to underlie learning and memory formation. Long-term potentiation (LTP) and long-term depression (LTD) of excitatory synaptic transmission are two alternative forms of synaptic plasticity, providing the best models of these cellular processes. The experimental protocols typically used to induce LTP and LTD, in particular the stimulation of large numbers of fibers to evoke compound synaptic responses, have proven invaluable for studying the fundamental mechanisms by which these phenomena are generated, but may have little relevance to the patterns of activity occurring in the brain during learning and memory. The associative induction of LTP at connections between pairs of hippocampal CA3 and CAl neurons has been observed when low-frequency stimulation of the presynaptic neuron is paired with a maintained postsynaptic depolarization (5), but was not observed with high-frequency presynaptic tetani alone (6). The failure to observe tetanus-induced LTP in the latter study could result either because unitary inputs are simply too weak to engage the biochemical machinery responsible for potentiation or because of something intrinsic to the individual synapses studied, such as an inherent nonplasticity. To distinguish between these possibilities, the relative ability of tetanization and synchronous pairing to induce LTP must be compared on the same synaptic connections.The induction of LTD in the CAl region of the hippocampus also requires NMDA receptor activation and increases in postsynaptic Ca2+ (7-9). LTD can display associative properties (10), and it has recently been concluded that cooperative interactions are required for its induction (11). This conclusion is, however, difficult to reconcile with the successful induction of homosynaptic LTD when only one or a few synapses are stimulated extracellularly (12).We MATERIALS AND METHODS Hippocampal slice cultures were prepared and maintained as described (15). In brief, the hippocampi were dissected from 5-to Abbreviations: EPSP, excitatory postsynaptic potential; IPSP, inhibitory postsynaptic potential; LTP, long-term potentiation; LTD, longterm depression; NMDA, N-methyl-D-aspartate.

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Section: Discussionsupporting

confidence: 92%

Section: Discussionsupporting

confidence: 74%

mentioning

confidence: 99%

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Cooperative interactions in the induction of long-term potentiation and depression of synaptic excitation between hippocampal CA3-CA1 cell pairs in vitro.

Debanne

Gähwiler

Thompson

1996

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

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“…This hypothesis is supported by the observation that, following the induction of LTP and subsequent pharmacological blockade of AMPA receptors, the residual NMDA receptor-mediated component of synaptic responses shows only a small magnitude of potentiation compared with that exhibited by the AMPA receptor-mediated component. This finding is consistent with the supposition that NMDA receptor binding in the synapse is near saturation during each release of transmitter as a result of the high affinity of the receptor for glutamate (Herron et al 1986;Harris and Cotman 1986;Friedlander et al 1990;Grover and Teyler 1990;Zalutsky and Nicoll 1990). More recently, however, the view that LTP expression is mediated exclusively by changes in AMPA receptors has been challenged by us and other who have demonstrated that the NMDA component can express LTP with a magnitude equivalent to that expressed by the AMPA component (Xie et al 1992a,b;O'Connor et al 1995).…”

Section: Introductionsupporting

confidence: 91%

Differential expression of short-term potentiation by AMPA and NMDA receptors in dentate gyrus.

Xie

Barrionuevo²,

Berger³

1996

Learning & Memory

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Both a-amino-3-hydroxy-5-methyl-4-isoxazole propionate (AMPA) and N-methyl-n-aspartate (NMDA) glutamatergic receptor subtypes in hippocampus have been shown to express long-term potentiation (LTP), a form of synaptic modification believed to be involved in memory formation. Because of their postsynaptic localization, any differential expression of LTP by the two receptor subtypes would strongly support the existence of a postsynaptic mechanism of LTP expression. In this study, electrophysiological recordings from dentate granule cells were used to compare the potentiation of AMPA and NMDA receptor-mediated responses occurring during the initial phase of LTP, typically identified as STP. Results revealed that high-frequency stimulation (HFS) of perforant path afferents induces a robust STP of both AMPA and NMDA receptor-mediated components of granule cell EPSPs (referred to as AMPA STP and NMDA STP, respectively). Although STP for both receptor subtypes decayed to an aysymptotic, steady-state level of LTP and could be induced repetitively, there were substantial differences in several aspects of AMPA and NMDA STP dynamics. STP of the AMPA receptor reached its peak magnitude -30 sec after HFS and decayed with a time constant of -6 min. In contrast, peak 3Corresponding author. magnitude of NMDA STP always appeared immediatly after HFS and decayed with a time constant of only 1 min. Single-pulse stimulation of perforant path afferents paired with postsynaptic depolarization also induced LTP of both AMPA and NMDA components. When this induction paradigm was used, however, only the AMPA component showed significant STP. Our results demonstrate that AMPA and NMDA receptors exhibit markedly different degrees of activity-dependent, short-term modifiability, with the possibility that STP of the NMDA receptor reflects primarily post-tetanic potentiation (PTP). In addition, our results strongly suggest that the mechanisms underlying STP of the AMPA receptor are postsynaptic in origin.

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“…We compared how the parameter estimates depend on stimulus voltage to ascertain that the vesicular dynamics are not affected by the interactions between collaterals or boutons. This is relevant because at guinea pig CA3-CA1 synapses, the induction of LTP depends on how many synapses are stimulated (Friedlander et al 1990). The initial EPSC amplitudes expectedly increase with greater stimulus voltage (Fig.…”

Section: How the Parameters Of A Two Pool Vesicular System Affect Synmentioning

confidence: 99%

Synaptic activity slows vesicular replenishment at excitatory synapses of rat hippocampus

Bui

Glavinović

2012

Cogn Neurodyn

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Short-term synaptic depression mainly reflects the depletion of the readily releasable pool (RRP) of quanta. Its dynamics, and especially the replenishment rate of the RRP, are still not well characterized in spite of decades of investigation. Main reason is that the vesicular storage and release system is treated as time-independent. If it is time-dependent all parameters thus estimated become problematic. Indeed the reports about how prolonged stimulation affects the dynamics are contradictory. To study this, we used patterned stimulation on the Schaeffer collateral fiber pathway and model-fitting of the excitatory post-synaptic currents (EPSC) recorded from CA1 neurons in rat hippocampal slices. The parameters of a vesicular storage and release model with two pools were estimated by minimizing the squared difference between the ESPC amplitudes and simulated model output. This yields the 'basic' parameters (release coupling, replenishment coupling and RRP size) that underlie the 'derived' and commonly used parameters (fractional release and replenishment rate). The fractional release increases when [Ca ?? ] o is raised, whereas the replenishment rate is [Ca ?? ] o independent. Fractional release rises because release coupling increases, and the RRP becomes less able to contain quanta. During prolonged stimulation, the fractional release remains generally unaltered, whereas the replenishment rate decreases down to *10 % of its initial value with a decay time of *15 s, and this decrease in the replenishment rate significantly contributes to synaptic depression. In conclusion, the fractional release is [Ca ?? ] odependent and stimulation-independent, whereas the replenishment rate is [Ca ?? ] o -independent and stimulation-dependent.

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Evaluation of long-term potentiation of small compound and unitary EPSPs at the hippocampal CA3-CA1 synapse

Cited by 38 publications

References 52 publications

Cooperative interactions in the induction of long-term potentiation and depression of synaptic excitation between hippocampal CA3-CA1 cell pairs in vitro.

Cooperative interactions in the induction of long-term potentiation and depression of synaptic excitation between hippocampal CA3-CA1 cell pairs in vitro.

Differential expression of short-term potentiation by AMPA and NMDA receptors in dentate gyrus.

Synaptic activity slows vesicular replenishment at excitatory synapses of rat hippocampus

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