Synaptic disinhibition during maintenance of long-term potentiation in the CA1 hippocampal subfield.

Stelzer, Armin; Simon, Gábor; Kovács, Gábor G.; Rai, Rabindra

doi:10.1073/pnas.91.8.3058

Cited by 86 publications

(63 citation statements)

References 35 publications

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“…However, the present results suggest that L-LTP may be pathway dependent. In fact, in several original LTP studies in the hippocampus, the failure of LTP induction has been reported (between 57.9 and 85.2% success rate) (Chavez-Noriega et al, 1990;Clark and Collingridge, 1995;Malinow and Tsien, 1990;Stelzer et al, 1994;Wheal et al, 1983). Second, we found that L-LTP induction triggered the recruitment of cortical circuit.…”

Section: Discussionmentioning

confidence: 52%

Pharmacological Rescue of Cortical Synaptic and Network Potentiation in a Mouse Model for Fragile X Syndrome

Chen

Song

et al. 2014

Neuropsychopharmacol

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Fragile X syndrome, caused by the mutation of the Fmr1 gene, is characterized by deficits of attention and learning ability. In the hippocampus of Fmr1 knockout mice (KO), long-term depression is enhanced whereas long-term potentiation (LTP) including late-phase LTP (L-LTP) is reduced or unaffected. Here we examined L-LTP in the anterior cingulate cortex (ACC) in Fmr1 KO mice by using a 64-electrode array recording system. In wild-type mice, theta-burst stimulation induced L-LTP that does not occur in all active electrodes/ channels within the cingulate circuit and is typically detected in B75% of active channels. Furthermore, L-LTP recruited new responses from previous inactive channels. Both L-LTP and the recruitment of inactive responses were blocked in the ACC slices of Fmr1 KO mice. Bath application of metabotropic glutamate receptor 5 (mGluR5) antagonist or glycogen synthase kinase-3 (GSK3) inhibitors rescued the L-LTP and network recruitment. Our results demonstrate that loss of FMRP will greatly impair L-LTP and recruitment of cortical network in the ACC that can be rescued by pharmacological inhibition of mGluR5 or GSK3. This study is the first report of the network properties of L-LTP in the ACC, and provides basic mechanisms for future treatment of cortex-related cognitive defects in fragile X patients.

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Section: Discussionmentioning

confidence: 52%

Pharmacological Rescue of Cortical Synaptic and Network Potentiation in a Mouse Model for Fragile X Syndrome

Chen

Song

et al. 2014

Neuropsychopharmacol

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“…Moreover, exogenous GABA when paired with postsynaptic depolarization also produced LTT. LTT contributes to pairing-induced LTP but differs from changes previously observed for GABAergic synapses after LTP (23)(24)(25). Both LTT and pairing-induced LTP were prevented by 1 ,uM anandamide.…”

Section: Resultsmentioning

confidence: 64%

Long-term synaptic transformation of hippocampal CA1 gamma-aminobutyric acid synapses and the effect of anandamide.

Collin

Devane²,

Dahl³

et al. 1995

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

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Evidence is presented for a distinctive type of hippocampal synaptic modification [previously described for a molluscan y-aminobutyric acid (GABA) synapse after paired pre-and postsynaptic excitation]: transformation of GABA-mediated synaptic inhibition into synaptic excitation. This transformation persists with no further paired stimulation for 60 min or longer and is termed long-term transformation. Long-term transformation is shown to contribute to pairing-induced long-term potentiation but not to long-term potentiation induced by presynaptic stimulation alone. This synaptic LTT is shown to contribute significantly to pairing-induced LTP but not to tetanus-induced (i.e., not paired with depolarization) LTP. The same synaptic transformation was previously identified for the GABA synapses of the visual-vestibular sensory cells of the snail Hermissenda (4).MATERIALS AND METHODS The slicing procedure has been described (5). In brief, recordings were obtained in 400-,um-thick transverse hippocampal slices of adult (150 g) male Sprague-Dawley rats. Slices were maintained at 34-35°C in a submersion chamber perfused with artificial cerebrospinal fluid (126 mM NaCl/3.0 mM KCl/1.25 mM NaH2PO4/24 mM NaHCO3/2.0 mM MgSO4/2.0 mM CaCl2/10 mM glucose). The flow rate was adjusted to 1.5 ml-min-1 and was bubbled with 95% 02/5% CO2. Intracellular recordings were obtained with micropipettes filled with 1 M KAc/l mM KCl and with a resistance of 60-80 Mfl. Intracellular recordings from the CAl neurons were amplified with an Axoclamp 2A amplifier. Data were digitized at 1-10 KHz and stored in magnetic tape for later analysis using the PCLAMP computer program. Bipolar tungsten electrodes were placed at the stratum radiatum to stimulate the Schaeffer collaterals or very close to the intracellular electrode to directly stimulate the basket interneurons at the pyramidal layer. RESULTSExogenous GABA application to CAl pyramidal cell somata ( Fig. 1 A and B) elicited a hyperpolarizing response. It was often possible to discriminate two components within the GABA-elicited hyperpolarization. An initial fast-hyperpolarizing component (Fig. 2A1 Left, red trace) reversed at about -70 mV (±5) (Fig. 2 Al and C). This fast component was blocked by furosemide (0.8 mM), GABAA receptor-mediated Cl-pump blocker (7) and bicuculline methiodide (BMI), a GABAA receptor blocker (Fig. 2 A2). These observations are consistent with previous findings (6,8,9), and can be explained by GABAA receptor-mediated opening of Cl-channels (10, 11). A later, slower, and somewhat variable hyperpolarizing component (Fig. 2A1, red trace) was blocked by phaclofen ( Fig. 2 A2) but not by furosemide and can be explained by GABAB receptor-mediated opening of K+ channels (12, 13). The cell-membrane voltage changes to repetitive hyperpolarizing current pulses during the GABA responses were reduced, indicating that GABA applications caused a net increase in membrane conductance.GABA application paired with postsynaptic depolarization (Fig. 1B2) was initially followed by ...

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“…For instance, either LTD of IPSPs or a change in excitability likely underlies the cases of E-S potentiation that have been reported to occur in the absence of LTP (Bliss and Lomo, 1973;Andersen et al, 1980;Abraham et al, 1985;Taube and Schwartzkroin, 1988;Jester et al, 1995). Nonetheless, whereas E-S potentiation is reliably observed in the hippocampus after tetanus-LTP, studies addressing the issue of tetanus-induced plasticity in the inhibitory branch of the disynaptic circuit have reported a variety of results (McLean et al, 1996;McBain and Maccaferri, 1997;McBain et al, 1999;Gaiarsa et al, 2002), ranging from no changes in inhibition , to LTP of IPSPs (Kairiss et al, 1987;Stelzer et al, 1994;Ouardez and Lacaille, 1995;Xie et al, 1995;Maccaferri and McBain, 1996;Cowan et al, 1998;Shew et al, 2000;Perez et al, 2001) to LTD of IPSPs (McMahon and Kauer, 1997;Lu et al, 2000;Chevaleyre and Castillo, 2003). Although we argue that inhibitory plasticity does not contribute to E-S potentiation when using a relatively mild pairing protocol, it may play a significant role under other induction protocols that more strongly engage the inhibitory circuitry.…”

Section: Mechanisms Underlying E-s Potentiationmentioning

confidence: 99%

Timing and Balance of Inhibition Enhance the Effect of Long-Term Potentiation on Cell Firing

Marder

Buonomano²

2004

J. Neurosci.

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The role of a neuron in neural processing is ultimately determined by whether or not it fires an action potential in a given context. Studies on synaptic plasticity have focused primarily on changes in EPSPs, and not on whether plasticity translates into changes in firing. However, this issue has been addressed by examining EPSP-spike (E-S) potentiation, which enhances the ability of an EPSP of a fixed slope to elicit spikes after long-term potentiation (LTP). Although LTP is thought to underlie learning and memory, E-S potentiation could play an equally important role by potentiating the neuronal input-output function. Here, we used a combined experimental and theoretical approach to examine both the mechanisms underlying E-S potentiation as well as the role of inhibition in shaping the input-output function of neurons. Whereas previous studies examined tetanus-LTP, in which inhibitory synapses may have undergone plasticity, here we examined pairing-induced associative LTP. We determined that although intact inhibition was necessary for pairinginduced E-S potentiation, inhibitory plasticity was not. We further established using computer simulations that a primary mechanism of E-S potentiation was a change in the relative recruitment and latency of inhibitory neurons. Although these studies do not exclude the presence of additional mechanisms of E-S potentiation that may be engaged depending on the induction protocol, they do establish that under intact pharmacology, LTP of the Schaffer collateral to CA1 pyramidal neuron synapses will produce E-S potentiation as a result of changes in the balance and timing of excitation and inhibition.

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Synaptic disinhibition during maintenance of long-term potentiation in the CA1 hippocampal subfield.

Cited by 86 publications

References 35 publications

Pharmacological Rescue of Cortical Synaptic and Network Potentiation in a Mouse Model for Fragile X Syndrome

Pharmacological Rescue of Cortical Synaptic and Network Potentiation in a Mouse Model for Fragile X Syndrome

Long-term synaptic transformation of hippocampal CA1 gamma-aminobutyric acid synapses and the effect of anandamide.

Timing and Balance of Inhibition Enhance the Effect of Long-Term Potentiation on Cell Firing

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