Neocortical Long-Term Potentiation and Long-Term Depression: Site of Expression Investigated by Infrared-Guided Laser Stimulation

Eder, Matthias; Zieglgänsberger, W.; Dodt, Hans‐Ulrich

doi:10.1523/jneurosci.22-17-07558.2002

Cited by 31 publications

(36 citation statements)

References 70 publications

(84 reference statements)

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“…We used the Ca 2ϩ conductance and high glutamate affinity of the NMDAR to demonstrate that the photoreleased glutamate activated AMPARs that were confined to single spines. This resolution is at least an order of magnitude better than can be achieved in ex vivo hippocampal slices (3,4). Consistent with our conclusion, photolytically evoked EPSCs had amplitudes and kinetics comparable to those of miniature EPSCs generated by activation of single spines by a quantum of synaptically released glutamate.…”

Section: Discussionsupporting

confidence: 90%

“…Second, we observed that influx of Ca 2ϩ through NMDARs produced a higher intracellular [Ca 2ϩ ] in the confined, diffusionally restricted space of the spine head (34,35) as compared with dendritic shafts. Our ability to elicit potentiation with photolytic glutamate release, in contrast to previous attempts in ex vivo hippocampal slices (3,4), is thus likely to be caused by the better spatial resolution that can be achieved in cultured hippocampal slices. Larger, more diffuse sites of glutamate uncaging in ex vivo slices are likely to activate a much higher percentage of extrasynaptic shaft AMPARs.…”

Section: Discussionmentioning

confidence: 83%

“…Photolysis of caged glutamate offers the ability to directly control the strength, timing, and location of glutamate reaching postsynaptic receptors (4,14). In our experiments, an argon ion laser was fitted with UV optics to produce a continuous 300-mW beam of UV light at the 351-and 364-nm lines.…”

Section: Methodsmentioning

confidence: 99%

“…Some of these controversies are likely to stem from the use of conventional synaptic stimulation for studying LTP because the presynaptic nerve terminal is an unreliable source of glutamate. For example, several previous attempts to induce LTP with exogenous glutamate have not been successful (3,4), raising the possibility that there is a factor other than glutamate that is coreleased from nerve terminals with synaptic stimulation and is required for LTP induction. Likewise, changes in paired-pulse ratio (PPR) have been reported to accompany LTP in some studies and have been interpreted as evidence of a change in presynaptic release probability (5,6).…”

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confidence: 99%

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Long-term potentiation of exogenous glutamate responses at single dendritic spines

Bagal

Kao

Tang

et al. 2005

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

155

125

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Long-term increases in the strength of excitatory transmission at Schaffer collateral-CA1 cell synapses of the hippocampus require the insertion of new ␣-amino-3-hydroxy-5-methyl-4-isoxazolepropionate receptors (AMPARs) into the synapse, but the kinetics of this process are not well established. Using microphotolysis of caged glutamate to activate receptors at single dendritic spines in hippocampal CA1 cells, we report the long-lasting potentiation of AMPAR-mediated currents with only a single pairing of photoreleased glutamate and brief postsynaptic depolarization. This potentiation was N-methyl-D-aspartate receptor (NMDAR)-dependent and was reversed with low-frequency photostimulation in an NMDAR-dependent manner, suggesting that it is mediated by the same mechanism(s) as conventional synaptic long-term potentiation. Potentiation of photolytic responses developed rapidly in a stepwise manner after a brief and variable delay (<60 s) at spines, but could not be induced at extrasynaptic sites on the dendritic shaft. Potentiation was accompanied by a concomitant decrease in postsynaptic, polyamine-dependent paired-pulse facilitation of the photolytic currents, indicating that a change in the subunit composition of the AMPARs underlying the response contributed to the potentiation. These changes are consistent with an increase in the proportion of GluR2-containing AMPARs in the spine head. These results demonstrate that activation of postsynaptic glutamate receptors by glutamate is not only necessary, but sufficient, for the induction of NMDAR-dependent long-term potentiation and reveal additional aspects of its expression.synaptic plasticity ͉ hippocampus ͉ plasticity L ong-term plasticity of excitatory synaptic transmission that depends on N-methyl-D-aspartate receptor (NMDAR) activation is likely to underlie learning and memory formation (1, 2). Despite an abundance of knowledge about long-term potentiation (LTP), considerable uncertainty and controversy about the mechanisms of LTP induction and expression persist. Some of these controversies are likely to stem from the use of conventional synaptic stimulation for studying LTP because the presynaptic nerve terminal is an unreliable source of glutamate. For example, several previous attempts to induce LTP with exogenous glutamate have not been successful (3, 4), raising the possibility that there is a factor other than glutamate that is coreleased from nerve terminals with synaptic stimulation and is required for LTP induction. Likewise, changes in paired-pulse ratio (PPR) have been reported to accompany LTP in some studies and have been interpreted as evidence of a change in presynaptic release probability (5, 6). Matsuzaki et al. (7) have demonstrated that potentiation of glutamate responses can be achieved with repeated photorelease from caged glutamate targeted to dendritic spines, suggesting that activation of synaptic glutamate receptors is critical.The ability to study LTP with exogenous glutamate offers a powerful tool for answering fundamental questions...

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Section: Discussionsupporting

confidence: 90%

Section: Discussionmentioning

confidence: 83%

Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 99%

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Long-term potentiation of exogenous glutamate responses at single dendritic spines

Bagal

Kao

Tang

et al. 2005

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

155

125

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“…There is evidence for both presynaptic (Torii et al 1997) and postsynaptic (Eder et al 2002) components to neocortical LTD. Normalized CV 2 /amplitude plots for individual experiments in the present study mostly had trajectories steeper than the unity line, suggesting a similar predominantly presynaptic mechanism to the LTD, but again there was considerable heterogeneity between individual plots with a number of lines above the diagonal (Fig. 5B).…”

Section: Ltd Also Occurs Predominantly By a Reduction In Quantal Releasementioning

confidence: 99%

Presynaptic Efficacy Directs Normalization of Synaptic Strength in Layer 2/3 Rat Neocortex After Paired Activity

Hardingham

Hardingham²,

Fox³

et al. 2007

Journal of Neurophysiology

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Hardingham NR, Hardingham GE, Fox KD, Jack JB. Presynaptic efficacy directs normalization of synaptic strength in layer 2/3 rat neocortex after paired activity. J Neurophysiol 97: [2965][2966][2967][2968][2969][2970][2971][2972][2973][2974][2975] 2007. First published January 31, 2007; doi:10.1152/jn.01352.2006. Paired neuronal activity is known to induce changes in synaptic strength that result in the synapse in question having different properties to unmodified synapses. Here we show that in layer 2/3 excitatory connections in young adult rat cortex paired activity acts to normalize the strength and quantal parameters of connections. Paired action potential firing produces long-term potentiation in only a third of connections, whereas a third remain with their amplitude unchanged and a third exhibit long-term depression. Furthermore, the direction of plasticity can be predicted by the initial strength of the connection: weak connections potentiate and strong connections depress. A quantal analysis reveals that changes in synaptic efficacy were predominantly presynaptic in locus and that the key determinant of the direction and magnitude of synaptic modification was the initial release probability (P r ) of the synapse, which correlated inversely with change in P r after pairing. Furthermore, distal synapses also exhibited larger potentiations including postsynaptic increases in efficacy, whereas more proximal inputs did not. This may represent a means by which distal synapses preferentially increase their efficacy to achieve equal weighting at the soma. Paired activity thus acts to normalize synaptic strength, by both pre-and postsynaptic mechanisms. I N T R O D U C T I O NPaired bursts of pre-and postsynaptic action potentials (APs) are believed to be a physiological mechanism of plasticity at many central synapses (e.g., Markram and Tsodyks 1996;Paulsen and Sejnowski 2000). Paired recordings from hippocampal cultures and cortical slices suggest that the direction of synaptic plasticity that paired activity produces is dependent on the order of the presynaptic and postsynaptic spikes (Bi and Poo 1998;Markram et al. 1997). Pairing presynaptic spikes shortly before postsynaptic spikes produces long-term potentiation (LTP), whereas pairing postsynaptic spikes before presynaptic spikes produces long-term depression (LTD), with less temporal spike constraint (Bi and Poo 1998;Feldman 2000;Markram et al. 1997). The initial strength of the synapse may also dictate whether a synapse potentiates, with weaker synapses potentiating preferentially over stronger ones (Bi and Poo 1998). The relative timing of the presynaptic and postsynaptic spikes could be reflected by both the amplitude and kinetics of calcium transients in spines, with larger, more transient calcium signals producing LTP and smaller, longer-lasting ones producing LTD (Cormier et al. 2001;Hansel et al. 1997;Ismailov et al. 2004;Koester and Sakmann 1998;Yang et al. 1999).Pairing presynaptic before postsynaptic spikes has been shown to induce both LTP and...

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A New Inorganic Photolabile Protecting Group for Highly Efficient Visible Light GABA Uncaging

et al. 2007

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Neocortical Long-Term Potentiation and Long-Term Depression: Site of Expression Investigated by Infrared-Guided Laser Stimulation

Cited by 31 publications

References 70 publications

Long-term potentiation of exogenous glutamate responses at single dendritic spines

Long-term potentiation of exogenous glutamate responses at single dendritic spines

Presynaptic Efficacy Directs Normalization of Synaptic Strength in Layer 2/3 Rat Neocortex After Paired Activity

A New Inorganic Photolabile Protecting Group for Highly Efficient Visible Light GABA Uncaging

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