Priming of short-term potentiation and synaptic tagging/capture mechanisms by ryanodine receptor activation in rat hippocampal CA1

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The consolidation process from short-to long-term memory depends on the type of stimulation received from a specific neuronal network and on the cooperativity and associativity between different synaptic inputs converging onto a specific neuron. We show here that the plasticity thresholds for inducing LTP are different in proximal and distal compartments of apical dendrites. In addition, we show interactions between the proximal and distal compartments of the apical dendrites by providing evidence that even a subthreshold stimulus can activate plasticity-related proteins, such as PKMz, enabling associativity between two distinct dendritic compartments in apical dendrites to occur.CA1 pyramidal neurons are the major output of the hippocampus (Amaral and Witter 1989) and activity-dependent changes such as long-term potentiation (LTP) and long-term depression (LTD) at CA1 synapses are important cellular correlates of learning and memory. The strength of CA1 excitatory synapses in the hippocampus is not fixed, but can change depending upon their activation pattern (Zucker 1999;Zucker and Regehr 2002). For example, it is well documented that different stimulation protocols can induce distinct forms of plasticity in the distal part of CA1 pyramidal neurons (Sajikumar et al. 2005a). The early and late forms of LTP/LTD can be induced by weak and strong stimulation paradigms (Malenka and Bear 2004). These protocols exert their action by activating different subcellular signaling pathways. One of the most important pathways in this respect involves the activation of an atypical PKC isotype, PKMz (PKMz) by a strong tetanization protocol (Sacktor 2008). PKMz is critical not only for the maintenance of late-LTP, but also for the associative processes of LTP, i.e., synaptic tagging and capture (STC) (Ling et al. 2002;Sajikumar et al. 2005b). STC is a mechanism that explains how weakly activated synapses express long-term plasticity (expression of late-LTP in a weakly tetanized synaptic input) by capturing plasticity-related proteins (PRPs) from a nearby strong synaptic input (Young and Nguyen 2005;Sajikumar et al. 2009). Recently, it has been reported that STC is compartment restricted to apical or basal dendrites of CA1 pyramidal neurons (Alarcon et al. 2006;Sajikumar et al. 2007;Sajikumar and Korte 2011). The consequence of such a model is that one distinct form of synaptic plasticity induced and expressed in a certain compartment will not affect other compartments (Alarcon et al. 2006;Sajikumar et al. 2007;Sajikumar and Korte 2011).A typical pyramidal neuron consists of apical and basal dendrites differing in their morphology, biophysical characters, and in their LTP induction and expression mechanisms (Arai et al. 1994;Haley et al. 1996;Kramar and Lynch 2003). The neuromodulatory requirements for inducing long-lasting plasticity in basal and apical dendrites is different: for instance, in apical dendrites dopamine receptor activation by dopamine or its agonists can induce slow onset potentiation lasting 6 h (Navakkode et ...

supporting

confidence: 92%

mentioning

confidence: 99%

Different compartments of apical CA1 dendrites have different plasticity thresholds for expressing synaptic tagging and capture

Sajikumar

Körte²

2011

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“…We used 101 transverse hippocampal slices (400-mm thick), prepared from 101 male Wistar rats (6-to 7-wk-old). Slice preparation, incubation, and recordings were conducted according to the protocol reported in our earlier publications (Sajikumar et al 2005(Sajikumar et al , 2009Navakkode et al 2007). …”

mentioning

confidence: 99%

Dopamine induces LTP differentially in apical and basal dendrites through BDNF and voltage-dependent calcium channels

Navakkode¹,

Sajikumar²,

Körte³

et al. 2012

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The dopaminergic modulation of long-term potentiation (LTP) has been studied well, but the mechanism by which dopamine induces LTP (DA-LTP) in CA1 pyramidal neurons is unknown. Here, we report that DA-LTP in basal dendrites is dependent while in apical dendrites it is independent of activation of L-type voltage-gated calcium channels (VDCC). Activation via NMDAR is critical for the induction of DA-LTP in both apical and basal dendrites, but only BDNF is required for the induction and maintenance of DA-LTP in apical dendrites. We report that dopaminergic modulation of LTP is lamina-specific at the Schaffer collateral/commissural synapses in the CA1 region.In the hippocampus, afferent inputs to the hippocampus CA1 occur via two major pathways, the temporoammonic and the Schaffer collateral/commissural fibers. Among these, the Schaffer collateral/commissural fibers from the CA3 region synapse on both the apical dendrites in the stratum radiatum (str. radiatum) and the basal dendrites in the stratum oriens (str. oriens).Studies of long-term potentiation (LTP) in the hippocampal slices both in vitro and in vivo have shown that the threshold for inducing LTP is lower in basal dendrites in comparison to apical dendrites (Kaibara and Leung 1993;Leung and Shen 1995;Sajikumar et al. 2007;Stramiello and Wagner 2010;Sajikumar and Korte 2011a). The CA1 region receives a variety of neuromodulatory inputs including the dopaminergic, cholinergic, and noradrenergic pathways (Otmakhova and Lisman 2000;Leung et al. 2003), and the distributions of these neuromodulatory inputs are not uniform. For example, the hippocampus receives dispersed cholinergic innervations with the highest density of cholinergic axons in the str. oriens and principal cell layer (Arai et al. 1994;Gasbarri et al. 1994b;Aznavour et al. 2002), and anatomical studies suggest that, not only the str. radiatum but also the str. oriens, is innervated by dopaminergic projections from the meso-limbo-cortical system (Verney et al. 1985; Gasbarri et al. 1994a,b) The neuromodulatory influences in the str. radiatum and str. oriens regions are also different. One example of a spatially restricted effect of a neuromodulatory neurotransmitter is the action of acetylcholine on the muscarinic acetylcholine receptors. Cholinergic activation by carbachol produces a significantly stronger suppression of synaptic transmission at the CA3-CA1 synapses of the proximal apical dendrites, while being less effective at synapses of the apical tuft (Hasselmo and Schnell 1994). This cholinergic suppression has been shown to enhance associative memory functions (De Rosa and Hasselmo 2000). In neocortical pyramidal neurons, pairing of excitatory post-synaptic potentials (EPSPs) and action potentials (Gordon et al. 2006) leads to the potentiation of synapses at the proximal basal dendrites but not the distal basal dendrites. In the distal basal dendrites, synaptic potentiation occurs only when synaptic activation (which is strong enough to evoke an NMDA spike) is paired with BDNF applicatio...

“…Metaplasticity, by expanding the temporal window for formation of associative memories, may provide the necessary mechanisms for binding temporally separated events. For example, prior activation of ryanodine receptors facilitates the induction and persistence of homosynaptic and heterosynaptic LTP elicited by a subthreshold stimulation protocol applied 30 min later (Mellentin et al 2007;Sajikumar et al 2009). Thus, prior cellular activity can alter the threshold for the induction of LTP in a cellwide manner and extend the time periods typically associated with synaptic integration.…”

mentioning

confidence: 99%

‘Silent’ priming of translation-dependent LTP by β-adrenergic receptors involves phosphorylation and recruitment of AMPA receptors

Tenorio¹,

Connor²,

Guévremont³

et al. 2010

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The capacity for long-term changes in synaptic efficacy can be altered by prior synaptic activity, a process known as "metaplasticity." Activation of receptors for modulatory neurotransmitters can trigger downstream signaling cascades that persist beyond initial receptor activation and may thus have metaplastic effects. Because activation of b-adrenergic receptors (b-ARs) strongly enhances the induction of long-term potentiation (LTP) in the hippocampal CA1 region, we examined whether activation of these receptors also had metaplastic effects on LTP induction. Our results show that activation of b-ARs induces a protein synthesis-dependent form of metaplasticity that primes the future induction of late-phase LTP by a subthreshold stimulus. b-AR activation also induced a long-lasting increase in phosphorylation of a-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor (AMPAR) GluA1 subunits at a protein kinase A (PKA) site (S845) and transiently activated extracellular signal-regulated kinase (ERK). Consistent with this, inhibitors of PKA and ERK blocked the metaplastic effects of b-AR activation. b-AR activation also induced a prolonged, translation-dependent increase in cell surface levels of GluA1 subunit-containing AMPA receptors. Our results indicate that bARs can modulate hippocampal synaptic plasticity by priming synapses for the future induction of late-phase LTP through up-regulation of translational processes, one consequence of which is the trafficking of AMPARs to the cell surface.