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

Abstract

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 ...

Competition between recently potentiated synaptic inputs reveals a winner-take-all phase of synaptic tagging and capture

“…with the concept that there are two contributors to the plasticity threshold essential for the effective coding of information from multiple inputs (11,12). First, information must be encoded by means of a change in synaptic weights, and synaptic tags must be set.…”

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

“…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.…”

“…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 application (Gordon et al 2006). Even within the apical dendrites, the plasticity thresholds for inducing LTP and LTD are different in distal and proximal regions (Parvez et al 2010;Sajikumar and Korte 2011a).…”

“…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 application (Gordon et al 2006). Even within the apical dendrites, the plasticity thresholds for inducing LTP and LTD are different in distal and proximal regions (Parvez et al 2010;Sajikumar and Korte 2011a).Persistence of long-term memory depends on the activation of the ventral tegmental area (VTA)/hippocampus dopaminergic connections (Rossato et al 2009). Dopamine also regulates the expression of proteins essential for the establishment of long-lasting neuronal plasticity like brain-derived neurotrophic factor (BDNF), and this requires NMDA-receptor activity (Kuppers and Beyer 2001).…”

Investigation of Synaptic Tagging/Capture and Cross-capture using Acute Hippocampal Slices from Rodents

“…Allow 20 min for the slices to recover. Test the pathway independence with a paired-pulse facilitation protocol 27,28 .…”