A novel form of presynaptic CaMKII-dependent short-term potentiation between Lymnaea neurons

Abstract

Short-term plasticity is thought to form the basis for working memory, the cellular mechanisms of which are the least understood in the nervous system. In this study, using in vitro reconstructed synapses between the identified Lymnaea neuron visceral dorsal 4 (VD4) and left pedal dorsal 1 (LPeD1), we demonstrate a novel form of short-term potentiation (STP) which is 'use'- but not time-dependent, unlike most previously defined forms of short-term synaptic plasticity. Using a triple-cell configuration we demonstrate for the first time that a single presynaptic neuron can reliably potentiate both inhibitory and excitatory synapses. We further demonstrate that, unlike previously described forms of STP, the synaptic potentiation between Lymnaea neurons does not involve postsynaptic receptor sensitization or presynaptic residual calcium. Finally, we provide evidence that STP at the VD4-LPeD1 synapse requires presynaptic calcium/calmodulin dependent kinase II (CaMKII). Taken together, our study identifies a novel form of STP which may provide the basis for both short- and long-term potentiation, in the absence of any protein synthesis-dependent steps, and involve CaMKII activity exclusively in the presynaptic cell.

Pentylenetetrazol-Induced Epileptiform Activity Affects Basal Synaptic Transmission and Short-Term Plasticity in Monosynaptic Connections

“…In view of this, we can speculate that chemically-induced epileptiform activity effectively promotes a short-lasting form of synaptic plasticity in our system. Our observations bear resemblance to a novel form of short-term potentiation described in reconstructed synapses between Lymnaea VD4 and LPeD1 neurons, which exhibit an enhancement of basal transmission with comparable decay kinetics following tetanisation [83]. In both cases, there is an increase in the first EPSP amplitude followed by a rapid depotentiation upon triggering a few action potentials.…”

“…The same synaptic enhancement is displayed when stimulated at different time-points, since we observed that the potentiated response is similar from 15 to 30 minutes following epileptiform activity. On the basis of these properties, these forms of plasticity have been defined as use- rather than time-dependent [83]. A similar use-dependent dynamic upregulation of synaptic transmission has also previously been described in the CA1 area of rat hippocampus [84], thus excluding that these synaptic modulations are restricted to invertebrate neurons.…”

Roles of Calcium/Calmodulin-Dependent Kinase II in Long-Term Memory Formation in Crickets

“…In mollusks, CaMKII participates in short-term synaptic potentiation [12], intermediate-term sensitization [13] and consolidation of long-term memory (LTM) [14], but its molecular mechanisms are not well understood. In the courtship conditioning in the fruit-fly Drosophila , in which a male fly exposed to a previously mated female exhibits suppression of courtship to a virgin female, inhibition of CaMKII in the central complex and parts of the lateral protocerebrum impairs memory formation [15], [16].…”

Ca2+-independent Activation of Ca2+/Calmodulin-dependent Protein Kinase II Bound to the C-terminal Domain of CaV2.1 Calcium Channels

“…Previous studies implicate presynaptic CaMKII in different forms of synaptic plasticity (25)(26)(27)(28)(29), including modulation of paired-pulse facilitation (30 -32). CaMKII forms a complex with Ca V 2.1 channels in transfected cells via a site in the proximal C-termi-nal domain (33).…”