Abstract
Synaptic plasticity, which underlies learning and memory, depends on calcium elevation in neurons, but the precise relationship between calcium and spatiotemporal patterns of synaptic inputs is unclear. Here, we develop a biologically realistic computational model of striatal spiny projection neurons with sophisticated calcium dynamics, based on data from rodents of both sexes, to investigate how spatiotemporally clustered and distributed excitatory and inhibitory inputs affect spine calcium. We demonstrate that coordinated excitatory synaptic inputs evoke enhanced calcium elevation specific to stimulated spines, with lower but physiologically relevant calcium elevation in nearby non-stimulated spines. Results further show a novel and important function of inhibition-to enhance the difference in calcium between stimulated and non-stimulated spines. These findings suggest that spine calcium dynamics encode synaptic input patterns and may serve as a signal for both stimulus-specific potentiation and heterosynaptic depression, maintaining balanced activity in a dendritic branch while inducing pattern-specific plasticity.
Highlights
Neurons receive information from other neural cells in the form of patterns of activation of different synaptic inputs
Peak calcium in a proximal spine from a back-propagating action potential (bAP) was 0.18 mM with a time constant of decay of 74 ms, and in response to a single excitatory postsynaptic potential (EPSP) peaked at 0.2 mM with a time constant of decay of 73 ms, similar to experimental results when simulated under similar calcium-indicator conditions (Shindou et al, 2011)
These results demonstrate that the model peak spine calcium response is robust to parameter variations, with at most a 10% change in response to a bAP and a 30% change in response to an EPSP (Shindou et al, 2011)
Summary
Neurons receive information from other neural cells in the form of patterns of activation of different synaptic inputs. In vitro studies have shown that near-simultaneous stimulation of a group of spatially clustered excitatory synapses on a thin dendritic branch can elicit supralinear, prolonged membrane depolarizations in the soma (known as plateau potentials). These plateau potentials have been observed in pyramidal neurons of the cortex (Larkum et al, 2009; Schiller et al, 2000) and hippocampus (Golding et al, 2002; Harnett et al, 2012; Makara and Magee, 2013), and in spiny projection neurons of the Dorman et al eLife 2018;7:e38588.
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