Abstract
CA1 pyramidal neurons receive hundreds of synaptic inputs at different distances from the soma. Distance-dependent synaptic scaling enables distal and proximal synapses to influence the somatic membrane equally, a phenomenon called “synaptic democracy”. How this is established is unclear. The backpropagating action potential (BAP) is hypothesised to provide distance-dependent information to synapses, allowing synaptic strengths to scale accordingly. Experimental measurements show that a BAP evoked by current injection at the soma causes calcium currents in the apical shaft whose amplitudes decay with distance from the soma. However, in vivo action potentials are not induced by somatic current injection but by synaptic inputs along the dendrites, which creates a different excitable state of the dendrites. Due to technical limitations, it is not possible to study experimentally whether distance information can also be provided by synaptically-evoked BAPs. Therefore we adapted a realistic morphological and electrophysiological model to measure BAP-induced voltage and calcium signals in spines after Schaffer collateral synapse stimulation. We show that peak calcium concentration is highly correlated with soma-synapse distance under a number of physiologically-realistic suprathreshold stimulation regimes and for a range of dendritic morphologies. Peak calcium levels also predicted the attenuation of the EPSP across the dendritic tree. Furthermore, we show that peak calcium can be used to set up a synaptic democracy in a homeostatic manner, whereby synapses regulate their synaptic strength on the basis of the difference between peak calcium and a uniform target value. We conclude that information derived from synaptically-generated BAPs can indicate synapse location and can subsequently be utilised to implement a synaptic democracy.
Highlights
CA1 pyramidal neurons receive numerous synaptic inputs across their extensive dendritic tree, with synapses located up to hundreds of micrometres from the soma [1]
How can a synapse ‘‘know’’ how far it is from the soma? Using a computational model of a hippocampal neuron, we show that the action potential, which propagates from the soma back into the dendrites, contains information with which synapses can estimate their somatic distance
The calcium concentration at the synapse, which is modulated by the backpropagating action potential, decreases with distance from the soma
Summary
CA1 pyramidal neurons receive numerous synaptic inputs across their extensive dendritic tree, with synapses located up to hundreds of micrometres from the soma [1]. In CA1 pyramidal neurons, synaptic scaling overcomes this inequality with larger synaptic conductances at distal Schaffer collateral synapses than at proximal synapses [3,4,5]. This makes the amplitude of a synaptic response at the soma independent of its dendritic location, a phenomenon known as ‘dendritic democracy’ [6]. It is not clear what cues synapses may use to establish this distance-dependent scaling along the dendrites but internal activity-dependent signalling by the neuron may provide this information. The relationship between BAP features and distance may vary across different branches of the dendritic tree and depend on previous synaptic activity
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