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.
Neurons receive information from other neurons via hundreds of contacts (synapses) spread across their dendritic branches. Input signals from synapses propagate along a dendrite to the cell body (soma), where the neuron decides whether or not to produce an action potential. Signals that travel further decay more. Were all synapses equally strong, a synapse far from the soma would have less influence on the decision than a synapse close by. However, neurons in the hippocampus, which are involved in learning and memory, have synapses far from the soma that are stronger than those close by, so that all synapses have an equal voice (“synaptic democracy”). But 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. Specifically, the calcium concentration at the synapse, which is modulated by the backpropagating action potential, decreases with distance from the soma. We show that when the strength of a synapse is adapted in a self-organising manner based on calcium concentration, synaptic democracy is obtained.