Neurons receive thousands of inputs onto their dendritic arbour, where individual synapses undergo activity-dependent changes in strength. The durable forms of synaptic strength change, long-term potentiation (LTP) and long-term depression (LTD), require calcium entry through N-methyl-D-aspartate receptors (NMDARs) that triggers downstream protein signalling cascades in the dendrite. Intriguingly, sLTP and sLTD are not necessarily restricted to the active, targeted synapses (homosynapses), and the changes in synaptic strength can spread and affect the strengths of inactive or non-stimulated synapses (heterosynapses) on the same cell. Precisely how neurons allocate resources for implementing the changes in strength at individual synapses depending on their proximity to activity across space and time remains an open question. In order to gain insights into the elementary processes underlying heterosynaptic plasticity and their interplay with homosynaptic plasticity, we have combined experimental and mathematical modelling approaches. On the one hand, we used glutamate uncaging to precisely and systematically stimulate variable numbers of homosynapses sharing the same dendritic branch whilst monitoring tens of other heterosynapses on the same dendrite. Homosynaptic potentiation of clusters of dendritic spines leads to heterosynaptic changes that are NMDAR-dependent, requiring CaMKII and calcineurin activity. On the other hand, inspired by the calcium levels hypothesis where different amounts of calcium lead to either growth or shrinkage of spines, we have built a model based on a dual-role calcium-dependent protein that induces spine shrinkage or potentiation dynamics. Comparing our experimental results with model predictions, we find that (i) both collaboration and competition among spines for protein resources are key drivers of heterosynaptic plasticity and (ii) the temporal and spatial distance between simultaneously stimulated spines impact the resulting spine dynamics. Moreover, our model can reconcile a number of disparate and sometimes contradictory experimental reports of heterosynaptic sLTP or sLTD at homo and heterosynaptic spines. Our results provide a quantitative description of the heterosynaptic footprint unfolding across minutes and hours post-stimulation across tens of microns of dendritic space. This broadens our knowledge about the operation of non-linear dendritic summation rules and how they impact spiking decisions.