Branch-specific plasticity explains distal enrichment of retinotopically displaced inputs in visual cortex

Neurons distribute synaptic inputs across their dendritic tree. In layer 2/3 pyramidal cells of primary visual cortex, spines on distal dendrites share somatic orientation preference but have receptive fields displaced in retinotopic space, which supports tuning to visual edges. However, it is not known how synaptic plasticity rules can lead to specialization of tuning properties across dendritic compartments. We demonstrate an experimentally grounded model of compartment-specific spike-timing dependent plasticity (STDP) that accounts for the enrichment of retinotopically-displaced inputs on distal branches. Our previous experimental work revealed compartment-specific calcium signals that predict reduced STDP-mediated depression but preserved potentiation. Based on these findings, we built an STDP model with compartment-specific properties, in which some distal branches are relatively resistant to STDP-mediated depression. Synapses on these branches are more likely to stabilize inputs with weaker correlations to postsynaptic spiking. Using a visual input model, we show that compartment-specific reduction in STDP-mediated depression recapitulates in vivo experimental measurements of spine tuning. Furthermore, our experimental results show that reduced STDP-mediated depression is restricted to distal dendritic compartments with complex branching structure and not observed in other distal branches. Therefore, our model makes an untested prediction that complex branches will be hotspots for retinotopically-displaced inputs.