Previous studies show that the activation of voltage-dependent channels is dependent on the local density of synapses in the dendritic region containing voltage-dependent channels. We hypothesized that the selective innervation of excitatory vestibulospinal (VST) neurons on the medial dendrites of contralateral splenius motoneurons is designed to enhance the activation of persistent inward currents (PICs) mediated by dendritic L-type Ca(2+) channels. Using compartmental models of splenius motoneurons we compared the synaptic current reaching the soma in response to excitatory input generated by synapses with two different distribution patterns. The medial distribution was based on the arrangement of VST synapses on the dendrites of contralateral splenius motoneurons and the uniform distribution was based on an arrangement of synapses with no particular bias to any region of the dendritic tree. The number of synapses in each distribution was designed to match estimates of the number of VST synapses activated by head movements. In the absence of PICs, the current delivered by the synapses in the uniform distribution was slightly greater. However, the maximal currents were small, < or = 4.1 nA, regardless of the distribution of synapses. In models equipped with L-type Ca(2+) channels, PIC activation was largely determined by the local density of synapses in proximity to the L-type Ca(2+) channels. In 3 of 5 cells, this led to a 2- to 4-fold increase in the current generated by synapses in the medial distribution compared to the uniform distribution. In the other two cells, the amplification bias was in favour of the medial distribution but was either small or restricted to a narrow range of frequencies. These simulations suggest that the innervation pattern of VST axons on contralateral splenius motoneurons is arranged to strengthen an otherwise weak synaptic input by increasing the likelihood of activating PICs. Additional simulations suggest that this prediction can be tested using common experimental protocols.