Synaptic amplification by dendritic spines enhances input cooperativity

Dendritic spines are the nearly ubiquitous site of excitatory synaptic input onto neurons(1–2) and as such are critically positioned to influence diverse aspects of neuronal signaling. Decades of theoretical studies have proposed that spines may function as highly effective and modifiable chemical and electrical compartments that regulate synaptic efficacy, integration, and plasticity(3–8). Experimental studies have confirmed activity-dependent structural dynamics and biochemical compartmentalization by spines(9–12). However, a longstanding debate remains over the influence of spines on the electrical aspects of synaptic transmission and dendritic operation(3–8,13–18). Here, we measured the amplitude ratio (AR) of spine head to parent dendrite voltage across a range of dendritic compartments and calculated the associated R(neck) for spines at apical trunk dendrites in hippocampal CA1 pyramidal neurons. We found that R(neck) is large enough (~500 MΩ) to substantially amplify the spine head depolarization associated with a unitary synaptic input by ~1.5- to ~45-fold depending on parent dendritic impedance. A morphologically realistic compartmental model capable of reproducing the observed spatial profile of AR indicates that spines provide a consistently high impedance input structure throughout the dendritic arbor. Finally, we demonstrate that the amplification produced by spines encourages electrical interaction among coactive inputs through an R(neck)-dependent increase in spine head voltage- dependent conductance activation. We conclude that the electrical properties of spines promote nonlinear dendritic processing and associated forms of plasticity and storage, thus fundamentally enhancing the computational capabilities of neurons(19–21).