Synaptic motility and functional stability in the whisker cortex

The high motility of synaptic weights raises the question of how the brain can retain its functionality in the face of constant synaptic remodeling. Here we used the whisker system of rats and mice to study the interplay between synaptic plasticity (motility) and the transmission of sensory signals downstream. Rats and mice probe their surroundings by rhythmically moving their whiskers back and forth. The azimuthal position of a whisker can be estimated from the activity of whisking neurons that respond selectively to a preferred phase along the whisking cycle. These preferred phases are widely distributed on the ring. However, simple models for the transmission of the whisking signal downstream predict a distribution of preferred phases that is an order of magnitude narrower than empirically observed. Here, we suggest that synaptic plasticity in the form of spike-timing-dependent plasticity (STDP) may provide a solution to this conundrum. This hypothesis is addressed in the framework of a modeling study that investigated the STDP dynamics in a population of synapses that propagates the whisking signal downstream. The findings showed that, for a wide range of parameters, STDP dynamics do not relax to a fixed point. As a result, the preferred phases of downstream neurons drift in time at a nonuniform velocity, which in turn induces a nonuniform distribution of the preferred phases of the downstream population. This demonstrates how functionality, in terms of the distribution of preferred phases, can be retained not simply despite, but because of constant synaptic motility. Our analysis leads to several key empirical predictions to test this hypothesis.