STDP and the distribution of preferred phases in the whisker system

Abstract

Rats and mice use their whiskers to probe the environment. By rhythmically swiping their whiskers back and forth they can detect the existence of an object, locate it, and identify its texture. Localization can be accomplished by inferring the position of the whisker. Rhythmic neurons that track the phase of the whisking cycle encode information about the azimuthal location of the whisker. These neurons are characterized by preferred phases of firing that are narrowly distributed. Consequently, pooling the rhythmic signal from several upstream neurons is expected to result in a much narrower distribution of preferred phases in the downstream population, which however has not been observed empirically. Here, we show how spike timing dependent plasticity (STDP) can provide a solution to this conundrum. We investigated the effect of STDP on the utility of a neural population to transmit rhythmic information downstream using the framework of a modeling study. We found that under a wide range of parameters, STDP facilitated the transfer of rhythmic information despite the fact that all the synaptic weights remained dynamic. As a result, the preferred phase of the downstream neuron was not fixed, but rather drifted in time at a drift velocity that depended on the preferred phase, thus inducing a distribution of preferred phases. We further analyzed how the STDP rule governs the distribution of preferred phases in the downstream population. This link between the STDP rule and the distribution of preferred phases constitutes a natural test for our theory. Author summaryThe distribution of preferred phases of whisking neurons in the somatosensory system of rats and mice presents a conundrum: a simple pooling model predicts a distribution that is an order of magnitude narrower than what is observed empirically. Here, we suggest that this non-trivial distribution may result from activity-dependent plasticity in the form of spike timing dependent plasticity (STDP). We show that under STDP, the synaptic weights do not converge to a fixed value, but rather remain dynamic. As a result, the preferred phases of the whisking neurons vary in time, hence inducing a non-trivial distribution of preferred phases, which is governed by the STDP rule. Our results imply that the considerable synaptic volatility which has long been viewed as a difficulty that needs to be overcome, may actually be an underlying principle of the organization of the central nervous system.