Rosenbaum R, Rubin JE, Doiron B. Short-term synaptic depression and stochastic vesicle dynamics reduce and shape neuronal correlations. J Neurophysiol 109: 475-484, 2013. First published October 31, 2012 doi:10.1152/jn.00733.2012.-Correlated neuronal activity is an important feature in many neural codes, a neural correlate of a variety of cognitive states, as well as a signature of several disease states in the nervous system. The cellular and circuit mechanics of neural correlations is a vibrant area of research. Synapses throughout the cortex exhibit a form of short-term depression where increased presynaptic firing rates deplete neurotransmitter vesicles, which transiently reduces synaptic efficacy. The release and recovery of these vesicles are inherently stochastic, and this stochasticity introduces variability into the conductance elicited by depressing synapses. The impact of spiking and subthreshold membrane dynamics on the transfer of neuronal correlations has been studied intensively, but an investigation of the impact of short-term synaptic depression and stochastic vesicle dynamics on correlation transfer is lacking. We find that short-term synaptic depression and stochastic vesicle dynamics can substantially reduce correlations, shape the timescale over which these correlations occur, and alter the dependence of spiking correlations on firing rate. Our results show that short-term depression and stochastic vesicle dynamics need to be taken into account when modeling correlations in neuronal populations. Synaptic neurotransmitter vesicles are released probabilistically in response to a presynaptic spike, and released vesicles are recovered stochastically over a timescale of several hundred milliseconds (Vere-Jones 1966;Wang 1999;Fuhrmann et al. 2002;Goldman 2004;Rosenbaum et al. 2012). The depletion of neurotransmitter vesicles by trains of presynaptic action potentials gives rise to a form of short-term synaptic depression that is pervasive in the cortex (Zucker and Regehr 2002). We find that when two postsynaptic neurons receive correlated input through depressing synapses, the correlation between the synaptic conductances across the neurons' membranes, as well as the neurons' spike trains, are drastically smaller than the correlations predicted by a nondepressing, static synapse model. This reduction in correlation is especially prevalent at higher presynaptic firing rates that more effectively deplete neurotransmitter vesicles. Coupled with the fact that cellular dynamics suppress correlations at low firing rates (de la Rocha et al. 2007), these results show that a population of neurons with depressing synapses exhibit small correlations over a broad range of firing rates, even when their inputs are strongly correlated. Our conclusions reveal an important, yet often ignored, mechanism that promotes asynchronous spiking activity in densely connected neuronal populations.
METHODSWe begin by describing the statistical measures used to quantify correlations in this study. We then describe the presyn...