Short-Term Synaptic Depression Causes a Non-Monotonic Response to Correlated Stimuli

Abstract

Unreliability is a ubiquitous feature of synaptic transmission in the brain. The information conveyed in the discharges of an ensemble of cells (e.g., in the spike count or in the timing of synchronous events) may not be faithfully transmitted to the postsynaptic cell because a large fraction of the spikes fail to elicit a synaptic response. In addition, short-term depression increases the failure rate with the presynaptic activity. We use a simple neuron model with stochastic depressing synapses to understand the transformations undergone by the spatiotemporal patterns of incoming spikes as these are first converted into synaptic current and afterward into the cell response. We analyze the mean and SD of the current produced by different stimuli with spatiotemporal correlations. We find that the mean, which carries information only about the spike count, rapidly saturates as the input rate increases. In contrast, the current deviation carries information about the correlations. If the afferent action potentials are uncorrelated, it saturates monotonically, whereas if they are correlated it increases, reaches a maximum, and then decreases to the value produced by the uncorrelated stimulus. This means that, at high input rates, depression erases from the synaptic current any trace of the spatiotemporal structure of the input. The non-monotonic behavior of the deviation can be inherited by the response rate provided that the mean current saturates below the current threshold setting the cell in the fluctuation-driven regimen. Afferent correlations therefore enable the modulation of the response beyond the saturation of the mean current.

Control of neuronal firing by dynamic parallel fiber feedback:implications for electrosensory reafference suppression

“…The resulting non-monotonic response in pyramidal neuron firing is similar to that described in other studies, involving both experimental and modeling contexts (e.g. Wu et al, 2006;Tan et al, 2007;Mikula and Niebur, 2003;Kuhn et al, 2004;de la Rocha and Parga, 2005). However, the underlying mechanisms vary.…”

“…However, the underlying mechanisms vary. In cases where correlations are present in the input, synaptic depression effectively decorrelates the high frequency inputs resulting in a decreased output rate (and a non-monotonic response) as input frequency rises (Mikula and Niebur, 2003;de la Rocha and Parga, 2005). Kuhn et al (Kuhn et al, 2004) described a non-monotonic response function that results from a different mechanism.…”

“…Several computational advantages of non-monotonic neuronal response functions have been reviewed recently (Kuhn et al, 2004;de la Rocha and Parga, 2005). For example, it allows neurons to be in a firing state far from saturation, such that changes in input rates can be encoded over a wide range of average rates.…”

Thalamocortical transformations of periodic stimuli: the effect of stimulus velocity and synaptic short-term depression in the vibrissa–barrel system

“…We use a simple model of vesicle turnover (Vere-Jones 1966;Wang 1999;de la Rocha et al 2002), with synapses consisting of M = 7 functional contacts (Gil et al 1999), each of them containing a vesicle releasable pool which can host at most one vesicle ready for release (Matveev and Wang 2000;de la Rocha and Parga 2005). When this pool is empty, spikes arriving to the terminal fail to transmit any signal.…”

“…The average probability P t , hereafter referred to as the 1 The difference between this synaptic model and averaged synaptic response models of STD (Abbott et al 1997;Tsodyks and Markram 1997), is that release and recovery are stochastic in one case and deterministic in the other. Neglecting the stochastic nature of the transmission leads to an underestimation of the fluctuations of the synaptic current and the post-synaptic response rate (de la Rocha and Parga 2005). transmission probability, equals the overall fraction of successful spikes.…”