Short-term synaptic depression can increase the rate of information transfer at a release site

Abstract

The release of neurotransmitters from synapses obeys complex and stochastic dynamics. Depending on the recent history of synaptic activation, many synapses depress the probability of releasing more neurotransmitter, which is known as synaptic depression. Our understanding of how synaptic depression affects the information efficacy, however, is limited. Here we propose a mathematically tractable model of both synchronous spike-evoked release and asynchronous release that permits us to quantify the information conveyed by a synapse. The model transits between discrete states of a communication channel, with the present state depending on many past time steps, emulating the gradual depression and exponential recovery of the synapse. Asynchronous and spontaneous releases play a critical role in shaping the information efficacy of the synapse. We prove that depression can enhance both the information rate and the information rate per unit energy expended, provided that synchronous spike-evoked release depresses less (or recovers faster) than asynchronous release. Furthermore, we explore the theoretical implications of short-term synaptic depression adapting on longer time scales, as part of the phenomenon of metaplasticity. In particular, we show that a synapse can adjust its energy expenditure by changing the dynamics of short-term synaptic depression without affecting the net information conveyed by each successful release. Moreover, the optimal input spike rate is independent of the amplitude or time constant of synaptic depression. We analyze the information efficacy of three types of synapses for which the short-term dynamics of both synchronous and asynchronous release have been experimentally measured. In hippocampal autaptic synapses, the persistence of asynchronous release during depression cannot compensate for the reduction of synchronous release, so that the rate of information transmission declines with synaptic depression. In the calyx of Held, the information rate per release remains constant despite large variations in the measured asynchronous release rate. Lastly, we show that dopamine, by controlling asynchronous release in corticostriatal synapses, increases the synaptic information efficacy in nucleus accumbens.

Local design principles at hippocampal synapses revealed by an energy-information trade-off

“…Here, we use a computational model to investigate the relevance of energetic constraints to design and function of hippocampal synapses that are characterized by low initial release probabilities but marked activity-dependent STP. Previous studies of information transmission at cortical synapses considered short-time dynamics arising from vesicle depletion alone [20][21][22][23] , or made simplifying model assumptions about presynaptic organization (e.g., availability of at most one vesicle per release site) 9,24 , limiting their physiological relevance for describing facilitating hippocampal synapses.…”

Adaptive Synaptic Memory via Lithium Ion Modulation in RRAM Devices

“…In doing so, this RRAM device has the capacity to mimic ionic mechanisms in synapses faithfully that enables efficient learning and data processing. [18][19][20][21][22][23][24] We also present an empirically-driven conduction-based model of our device.…”

Synaptic Information Transmission in a Two-State Model of Short-Term Facilitation

“…In previous work, we studied the information transmission in a synapse during short-term depression [ 9 , 12 ]. There, the state of the binary asymmetric channel, which models the synapse, depended on the history of the output .…”

“…Several studies have addressed the modulatory role of short-term depression on synaptic information transmission [ 7 , 8 , 9 ]. In contrast, the information rate of a facilitating synapse is not yet fully understood, though it has been suggested that short-term facilitation temporally filters the incoming spike train [ 10 ].…”