Temporal filters in response to presynaptic spike trains: interplay of cellular, synaptic and short-term plasticity time scales

Abstract

Temporal filters, the ability of postsynaptic neurons to preferentially select certain presynaptic input patterns over others, have been shown to be associated with the notion of information filtering and coding of sensory inputs. Short-term plasticity (depression and facilitation; STP) has been proposed to be an important player in the generation of temporal filters. We carry out a systematic modeling, analysis and computational study to understand how characteristic postsynaptic (low-, high- and band-pass) temporal filters are generated in response to periodic presynaptic spike trains in the presence STP. We investigate how the dynamic properties of these filters depend on the interplay of a hierarchy of processes, including the arrival of the presynaptic spikes, the activation of STP, its effect on the excitatory synaptic connection efficacy, and the response of the postsynaptic cell. These mechanisms involve the interplay of a collection of time scales that operate at the single-event level (roughly, during each presynaptic interspike-interval) and control the long-term development of the temporal filters over multiple presynaptic events. These time scales are generated at the levels of the presynaptic cell (captured by the presynaptic interspike-intervals), short-term depression and facilitation, synaptic dynamics and the post-synaptic cellular currents. We develop mathematical tools to link the single-event time scales with the time scales governing the long-term dynamics of the resulting temporal filters for a relatively simple model where depression and facilitation interact at the level of the synaptic efficacy change. We extend our results and tools to account for more complex models. These include multiple STP time scales and non-periodic presynaptic inputs. The results and ideas we develop have implications for the understanding of the generation of temporal filters in complex networks for which the simple feedforward network we investigate here is a building block.

Keywords: Band-pass temporal filter; Frequency dependent filters; High-pass temporal filter; Interplay of time scales across levels of organization; Low-pass temporal filter; Short-term synaptic dynamics; Synaptic depression; Synaptic facilitation; Temporal resonance.