Pre- and postsynaptically expressed spiking-timing-dependent plasticity contribute differentially to neuronal learning

A plethora of experimental studies have shown that long-term plasticity can be expressed pre- or postsynaptically depending on a range of factors such as developmental stage, synapse type, and activity patterns. The functional consequences of this diversity are unknown. However, in models of neuronal learning, long-term synaptic plasticity is implemented as changes in connective weights. Whereas postsynaptic expression of plasticity predominantly affects synaptic response amplitude, presynaptic expression alters both synaptic response amplitude and short-term dynamics. In other words, the consideration of long-term plasticity as a fixed change in amplitude corresponds more closely to post- than to presynaptic expression, which means theoretical outcomes based on this choice of implementation may have a postsynaptic bias. To explore the functional implications of the diversity of expression of long-term synaptic plasticity, we modelled spike-timing-dependent plasticity (STDP) such that it was expressed either pre- or postsynaptically, or both. We tested pair-based standard STDP models and a biologically tuned triplet STDP model, and investigated the outcome in a feed-forward setting, with two different learning schemes: either inputs were triggered at different latencies, or a subset of inputs were temporally correlated. Across different STDP models and learning paradigms, we found that presynaptic changes adjusted the speed of learning, while postsynaptic expression was better at regulating spike timing and frequency. When combining both expression loci, postsynaptic changes amplified the response range, while presynaptic plasticity maintained control over postsynaptic firing rates, potentially providing a form of activity homeostasis. Our findings highlight how the seemingly innocuous choice of implementing synaptic plasticity by direct weight modification may unwittingly introduce a postsynaptic bias in modelling outcomes. We conclude that pre- and postsynaptically expressed plasticity are not interchangeable, but enable complimentary functions. Author summary Differences between functional properties of pre- or postsynaptically expressed long-term plasticity have not yet been explored in much detail. In this paper, we used minimalist models of STDP with different expression loci, in search of fundamental functional consequences. Presynaptic expression acts mostly on neurotransmitter release, thereby altering short-term synaptic dynamics, whereas postsynaptic expression affects mainly synaptic gain. We compared cases where plasticity was expressed presynaptically, postsynaptically, or both. We found that postsynaptic plasticity was more effective at changing response times, while both pre- and postsynaptic plasticity were similarly capable of detecting correlated inputs. A model with biologically tuned expression of plasticity also achieved this separation over a range of frequencies without the need of external competitive mechanisms. Postsynaptic spiking frequency was not directly affected by presynaptic plasticity of short-term plasticity alone, however in combination with a postsynaptic component, it helped restrain positive feedback, contributing to activity homeostasis. In conclusion, expression locus may determine distinct coding schemes while also keeping activity within bounds. Our findings highlight the importance of correctly implementing expression of plasticity in modelling, since the locus of expression may affect functional outcomes in simulations.