A two-compartment model of synaptic computation and plasticity

Abstract

The synapse is typically viewed as a single compartment, which acts as a linear gain controller on incoming input. Traditional plasticity rules enable this gain control to be dynamically optimized by Hebbian activity. Whilst this view nicely captures postsynaptic function, it neglects the non-linear dynamics of presynaptic function. Here we present a two-compartment model of the synapse in which the presynaptic terminal first acts to filter presynaptic input before the postsynaptic terminal, acting as a gain controller, amplifies or depresses transmission. We argue that both compartments are equipped with distinct plasticity rules to enable them to optimally adapt synaptic transmission to the statistics of pre-and postsynaptic activity. Specifically, we focus on how presynaptic plasticity enables presynaptic filtering to be optimally tuned to only transmit information relevant for postsynaptic firing. We end by discussing the advantages of having a presynaptic filter and propose future work to explore presynaptic function and plasticity in vivo.

Astrocyte-mediated switch in spike timing-dependent plasticity during hippocampal development

“…Why some synapses, as we observe at CA3–CA1 synapses, show pre- or postsynaptic plasticity has yet to be determined, although this may reflect different computational requirements. As indicated above, presynaptic t-LTP may contribute to circuit computation by changing short-term dynamics and it may shift synapses between low-pass and high-pass filtering modes, thereby changing the computational properties of the synapse 48 , 83 , 84 . At somatosensory cortex, L4-L2/3 and L2/3-L2/3 synapses, STDP shows different requirements, indicating that the pre- or post-synaptic expression of plasticity is fundamental for the proper brain circuits functioning and that it is possible they are differently regulated 85 , 86 .…”

Heterosynaptic cross-talk of pre- and postsynaptic strengths along segments of dendrites

“…Such a mechanism could confer homeostatic stability to synapses, although the precise properties of disjunctional plasticity warrant further studies. Notably, the independent regulation of pre-and postsynaptic strengths has recently been explained by the difference in functional impact on the postsynaptic neuron (Costa et al, 2017, Tong et al, 2020. For future studies on the regulation of synaptic strength, it is therefore crucial to consider both, pre-and postsynaptic strengths for fully interpreting the consequences on neural network activity.…”

“…This knowledge gap can mainly be attributed to the technical difficulties of measuring presynaptic strength, especially in more intact systems, such as brain slices, or in vivo (O'Rourke et al, 2012;Burette et al, 2015). However, investigating synaptic plasticity at both loci is particularly important because pre-and postsynaptic terminals might represent functionally distinct and independently regulated compartments (Padamsey et al, 2017;Costa et al, 2017;Xu et al, 2013;Sá ez and Friedlander, 2009;Letellier et al, 2019) and are therefore likely to also differ in their spatial regulation with consequences on the property of information transfer (Costa et al, 2017;Tong et al, 2020).…”

Disruption of Cholinergic Circuits as an Area for Targeted Drug Treatment of Alzheimer’s Disease: In Vivo Assessment of Short-Term Plasticity in Rat Brain

“…The striking interplay in target-specific homeostasis modulates the efficacy of neurotransmission required for both hypo- and hyper-innervation to maintain stable synaptic strength [ 35 ]. Presynaptic plasticity optimally tunes presynaptic filtering, acting as a gain controller to amplify or depress transmission maximizing the efficiency of information transfer [ 46 ].…”