Synaptic Plasticity Is Predicted by Spatiotemporal Firing Rate Patterns and Robust to In Vivo-like Variability

Abstract

Synaptic plasticity, the experience-induced change in connections between neurons, underlies learning and memory in the brain. Most of our understanding of synaptic plasticity derives from in vitro experiments with precisely repeated stimulus patterns; however, neurons exhibit significant variability in vivo during repeated experiences. Further, the spatial pattern of synaptic inputs to the dendritic tree influences synaptic plasticity, yet is not considered in most synaptic plasticity rules. Here, we investigate how spatiotemporal synaptic input patterns produce plasticity with in vivo-like conditions using a data-driven computational model with a plasticity rule based on calcium dynamics. Using in vivo spike train recordings as inputs to different size clusters of spines, we show that plasticity is strongly robust to trial-to-trial variability of spike timing. In addition, we derive general synaptic plasticity rules describing how spatiotemporal patterns of synaptic inputs control the magnitude and direction of plasticity. Synapses that strongly potentiated have greater firing rates and calcium concentration later in the trial, whereas strongly depressing synapses have hiring firing rates early in the trial. The neighboring synaptic activity influences the direction and magnitude of synaptic plasticity, with small clusters of spines producing the greatest increase in synaptic strength. Together, our results reveal that calcium dynamics can unify diverse plasticity rules and reveal how spatiotemporal firing rate patterns control synaptic plasticity.

Treadmill exercise pretreatment ameliorated structural synaptic plasticity impairments of medial prefrontal cortex in vascular dementia rat and improved recognition memory

“…As small protrusions that form on dendrites, structural changes in dendritic spines of neurons are crucial in the implementation of synaptic plasticity, and for memory storage and neuronal connectivity 21 . Synaptic plasticity is influenced by the spatial pattern of synaptic inputs to the dendritic spines 47 . In vivo studies have shown that dendritic spines of the cortex in the VD mice were also impaired 48 .…”

Heterosynaptic plasticity-induced modulation of synapses

“…Calcium dynamics are extremely predictive of the change in synaptic weight. Calcium dynamics are affected by local synaptic activity and depolarization [ 85 ]. Voltage-dependent calcium channels that are activated by back-propagating action potentials lead to the enhancement of [Ca 2+ ] in , even in non-active dendrites [ 13 ] that can support backpropagation and the rate of firing [ 86 , 87 ].…”

Cations Control Lipid Bilayer Memcapacitance Associated with Long-Term Potentiation

“…7 This observed behavior is reminiscent of capacitive energy harvesting 9 from self-powered nanogenerators 10 and the movement of biomolecules that occurs during LTP at biological synapses. 11 Importantly, the presence of LTP in a pure lipid bilayer suggests that the specific capacitance, C m , of a biological membrane may not be a "biological" constant. 12 Here, we describe the molecular mechanisms responsible for LTP generation in a lipid bilayer induced by electrical stimulation.…”

“…Scott et al attributed this emergent LTP behavior to a combination of molecular and mesoscopic structural changes to the zwitterionic phosphatidylcholine (PC) lipid headgroups, the dielectric properties of the lipid bilayer, and the asymmetric buildup of charges across the lipid bilayer . This observed behavior is reminiscent of capacitive energy harvesting from self-powered nanogenerators and the movement of biomolecules that occurs during LTP at biological synapses . Importantly, the presence of LTP in a pure lipid bilayer suggests that the specific capacitance, C m , of a biological membrane may not be a “biological” constant …”