Dendro-plexing of Single Input Spikes via Multiple Synaptic Contacts Can Enhance Cortical Neuron Computation and Reduce Axonal Wiring

Abstract

A cortical neuron typically makes multiple synaptic contacts on the dendrites of its postsynaptic target neuron. The functional implications of this apparent redundancy are unclear. Due to dendritic cable filtering, proximal dendritic synapses generate brief somatic postsynaptic potentials (PSPs) whereas distal synapses give rise to broader PSPs. Consequently, with multiple synaptic contacts, a single presynaptic spike results in a somatic PSP composed of multiple temporal profiles. We developed a "Filter-and-Fire" (F&F) neuron model that incorporates multiple contacts and cable filtering; it demonstrates threefold increase in memory capacity as compared to a leaky Integrate-and-Fire (I&F) neuron, when trained to emit precisely timed spikes for specific input patterns. Furthermore, the F&F neuron can learn to recognize spatio-temporal input patterns, e.g., MNIST digits, where the I&F model completely fails. We conclude that “dendro-plexing” single input spikes by multiple synaptic contacts enriches the computational capabilities of cortical neurons and can dramatically reduce axonal wiring. Significance Statement Cortical neurons often connect to their postsynaptic targets by making multiple synaptic contacts over the dendrites of the receiving cell. This multi-synapse connectivity pattern, discovered some 30 years ago and rediscovered many times since (including recently via EM studies), is puzzling as it appears to be redundant and wasteful. To date, no convincing explanation for this phenomenon has been provided. Here we propose a novel potential solution to this puzzle by incorporating temporal filtering properties of dendrites. We propose a conceptually and mathematically simple filter and fire (F&F) neuron model that incorporates both multiple contacts and dendritic filtering and reach surprising consequences from both the computational perspective as well as the "hardware savings" perspective.