A cortical neuron typically makes multiple synaptic contacts on the dendrites of a post-synaptic target neuron. The functional implications of this apparent redundancy are unclear. The dendritic location of a synaptic contact affects the time-course of the somatic post-synaptic potential (PSP) due to dendritic cable filtering. Consequently, a single pre-synaptic axonal spike results with a PSP composed of multiple temporal profiles. Here, we developed a "filter-and-fire" (F&F) neuron model that captures these features and show that the memory capacity of this neuron is threefold larger than that of a leaky integrate-and-fire (I&F) neuron, when trained to emit precisely timed output 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. Multiple synaptic contacts between pairs of cortical neurons are therefore an important feature rather than a bug and can serve to reduce axonal wiring requirements.
Human-specific cognitive abilities depend on information processing in the cerebral cortex, where neurons are significantly larger and sparser compared to rodents. We found that, in synaptically-connected layer 2/3 pyramidal cells (L2/3 PCs), soma-to-soma signal propagation delay is similar in humans and rodents. Thus, to compensate for the increase in neurons size, membrane potential changes must propagate faster in human axons and/or dendrites. Dual somato-dendritic and somato-axonal patch recordings show that action potentials (APs) propagation speed is similar in human and rat axons, but the forward propagation of the EPSPs and the back-propagating APs are ~1.7-fold faster in human dendrites. Faithful biophysical models of human and rat L2/3 PCs, combined with pharmacological manipulations of membrane properties, showed that the larger dendritic diameter, combined with differences in cable properties, underlie the accelerated signal propagation in human cortical circuits. The implication for information processing in the human brain are discussed.
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