Near-optimal information relay by the neuronal population of layer 4 barrel cortex

SUMMARY Cortical function reflects the activities of populations of neurons. How accurately they can encode information depends on the speed with which each neuron can respond to input, as revealed by dynamic gain analysis. In a simple model, we show that disparate parameters control this response speed and thereby the precision of encoding, namely cell number, cell size, and the correlation time of the background noise. We experimentally test these predictions on excitatory populations in the mouse barrel cortex population. We confirm predictions as to the impacts of cell size and input correlation time and we demonstrate that these disparate factors are precisely matched with the number of neurons in layer 4, such that even a single thalamocortical spike at the input is reliably reflected in the population output. However, this encoding performance can be modulated by the channels that mediate M-current, suggesting that coding in layer 4 may vary as a function of brain state. In Brief A single thalamocortical spike, the smallest conceivable input, can be faithfully encoded by Layer 4 of the somatosensory cortex, because a set of disparate parameters are matched. Highlights - A neuronal population encodes external input more precisely, if the population is more expansive (more cells, larger dendrites), or if the neurons’ local, recurrent input fluctuates more slowly - In a structure with tightly limited spatial extension, layer 4 of barrel cortex, a population of the smallest excitatory cells achieves single spike sensitivity by slowing down recurrent synaptic inputs - Ion channels under cholinergic neuromodulatory control regulate the high sensitivity