Dynamical response properties of neocortical neurons to conductance-driven time-varying inputs

Ensembles of cortical neurons can track fast-varying inputs and relay them in their spike trains, far beyond the cut-off imposed by membrane passive electrical properties and mean firing rates. Initially explored in silico and later demonstrated experimentally, investigating how neurons respond to sinusoidally modulated stimuli provides a deeper insight into spike initiation mechanisms and information processing than conventional F–I curve methodologies. Besides net membrane currents, physiological synaptic inputs can also induce a stimulus-dependent modulation of the total membrane conductance, which is not reproduced by standard current-clamp protocols. Here, we investigated whether rat cortical neurons can track fast temporal modulations over a noisy conductance background. We also determined input–output transfer properties over a range of conditions, including: distinct presynaptic activation rates, postsynaptic firing rates and variability and type of temporal modulations. We found a very broad signal transfer bandwidth across all conditions, similar large cut-off frequencies and power-law attenuations of fast-varying inputs. At slow and intermediate input modulations, the response gain decreased for increasing output mean firing rates. The gain also decreased significantly for increasing intensities of background synaptic activity, thus generalising earlier studies on F-I curves. We also found a direct correlation between the action potentials' onset rapidness and the neuronal bandwidth. Our novel results extend previous investigations of dynamical response properties to non-stationary and conductance-driven conditions, and provide computational neuroscientists with a novel set of observations that models must capture when aiming to replicate cortical cellular excitability.