Excitability and responsiveness of rat barrel cortex neurons in the presence and absence of spontaneous synaptic activity in vivo

Abstract

The brain continuously and endogenously generates electrical activities that fluctuate as a function of vigilance states. In cortical neurons, this spontaneous activity takes the form of complex synaptic barrages, with distinct temporal profiles and amplitudes during sleep and wakefulness. In this study, we explored in vivo how these two types of ongoing synaptic activities control the excitability and action potential responses of cortical neurons and analysed the subsequent effect of a complete suppression of brain electrical activity. We found that waking- and sleep-like activities facilitate similarly the integration of weak excitatory inputs and cause a similar trial-to-trial variability in firing patterns; compared to sleep-like pattern, the waking-type synaptic profile amplifies the neuronal gain to inputs of increasing magnitude. During the isoelectric brain state, neurons still fire action potentials in response to excitations but their sensitivity to weak inputs is reduced. The amplitude and temporal dynamics of spontaneous synaptic activity in the cerebral cortex vary as a function of brain states. To directly assess the impact of different ongoing synaptic activities on neocortical function, we performed in vivo intracellular recordings from barrel cortex neurons in rats under two pharmacological conditions generating either oscillatory or tonic synaptic drive. Cortical neurons membrane excitability and firing responses were compared, in the same neurons, before and after complete suppression of background synaptic drive following systemic injection of a high dose of anaesthetic. Compared to the oscillatory state, the tonic pattern resulted in a more depolarized and less fluctuating membrane potential (Vm), a lower input resistance (Rm) and steeper relations of firing frequency versus injected current (F-I). Whatever their temporal dynamics, suppression of background synaptic activities increased mean Vm, without affecting Rm, and induced a rightward shift of F-I curves. Both types of synaptic drive generated a high variability in current-induced firing rate and patterns in cortical neurons, which was much reduced after removal of spontaneous activity. These findings suggest that oscillatory and tonic synaptic patterns differentially facilitate the input-output function of cortical neurons but result in a similar moment-to-moment variability in spike responses to incoming depolarizing inputs. © 2014 The Authors.