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Abstract:
Although prevailing thought holds that neuronal spiking activity decreases from the awake state to the anesthesia induced state, changes in population dynamics during this transition are not understood. Extracellular unit recordings have enabled simultaneous measurements from multiple neurons but suffer from poorly defined cell identities, lack of spatial resolution, a bias toward higher firing rates, and the inability to resolving non-active neurons. Thus, arousal-related changes in synchrony and firing rate in local populations of cortical neurons remain unclear, as does the spatial organization of these activity changes. We used two-photon calcium-imaging to record neuronal spiking activity in the same layer 2/3 populations in visual cortex of awake and anesthetized rats. In addition, using cell-attached recordings from the anesthesia state, we were able to estimate with about 90% accuracy the number of action potentials in each calcium transient, allowing comparison of spike rates between awake and anesthetized states. Average neuronal firing rates remain low in awake (0.30 +/- 0.01 Hz, n = 297 neurons) and anesthetized states (0.21 +/- 0.01 Hz, n = 136 neurons). Although on average firing rates were higher in the awake state, only 60% of neurons decreased their firing upon anesthesia, whereas 40% increased their firing. Firing rate changes brought on by anesthesia in individual neurons depended directly on their prior awake firing rates. Neurons that fired at higher rates in the anesthetized state exhibited decreased firing in the awake state. AP firing was significantly less synchronous in the awake state, both in neuronal pairs and in larger populations. There was no relationship between the strength of pairwise correlations in the awake and anesthetized states, suggesting that changes in arousal state can reset functional connectivity. In both awake and anesthetized states, simultaneous firing of many neurons occurred significantly more often than would be expected from populations of independent neurons. Together this shows that although synchrony and firing rates are both modulated by arousal state at the population level, individual neurons within the population respond heterogeneously and independently.
