Latent dynamics of primary sensory cortical population activity structured by fluctuations in the local field potential.

Introduction: As emerging technologies enable measurement of precise details of the activity within microcircuits at ever-increasing scales, there is a growing need to identify the salient features and patterns within the neural populations that represent physiologically and behaviorally relevant aspects of the network. Accumulating evidence from recordings of large neural populations suggests that neural population activity frequently exhibits relatively low-dimensional structure, with a small number of variables explaining a substantial fraction of the structure of the activity. While such structure has been observed across the brain, it is not known how reduced-dimension representations of neural population activity relate to classical metrics of "brain state," typically described in terms of fluctuations in the local field potential (LFP), single-cell activity, and behavioral metrics.

Methods: Hidden state models were fit to spontaneous spiking activity of populations of neurons, recorded in the whisker area of primary somatosensory cortex of awake mice. Classic measures of cortical state in S1, including the LFP and whisking activity, were compared to the dynamics of states inferred from spiking activity.

Results: A hidden Markov model fit the population spiking data well with a relatively small number of states, and putative inhibitory neurons played an outsize role in determining the latent state dynamics. Spiking states inferred from the model were more informative of the cortical state than a direct readout of the spiking activity of single neurons or of the population. Further, the spiking states predicted both the trial-by-trial variability in sensory responses and one aspect of behavior, whisking activity.

Discussion: Our results show how classical measurements of brain state relate to neural population spiking dynamics at the scale of the microcircuit and provide an approach for quantitative mapping of brain state dynamics across brain areas.