Single-Cell Membrane Potential Fluctuations Evince Network Scale-Freeness and Quasicriticality

What information single neurons receive about general neural circuit activity is a fundamental question for neuroscience. Somatic membrane potential (V_m) fluctuations are driven by the convergence of synaptic inputs from a diverse cross-section of upstream neurons. Furthermore, neural activity is often scale-free, implying that some measurements should be the same, whether taken at large or small scales. Together, convergence and scale-freeness support the hypothesis that single V_m recordings carry useful information about high-dimensional cortical activity. Conveniently, the theory of "critical branching networks" (one purported explanation for scale-freeness) provides testable predictions about scale-free measurements that are readily applied to V_m fluctuations. To investigate, we obtained whole-cell current-clamp recordings of pyramidal neurons in visual cortex of turtles with unknown genders. We isolated fluctuations in V_m below the firing threshold and analyzed them by adapting the definition of "neuronal avalanches" (i.e., spurts of population spiking). The V_m fluctuations which we analyzed were scale-free and consistent with critical branching. These findings recapitulated results from large-scale cortical population data obtained separately in complementary experiments using microelectrode arrays described previously (Shew et al., 2015). Simultaneously recorded single-unit local field potential did not provide a good match, demonstrating the specific utility of V_m Modeling shows that estimation of dynamical network properties from neuronal inputs is most accurate when networks are structured as critical branching networks. In conclusion, these findings extend evidence of critical phenomena while also establishing subthreshold pyramidal neuron V_m fluctuations as an informative gauge of high-dimensional cortical population activity.SIGNIFICANCE STATEMENT The relationship between membrane potential (V_m) dynamics of single neurons and population dynamics is indispensable to understanding cortical circuits. Just as important to the biophysics of computation are emergent properties such as scale-freeness, where critical branching networks offer insight. This report makes progress on both fronts by comparing statistics from single-neuron whole-cell recordings with population statistics obtained with microelectrode arrays. Not only are fluctuations of somatic V_m scale-free, they match fluctuations of population activity. Thus, our results demonstrate appropriation of the brain's own subsampling method (convergence of synaptic inputs) while extending the range of fundamental evidence for critical phenomena in neural systems from the previously observed mesoscale (fMRI, LFP, population spiking) to the microscale, namely, V_m fluctuations.