Two-State Membrane Potential Fluctuations Driven by Weak Pairwise Correlations

Physiological experiments demonstrate the existence of weak pairwise correlations of neuronal activity in mammalian cortex (Singer, 1993). The functional implications of this correlated activity are hotly debated (Roskiesetal., 1999).Nevertheless, it is generally considered a wide spread feature of cortical dynamics. In recent years, another line of research has attracted great interest: the observation of a bimodal distribution of the membrane potential defining up states and down states at the single cell level (Wilson & Kawaguchi, 1996; Steriade, Contreras, & Amzica, 1994; Contreras & Steriade, 1995; Steriade, 2001). Here we use a theoretical approach to demonstrate that the latter phenomenon is a natural consequence of the former. In particular, we show that weak pairwise correlations of the inputs to a compartmental model of a layer V pyramidal cell can induce bimodality in its membrane potential. We show how this relationship can account for the observed increase of the power in the γ frequency band during up states, as well as the increase in the standard deviation and fraction of time spent in the depolarized state (Anderson, Lampl, Reichova, Carandini, & Ferster, 2000). In order to quantify the relationship between the correlation properties of a cortical network and the bistable dynamics of single neurons, we introduce a number of new indices. Subsequently, we demonstrate that a quantitative agreement with the experimental data can be achieved, introducing voltage-dependent mechanisms in our neuronal model such as Ca²⁺- and Ca²⁺-dependent K⁺ channels. In addition, we show that the up states and down states of the membrane potential are dependent on the dendritic morphology of cortical neurons. Furthermore, bringing together network and single cell dynamics under a unified view allows the direct transfer of results obtained in one context to the other and suggests a new experimental paradigm: the use of specific intracellular analysis as a powerful tool to reveal the properties of the correlation structure present in the network dynamics.