Network activity influences the subthreshold and spiking visual responses of pyramidal neurons in the three-layer turtle cortex

A primary goal of systems neuroscience is to understand cortical function, which typically involves studying spontaneous and stimulus-modulated cortical activity. Mounting evidence suggests a strong and complex relationship exists between the ongoing and stimulus-modulated cortical state. To date, most work in this area has been based on spiking in populations of neurons. While advantageous in many respects, this approach is limited in scope; it records the activity of a minority of neurons, and gives no direct indication of the underlying subthreshold dynamics. Membrane potential recordings can fill these gaps in our understanding, but stable recordings are difficult to obtain in vivo. Here, we recorded subthreshold cortical visual responses in the ex vivo turtle eye-attached whole-brain preparation, which is ideally-suited for such a study. We found that in the absence of visual stimulation, the network was "synchronous"; neurons displayed network-mediated transitions between low- and high-conductance membrane potential states. The prevalence of these slow-wave transitions varied across turtles and recording sessions. Visual stimulation evoked similar high-conductance states, which were on average larger and less reliable when the ongoing state was more synchronous. Responses were muted when immediately preceded by large, spontaneous high-conductance events. Evoked spiking was sparse, highly variable across trials, and mediated by concerted synaptic inputs that were in general only very weakly correlated with inputs to nearby neurons. Together, these results highlight the multiplexed influence of the cortical network on the spontaneous and sensory-evoked activity of individual cortical neurons.

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