Abstract
Cortical activity is organized across multiple spatial and temporal scales. Most research on the dynamics of neuronal spiking is concerned with timescales of 1 ms–1 s, and little is known about spiking dynamics on timescales of tens of seconds and minutes. Here, we used frequency domain analyses to study the structure of individual neurons’ spiking activity and its coupling to local population rate and to arousal level across 0.01–100 Hz frequency range. In mouse medial prefrontal cortex, the spiking dynamics of individual neurons could be quantitatively captured by a combination of interspike interval and firing rate power spectrum distributions. The relative strength of coherence with local population often differed across timescales: a neuron strongly coupled to population rate on fast timescales could be weakly coupled on slow timescales, and vice versa. On slow but not fast timescales, a substantial proportion of neurons showed firing anticorrelated with the population. Infraslow firing rate changes were largely determined by arousal rather than by local factors, which could explain the timescale dependence of individual neurons’ population coupling strength. These observations demonstrate how neurons simultaneously partake in fast local dynamics, and slow brain-wide dynamics, extending our understanding of infraslow cortical activity beyond the mesoscale resolution of fMRI.
Highlights
A single action potential lasts about a millisecond, and a second suffices for a vast range of sensory-motor and cognitive behaviors, such as recognizing pictures and sounds, getting up or sitting down, or recalling a memory
We found that neuronal spike trains have 1/f power spectral density (PSD), and that PSD in combination with interspike interval (ISI) distribution suffices for an accurate quantitative model of single neuron spiking dynamics on both fast and slow timescales
Population coupling in infraslow, but not fast frequencies reflected coupling to brain-wide arousal signal. While these general rules held for most neurons, a great diversity of fine-detailed behaviors was seen within local populations, for example regarding the slow-timescale dynamics as captured by a neuron’s power spectrum, and the way its coherency with population rate depended on frequency
Summary
A single action potential lasts about a millisecond, and a second suffices for a vast range of sensory-motor and cognitive behaviors, such as recognizing pictures and sounds, getting up or sitting down, or recalling a memory. Changes in arousal can span tens of seconds and minutes, yet they affect performance in subsecond behavioral tasks (Harris and Thiele 2011; Palva and Palva 2012; McGinley et al 2015). How much can the firing rate of an individual neuron change over tens of seconds and minutes, and how can these slow dynamics be summarized quantitatively? In frequencies ≤0.1 Hz population rate was highly correlated with arousal as reflected by the pupil area These results suggest that dynamics on fast and infraslow timescales are distinct processes, and likely regulated by distinct mechanisms at the single neuron level
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