Lognormal firing rate distribution reveals prominent fluctuation–driven regime in spinal motor networks

Abstract

When spinal circuits generate rhythmic movements it is important that the neuronal activity remains within stable bounds to avoid saturation and to preserve responsiveness. Here, we simultaneously record from hundreds of neurons in lumbar spinal circuits of turtles and establish the neuronal fraction that operates within either a ‘mean-driven’ or a ‘fluctuation–driven’ regime. Fluctuation-driven neurons have a ‘supralinear’ input-output curve, which enhances sensitivity, whereas the mean-driven regime reduces sensitivity. We find a rich diversity of firing rates across the neuronal population as reflected in a lognormal distribution and demonstrate that half of the neurons spend at least 50 $\%$ of the time in the ‘fluctuation–driven’ regime regardless of behavior. Because of the disparity in input–output properties for these two regimes, this fraction may reflect a fine trade–off between stability and sensitivity in order to maintain flexibility across behaviors.

DOI: http://dx.doi.org/10.7554/eLife.18805.001

eLife digest

Where and how are rhythmic movements, such as walking, produced? Many neurons, primarily in the spinal cord, are responsible for the movements, but it is not known how the activity is distributed across this group of cells and what type of activity the neurons use. Some neurons produce regular patterns of “spiking” activity, while others produce spikes at more irregular intervals. These two types of activity have different origins and represent different states of the neural network. It is not clear whether they participate equally in a movement, or if there is a hierarchy among the neurons, such that some neurons have more influence than others.

Petersen and Berg studied neurons in the lower spines of turtles during rhythmic movements. The experiments show that during rhythmic scratching some neurons are very active while most aren’t particularly active at all. This is known as a lognormal distribution and is seen in many other situations, such as the levels of income of people in a society.

Petersen and Berg also found that neurons can move between two regimes of activity, called the mean-driven and fluctuation-driven spiking regimes. During rhythmic scratching, the neurons are almost equally divided between the two regimes, and this division is also found in other types of rhythmic movement. This even division between the two regimes is likely to be important for maintaining a balance between the sensitivity and stability of the neural network. The next steps following on from this work are to reveal the mechanisms behind the two regimes and to find out what causes these differences in activity.

DOI: http://dx.doi.org/10.7554/eLife.18805.002