Electrical Signaling Beyond Neurons.

Abstract

Neural action potentials (APs) are difficult to interpret as signal encoders and/or computational primitives. Their relationships with stimuli and behaviors are obscured by the staggering complexity of nervous systems themselves. We can reduce this complexity by observing that "simpler" neuron-less organisms also transduce stimuli into transient electrical pulses that affect their behaviors. Without a complicated nervous system, APs are often easier to understand as signal/response mechanisms. We review examples of nonneural stimulus transductions in domains of life largely neglected by theoretical neuroscience: bacteria, protozoans, plants, fungi, and neuron-less animals. We report properties of those electrical signals-for example, amplitudes, durations, ionic bases, refractory periods, and particularly their ecological purposes. We compare those properties with those of neurons to infer the tasks and selection pressures that neurons satisfy. Throughout the tree of life, nonneural stimulus transductions time behavioral responses to environmental changes. Nonneural organisms represent the presence or absence of a stimulus with the presence or absence of an electrical signal. Their transductions usually exhibit high sensitivity and specificity to a stimulus, but are often slow compared to neurons. Neurons appear to be sacrificing the specificity of their stimulus transductions for sensitivity and speed. We interpret cellular stimulus transductions as a cell's assertion that it detected something important at that moment in time. In particular, we consider neural APs as fast but noisy detection assertions. We infer that a principal goal of nervous systems is to detect extremely weak signals from noisy sensory spikes under enormous time pressure. We discuss neural computation proposals that address this goal by casting neurons as devices that implement online, analog, probabilistic computations with their membrane potentials. Those proposals imply a measurable relationship between afferent neural spiking statistics and efferent neural membrane electrophysiology.