Motor control by precisely timed spike patterns

Abstract: A fundamental problem in neuroscience is to understand how sequences of action potentials ("spikes") encode information about sensory signals and motor outputs. Although traditional theories of neural coding assume that information is conveyed by the total number of spikes fired (spike rate), recent studies of sensory and motor activity have shown that far more information is carried by the millisecond-scale timing patterns of action potentials (spike timing). However, it is unknown whether or how subtle differences in spike timing drive differences in perception or behavior, leaving it unclear whether the information carried by spike timing actually plays a causal role in brain function. Here we demonstrate how a precise spike timing code is read out downstream by the muscles to control behavior. We provide both correlative and causal evidence to show that the nervous system uses millisecond-scale variations in the timing of spikes within multi-spike patterns to regulate a relatively simple behavior - respiration in the Bengalese finch, a songbird. These findings suggest that a fundamental assumption of current theories of motor coding requires revision, and that significant improvements in applications, such as neural prosthetic devices, can be achieved by using precise spike timing information.