Timing is (almost) everything in a comprehensive, spike-resolved flight motor program

Abstract

Sequences of action potentials, or spikes, carry information in the number of spikes and their timing. Spike timing codes are critical in many sensory systems, but there is now growing evidence that millisecond-scale changes in timing also carry information in motor brain regions, descending decision-making circuits, and individual motor units. Across all the many signals that control a behavior how ubiquitous, consistent, and coordinated are spike timing codes? Assessing these open questions ideally involves recording across the whole motor program with spike-level resolution. To do this, we took advantage of the relatively few motor units controlling the wings of a hawk moth, Manduca sexta. We simultaneously recorded nearly every action potential from all major wing muscles and the resulting forces in tethered flight. We found that timing encodes more information about turning behavior than spike count in every motor unit, even though there is sufficient variation in count alone. Flight muscles vary broadly in function as well as in the number and timing of spikes. Nonetheless, each muscle with multiple spikes consistently blends spike timing and count information in a 3:1 ratio. Coding strategies are consistent. Finally, we assess the coordination of muscles using pairwise redundancy measured through interaction information. Surprisingly, not only are all muscle pairs coordinated, but all coordination is accomplished almost exclusively through spike timing, not spike count. Spike timing codes are ubiquitous, consistent, and essential for coordination.\n\nSignificance StatementBrains can encode precise sensory stimuli and specific motor systems also appear to be precise, but how important are millisecond changes in timing of neural spikes across the whole motor program for a behavior? We record every spike that the hawk moths nervous system sends to its wing muscles. We show that all muscles convey the majority of their information in spike timing. The number of spikes does play a role, but not in a coordinated way across muscles. Instead, all coordination is done using in the millisecond timing of in spikes. The importance and prevalence of timing across the motor program pose new questions for how nervous systems create precise, coordinated motor commands.