Precise timing is ubiquitous, consistent, and coordinated across 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 of 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.

Hawkmoths use wingstroke-to-wingstroke frequency modulation for aerial recovery to vortex ring perturbations

“…From here, we calculated the the phase variable ψ(t) as the complex angle of H(φ)(t). This method of estimating phase from time series measurements is well established in the biology literature [39,40,18].…”

“…Manduca sexta typically fire only once per wingbeat [41,2,18], suggesting that wingbeat frequency is driven by a single event. Therefore, we defined an arbitrary phase threshold and defined wingbeat frequency as the inverse of the time between threshold crossings.…”

“…In Manduca sexta, wing kinematics are controlled by a set of 10 muscles, so any changes in wingbeat frequency likely affects the coordination of these muscles. In Manduca sexta, the downstroke is triggered by typically a single action potential to the left and right DLMs [46,2,18]. Precise changes in the activation phase of these DLMs can account for 50% of yaw torque production [2].…”

“…Because of the strong phase dependence of Manduca sexta DLMs [2], the nervous system may need to maintain precise control over muscle activation phase while the frequency of muscle strain changes from wingstroke-to-wingstroke. Further complications arise because recent work has shown that the timing of the 10 major muscles controlling wing kinematics are tightly coordinated in their activation timing [18]. Changes in wingbeat frequency may require changes in activation frequency for all ten muscles involved orchestrated through phase shifts across the entire motor program.…”

“…Insects have the capacity to change wingbeat frequency, regardless of whether they possess synchronous (neurogenic) or asynchronous (myogenic) flight strategies. In species with synchronous flight muscles such as Manduca sexta, wing motion is triggered by typically by a single action potential with sub-millisecond precision to the dorsolongitudinal muscles (DLMs) [17,2,18]. Although the nervous system can shift the timing of muscle activation [2], synchronous hawkmoths are often observed [4] and modeled [19,20] as maintaining a constant wingbeat frequency.…”