Flight power muscles have a coordinated, causal role in hawkmoth pitch turns.

Flying insects solve a daunting control problem of generating a patterned and precise motor program to stay airborne and generate agile maneuvers. In this motor program, each muscle encodes information about movement in precise spike timing down to the millisecond scale. Whereas individual muscles share information about movement, we do not know if they have separable effects on an animal's motion, or if muscles functionally interact such that the effects of any muscle's timing depend heavily on the state of the entire musculature. To answer these questions, we performed spike-resolution electromyography and electrical stimulation in the hawkmoth Manduca sexta during tethered flapping. We specifically explored how flight power muscles contribute to pitch control. Combining correlational study of visually-induced turns with causal manipulation of spike timing, we discovered likely coordination patterns for pitch turns, and investigated if these patterns can drive pitch control. We observed significant timing change of the main downstroke muscles, the dorsolongitudinal muscles (DLMs), associated with pitch turns. Causally inducing this timing change in the DLMs with electrical stimulation produced a consistent, mechanically relevant feature in pitch torque, establishing that power muscles in Manduca have a control role in pitch. Because changes were evoked in only the DLMs, however, these pitch torque features left large unexplained variation. We find this unexplained variation indicates significant functional overlap in pitch control such that precise timing of one power muscle does not produce a precise turn, demonstrating the importance of coordination across the entire motor program for flight.

An information theoretic method to resolve millisecond-scale spike timing precision in a comprehensive motor program.

Sensory inputs in nervous systems are often encoded at the millisecond scale in a precise spike timing code. There is now growing evidence in behaviors ranging from slow breathing to rapid flight for the prevalence of precise timing encoding in motor systems. Despite this, we largely do not know at what scale timing matters in these circuits due to the difficulty of recording a complete set of spike-resolved motor signals and assessing spike timing precision for encoding continuous motor signals. We also do not know if the precision scale varies depending on the functional role of different motor units. We introduce a method to estimate spike timing precision in motor circuits using continuous MI estimation at increasing levels of added uniform noise. This method can assess spike timing precision at fine scales for encoding rich motor output variation. We demonstrate the advantages of this approach compared to a previously established discrete information theoretic method of assessing spike timing precision. We use this method to analyze the precision in a nearly complete, spike resolved recording of the 10 primary wing muscles control flight in an agile hawk moth, Manduca sexta. Tethered moths visually tracked a robotic flower producing a range of turning (yaw) torques. We know that all 10 muscles in this motor program encode the majority of information about yaw torque in spike timings, but we do not know whether individual muscles encode motor information at different levels of precision. We demonstrate that the scale of temporal precision in all motor units in this insect flight circuit is at the sub-millisecond or millisecond-scale, with variation in precision scale present between muscle types. This method can be applied broadly to estimate spike timing precision in sensory and motor circuits in both invertebrates and vertebrates.

Precise timing is ubiquitous, consistent, and coordinated across a comprehensive, spike-resolved flight motor program.

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.

Accelerating fishes increase propulsive efficiency by modulating vortex ring geometry.

Swimming animals need to generate propulsive force to overcome drag, regardless of whether they swim steadily or accelerate forward. While locomotion strategies for steady swimming are well characterized, far less is known about acceleration. Animals exhibit many different ways to swim steadily, but we show here that this behavioral diversity collapses into a single swimming pattern during acceleration regardless of the body size, morphology, and ecology of the animal. We draw on the fields of biomechanics, fluid dynamics, and robotics to demonstrate that there is a fundamental difference between steady swimming and forward acceleration. We provide empirical evidence that the tail of accelerating fishes can increase propulsive efficiency by enhancing thrust through the alteration of vortex ring geometry. Our study provides insight into how propulsion can be altered without increasing vortex ring size and represents a fundamental departure from our current understanding of the hydrodynamic mechanisms of acceleration. Our findings reveal a unifying hydrodynamic principle that is likely conserved in all aquatic, undulatory vertebrates.

Neurotechnology and international security: Predicting commercial and military adoption of brain-computer interfaces (BCIs) in the United States and China.

In the past decade, international actors have launched "brain projects" or "brain initiatives." One of the emerging technologies enabled by these publicly funded programs is brain-computer interfaces (BCIs), which are devices that allow communication between the brain and external devices like a prosthetic arm or a keyboard. BCIs are poised to have significant impacts on public health, society, and national security. This research presents the first analytical framework that attempts to predict the dissemination of neurotechnologies to both the commercial and military sectors in the United States and China. While China started its project later with less funding, we find that it has other advantages that make earlier adoption more likely. We also articulate national security risks implicit in later adoption, including the inability to set international ethical and legal norms for BCI use, especially in wartime operating environments, and data privacy risks for citizens who use technology developed by foreign actors.

Iterative Covariance-Based Removal of Time-Synchronous Artifacts: Application to Gastrointestinal Electrical Recordings.

OBJECTIVE: The aim of this study was to develop, validate, and apply a fully automated method for reducing large temporally synchronous artifacts present in electrical recordings made from the gastrointestinal (GI) serosa, which are problematic for properly assessing slow wave dynamics. Such artifacts routinely arise in experimental and clinical settings from motion, switching behavior of medical instruments, or electrode array manipulation. METHODS: A novel iterative Covariance-Based Reduction of Artifacts (COBRA) algorithm sequentially reduced artifact waveforms using an updating across-channel median as a noise template, scaled and subtracted from each channel based on their covariance. RESULTS: Application of COBRA substantially increased the signal-to-artifact ratio (12.8 ± 2.5 dB), while minimally attenuating the energy of the underlying source signal by 7.9% on average ( -11.1 ± 3.9 dB). CONCLUSION: COBRA was shown to be highly effective for aiding recovery and accurate marking of slow wave events (sensitivity = 0.90 ± 0.04; positive-predictive value = 0.74 ± 0.08) from large segments of in vivo porcine GI electrical mapping data that would otherwise be lost due to a broad range of contaminating artifact waveforms. SIGNIFICANCE: Strongly reducing artifacts with COBRA ultimately allowed for rapid production of accurate isochronal activation maps detailing the dynamics of slow wave propagation in the porcine intestine. Such mapping studies can help characterize differences between normal and dysrhythmic events, which have been associated with GI abnormalities, such as intestinal ischemia and gastroparesis. The COBRA method may be generally applicable for removing temporally synchronous artifacts in other biosignal processing domains.

Determining the efficient inter-electrode distance for high-resolution mapping using a mathematical model of human gastric dysrhythmias.

Motility of the stomach is in part coordinated by an electrophysiological event called slow waves, which are generated by pacemaker cells called the interstitial cells of Cajal (ICC). In functional motility disorders, which can be associated with a reduction of ICC, dynamic slow wave dysrhythmias can occur. In recent years, high-resolution (HR) mapping techniques have been applied to describe both normal and dysrhythmic slow wave patterns. The main aim of this study was to inform gastric HR mapping array design by determining the efficient inter-electrode distance required to accurately capture normal and dysrhythmic gastric slow wave activity. A two-dimensional mathematical model was used to simulate normal activity and four types of reported slow wave dysrhythmias in human patients: ectopic activation, retrograde propagation, slow conduction, conduction block. For each case, the simulated data were re-sampled at 4, 6, 10, 12, 20 and 30mm inter-electrode distances. The accuracy of each distance was compared to a reference set sampled at 2mm inter-electrode distance, in terms of accuracy of velocity, using an ANOVA. Manual groupings were also conducted to test the ability of the human markers to distinguish separate cycles of slow waves as inter-electrode distance increases. The largest interelectrode distance for human gastric slow wave analysis, which produced both accurate grouping and velocity, was 10mm (CI [0.3 2.4]mms(-1); p<;0.05). Therefore an inter-electrode distance of less than 10mm was required to accurately describe the types of baseline and dysrhythmic activities reported in this study. However, it is likely that more spatially complex dysrhythmias, such as re-entry, may require finer inter-electrode distances.