Biology subjects

Putney, J.

Publications and source records attributed to Putney, J..

5 recordsLinked to original sources

bioRxiv2023

Flight power muscles have a coordinated, causal role in controlling 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 consisting of every action potential controlling wing musculature, each muscle encodes significant information about movement in precise spike timing down to the millisecond scale. While individual muscles share information about movement, we do not yet know if they have separable effects on an animals motion, or if muscles functionally interact such that the effects of any muscles timing depends heavily on the state of the entire musculature. To answer these questions, we performed spike-resolution electromyography and precise stimulation of individual spikes in the hawkmoth Manduca sexta during tethered flapping. We specifically explored how the flight power muscles themselves may contribute to pitch control which is necessary to stabilize flight. Combining correlational study of visually-induced turns with causal manipulation of spike timing, we discovered likely coordination patterns for pitch turns, investigated if these correlational patterns can individually drive pitch control, and studied whether the precise spike timing of indirect power muscles can lead to pitch maneuvers. We observed significant timing change of the main downstroke muscles, the dorsolongitudinal muscles (DLMs), associated with whether a moth was pitching up or down. Causally inducing this timing change in the DLMs with electrical stimulation produced a consistent, mechanically relevant feature in pitch torque, establishing that indirect power muscles in Manduca have a control role in pitch. Because changes were evoked in unconstrained flapping 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. Summary StatementWe investigate how individual muscles contribute to flight by manipulating muscle timing in behaving hawkmoths. We find precise timing of single muscles does not produce precise turns, highlighting the importance of coordination across the entire motor program.

neuroscience↗

bioRxiv2023

Cross-subject Mapping of Neural Activity with Restricted Boltzmann Machines

Subject-to-subject variability is a common challenge in generalizing neural data models across subjects. While many methods exist that map one subject to another, it remains challenging to combine many subjects in a computationally efficient manner, especially with features that are highly non-linear such as when considering populations of spiking neurons or motor units. Our objective is to transfer data from one or more target subjects to the data space of one or more source subject(s) such that the neural decoder of the source subject can directly decode the target data when the source(s) is not available during test time. We propose to use the Gaussian-Bernoulli Restricted Boltzmann Machine (RBM); once trained over the entire set of subjects, the RBM allows the mapping of target features on source feature spaces using Gibbs sampling. We also consider a novel computationally efficient training technique for RBMs based on the minimization of the Fisher divergence, which allows the gradients of the RBM to be computed in closed form, in contrast to the more traditional contrastive divergence. We apply our methods to decode turning behaviors from a comprehensive spike-resolved motor program - neuromuscular recordings of spike trains from the ten muscles that control wing motion in an agile flying Manduca sexta. The dataset consists of the comprehensive motor program recorded from nine subjects driven by six discrete visual stimuli. The evaluations show that the target features can be decoded using the source classifier with an accuracy of up to 95% when mapped using an RBM trained by Fisher divergence. Significant StatementIn this study, we address the variability of neural data across subjects, which is a significant obstacle in developing models that can generalize across subjects. Our objective is to create a task-specific representation of the target subject signal in the feature space of the source subject. Our proposed RBM architectures achieve highly flexible and accurate cross-subject mapping with few assumptions. Our Fisher RBM improved the previous state of the art method by 300%. Our methods show promise in generalizing features of complex neural datasets across individuals, tuning neural interfaces to subject-specific features, and leveraging data across multiple subjects when experiments are limited in time or completeness.

neuroscience↗

bioRxiv2021

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 temporally precise code. There is now a growing appreciation for the prevalence of precise timing encoding in motor systems. Animals from moths to birds control motor outputs using precise spike timing, but 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 relatively few methods for assessing spike timing precision. 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 a data set of simultaneous turning (yaw) torque output and EMG recordings from the 10 primary muscles of Manduca sexta as tethered moths visually tracked a robotic flower moving with a 1 Hz sinusoidal trajectory. 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 receive information encoded at different levels of precision. Using the continuous MI method, 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.

neuroscience↗

bioRxiv2021

Consistent coordination patterns provide near perfect behavior decoding in a comprehensive motor program for insect flight

Patterns of motor activity can be used to decode behavior state. Precise spike timing encoding is present in many motor systems, but is not frequently utilized to decode behavior or to examine how coordination is achieved across many motor units. Testing whether the same coordinated sets of muscles control different movements is difficult without a complete motor representation at the level of the currency of control - action potentials. Here, we demonstrate nearly perfect decoding of six hawk moth flight behaviors elicited in response to wide-field drifting visual stimuli about the flight axes - pitch, roll, and yaw - using a comprehensive, spike-resolved motor program and a simple linear decoding pipeline. A complex decoding scheme is not necessary, even if the functional patterns of control are nonlinear. We show that muscle covariation present in one pair of visual stimulus conditions can be used to decode behavior in a different pair of visual stimulus conditions, indicating the presence of conserved muscle coordination patterns at the level of motor neuronal timings in functionally distinct behaviors. We also demonstrate that as few as half the muscles can be used to retain decoding performance, linking coordination to redundancy in encoding, if not function, across the entire moth flight motor program.

neuroscience↗

bioRxiv2019

Timing is (almost) everything in 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 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.

neuroscience↗