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

Abstract

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.

Cross-subject Mapping of Neural Activity with Restricted Boltzmann Machines

“…The diagrams also show the confidence ellipses corresponding to one standard deviation for each of the conditions. It can be clearly observed that the data demonstrates strong separability properties even in the first two dimensions of the PCA-based feature space; adding more features (i.e., PCA modes) only increases this separability in the higher-dimensional feature space for each moth as we have observed in our past work [16]; for more details, we advise the interested reader to refer to [16] where the feature extraction procedure was first proposed and its performance thoroughly analyzed.…”

“…We study a comprehensive flight motor program for hawk moths. We will describe the experimental protocol and related procedures only briefly here; the interested reader is referred to [16] where the data set was first published for more details. The subjects, i.e., the moths are tethered inside a three-sided box formed by computer monitors displaying the visual stimuli.…”

“…The spheres drift at a constant velocity of 100 • per second, corresponding to a temporal frequency of 5 cycles/second. Moreover, the spheres also drift in opposite directions about the three April 13, 2023 9/19 axes of rotation which result in 6 different visual stimuli also known as pitch (up, down), roll (left, right), and yaw (left, right) [16].…”

“…The objective is to decode the visual stimulus from the comprehensive motor program recordings, i.e., the spike trains. The subject-specific formulation of the problem where the neural decoder (classifier) is both trained and tested on the same subject was analyzed in [16]. Here, we study the performance of the neural decoder in cross-subject settings, where the test data originates from the source subjects whereas the classifier is trained on destination subject data.…”

“…In Section 5, we evaluate the performance of our method for cross-subject decoding of discrete visual stimulus conditions using the spiking activity of the motor program, specifically the set of spiking motor units, in nine hawk moths [16]. Each moth is exposed to the same set of six visual stimuli and the neuromuscular activity is collected April 13, 2023 2/19 in the form of spike trains extracted from fine wire electromyography (EMGs) of the ten primary flight muscles that control the wings, resulting in a comprehensive, spike-resolved motor program [17].…”