Biology subjects

Whitehead, S. C.

Publications and source records attributed to Whitehead, S. C..

7 recordsLinked to original sources

bioRxiv2025

How tp1, an indirect wing steering muscle, stabilizes Drosophila's flight

Flapping flight is inherently unstable, requiring Drosophila to fine-tune their wing motions on a milliseconds timescale. Pioneering studies have shown that the direct steering muscles, which attach to the wing hinge, are important for generating these rapid flight reflexes. Recent connectome data, however, reveal that indirect steering muscles or tension muscles, which alter the mechanics of the thorax, receive some of the same synaptic inputs from the sensory apparatus as the direct steering muscles. This discovery suggests that the indirect steering muscles may also be important for flight control. Here, we show that the indirect tergopleural muscles indeed contribute substantially to stabilization, particularly for large pitch perturbations. We find that for small perturbations (less than 1000 deg/s), flies modulate their wing stroke amplitude to generate lift-based corrective torques, a strategy that has been previously documented. For larger perturbations, however, we observe that Drosophila engage an additional wing degree of freedom--the wing pitch angle--to leverage additional lift and drag forces during the corrective maneuver. Quasi-steady aerodynamic simulations reveal that this strategy minimizes power consumption, anaolgous to how some mammals (including humans) adjust their steady-state gaits in a near energy-optimal manner. Using optogenetics and a control theory framework we demonstrate that the tergopleural muscle is activated by a proportional gain component of a nonlinear PI controller responsible for determining the wing pitch angle during large perturbations. A simplified torsional-spring model for the wing hinge captures the changes in the wing pitch dynamics observed during correction maneuvers by using the tergopleural muscle to adjust the rest angle of the wing. These findings provide a striking example of reflex strategy selection in time-critical behaviors and underscores the vital role of indirect steering muscles in flight stabilization.

neuroscience↗

bioRxiv2025

A multi-muscular, redundant strategy for free-flight roll stability

Whether recovering after a gust of wind, or rapidly saccading away from an oncoming predator, fruit flies show remarkable aerial dexterity about their body roll axis. Here, we investigated the detailed wing kinematic changes during free-flight roll motion and probed the neuromuscular basis for such changes. Consistent with previous work, we observed that flies manipulated the stroke amplitude difference between their wings to control their roll angle. Here, we show that flies are capable of achieving such changes by altering the stroke amplitude of either or both of their wings. Further we found that during corrections flies can also take advantage of an aerodynamically significant change in the angle of attack of their uppermost wing. Curiously, these corrective wing changes cannot be eliminated when motor neurons hypothesized to be used during roll maneuvers (i1, i2, b1, b2, and b3) are individually inhibited. However, free-flight optogenetic manipulations and quasi-steady aerodynamic calculations show that each of these motor neurons individually can effect kinematic changes consistent with a roll correction. Combining this evidence with an analysis of haltere inputs found in the BANC connectome, we propose that the observed robustness could be the result of two sets of muscular redundancies that receive shared inputs from haltere sensory afferents: one set, containing b1 and b2, is able to increase the stroke amplitude of the lower wing; while the other set, containing i1, i2, and b3, is able to decrease the stroke amplitude and wing pitch angle of the upper wing. Because of the redundancy in the input sensory information and output wing motion in the muscles in each cluster, the fly is able to perform roll stability maneuvers even when one of the constituent motor neurons is inhibited. This framework proposes new ways fast aerial maneuverability can be implemented when dealing with the flys most unstable rotational degree of freedom.

animal behavior and cognition↗

bioRxiv2024

Exploration-exploitation trade-off is regulated by metabolic state and taste value in Drosophila

Similar to other animals, the fly, Drosophila melanogaster, changes its foraging strategy from exploration to exploitation upon encountering a nutrient-rich food source. However, the impact of metabolic state or taste/nutrient value on exploration vs. exploitation decisions in flies is poorly understood. Here, we developed a one-source foraging assay that uses automated video tracking coupled with high-resolution measurements of food ingestion to investigate the behavioral variables flies use when foraging for food with different taste/caloric values and when in different metabolic states. We found that flies alter their foraging and ingestive behaviors based on their hunger state and the concentration of the sucrose solution. Interestingly, sugar-blind flies did not transition from exploration to exploitation upon finding a high-concentration sucrose solution, suggesting that taste sensory input, as opposed to post-ingestive nutrient feedback, plays a crucial role in determining the foraging decisions of flies. Using a Generalized Linear Model (GLM), we showed that hunger state and sugar volume ingested, but not the nutrient or taste value of the food, influence flies radial distance to the food source, a strong indicator of exploitation. Our behavioral paradigm and theoretical framework offer a promising avenue for investigating the neural mechanisms underlying state and value-based foraging decisions in flies, setting the stage for systematically identifying the neuronal circuits that drive these behaviors.

animal behavior and cognition↗

bioRxiv2023

Single-cell type analysis of wing premotor circuits in the ventral nerve cord of Drosophila melanogaster

To perform most behaviors, animals must send commands from higher-order processing centers in the brain to premotor circuits that reside in ganglia distinct from the brain, such as the mammalian spinal cord or insect ventral nerve cord. How these circuits are functionally organized to generate the great diversity of animal behavior remains unclear. An important first step in unraveling the organization of premotor circuits is to identify their constituent cell types and create tools to monitor and manipulate these with high specificity to assess their functions. This is possible in the tractable ventral nerve cord of the fly. To generate such a toolkit, we used a combinatorial genetic technique (split-GAL4) to create 195 sparse transgenic driver lines targeting 196 individual cell types in the ventral nerve cord. These included wing and haltere motoneurons, modulatory neurons, and interneurons. Using a combination of behavioral, developmental, and anatomical analyses, we systematically characterized the cell types targeted in our collection. In addition, we identified correspondences between the cells in this collection and a recent connectomic data set of the ventral nerve cord. Taken together, the resources and results presented here form a powerful toolkit for future investigations of neuronal circuits and connectivity of premotor circuits while linking them to behavioral outputs.

neuroscience↗

bioRxiv2022

Neuromuscular embodiment of feedback control elements in Drosophila flight

While insects like Drosophila are flying, aerodynamic instabilities require that they make millisecond-timescale adjustments to their wing motion to stay aloft and on course. These stabilization reflexes can be modeled as a proportional-integral (PI) controller; however, it is unclear how such control might be instantiated in insects at the level of muscles and neurons. Here, we show that the b1 and b2 motor units--prominent components of the flys steering muscles system--modulate specific elements of the PI controller: the angular displacement (integral, I) and angular velocity (proportional, P), respectively. Moreover, these effects are observed only during the stabilization of pitch. Our results provide evidence for an organizational principle in which each muscle contributes to a specific functional role in flight control, a finding that highlights the power of using top-down behavioral modeling to guide bottom-up cellular manipulation studies.

animal behavior and cognition↗

bioRxiv2019

Tongue Kinematics. Cortex-dependent corrections as the mouse tongue reaches for, and misses, targets

AbstractPrecise tongue control is necessary for drinking, eating, and vocalizing1, 2. Yet because tongue movements are fast and difficult to resolve, neural control of lingual kinematics remains poorly understood. Here we combine kilohertz frame-rate imaging and a deep learning based neural network to resolve 3D tongue kinematics in mice drinking from a water spout. Successful licks required previously unobserved corrective submovements (CSMs) which, like online corrections during primate reaches3-10, occurred after the tongue missed unseen, distant, or displaced targets. Photoinhibition of anterolateral motor cortex (ALM) impaired online corrections, resulting in hypometric licks that missed the spout. ALM neural activity reflected upcoming, ongoing, and past CSMs, as well as errors in predicted spout contact. Though less than a tenth of a second in duration, a single mouse lick exhibits hallmarks of online motor control associated with a primate reach, including cortex-dependent corrections after misses.

neuroscience↗

bioRxiv2018

Cortical control of kinematic primitives in mice performing a hold-still-center-out reach task

Motor sequences are constructed from primitives, hypothesized building blocks of movement, but mechanisms of primitive generation remain unclear. Using automated homecage training and a novel forelimb sensor, we trained freely-moving mice to initiate forelimb sequences with clearly resolved submillimeter-scale micromovements followed by millimeter-scale reaches to learned spatial targets. Hundreds of thousands of trajectories were decomposed into millions of kinematic primitives, while closed-loop photoinhibition was used to test roles of motor cortical areas. Inactivation of contralateral motor cortex reduced primitive peak speed but, surprisingly, did not substantially affect primitive direction, initiation, termination, or complexity, resulting in isomorphic, spatially contracted trajectories that undershot targets. Our findings demonstrate separable loss of a single kinematic parameter, speed, and identify conditions where loss of cortical drive reduces the gain of motor primitives but does not affect their generation, timing or direction. The combination of high precision forelimb sensing with automated training and neural manipulation provides a system for studying how motor sequences are constructed from elemental building blocks.

neuroscience↗