Neuromuscular basis of Drosophila larval rolling escape behavior.

When threatened by dangerous or harmful stimuli, animals engage in diverse forms of rapid escape behaviors. In Drosophila larvae, one type of escape response involves C-shaped bending and lateral rolling followed by rapid forward crawling. The sensory circuitry that promotes larval escape has been extensively characterized; however, the motor programs underlying rolling are unknown. Here, we characterize the neuromuscular basis of rolling escape behavior. We used high-speed, volumetric, Swept Confocally Aligned Planar Excitation (SCAPE) microscopy to image muscle activity during larval rolling. Unlike sequential peristaltic muscle contractions that progress from segment to segment during forward and backward crawling, muscle activity progresses circumferentially during bending and rolling escape behavior. We propose that progression of muscular contraction around the larva's circumference results in a transient misalignment between weight and the ground support forces, which generates a torque that induces stabilizing body rotation. Therefore, successive cycles of slight misalignment followed by reactive aligning rotation lead to continuous rolling motion. Supporting our biomechanical model, we found that disrupting the activity of muscle groups undergoing circumferential contraction progression leads to rolling defects. We use EM connectome data to identify premotor to motor connectivity patterns that could drive rolling behavior and perform neural silencing approaches to demonstrate the crucial role of a group of glutamatergic premotor neurons in rolling. Our data reveal body-wide muscle activity patterns and putative premotor circuit organization for execution of the rolling escape response.

Axon-axon interactions determine modality-specific wiring and subcellular synaptic specificity in a somatosensory circuit.

Synaptic connections between neurons are often formed in precise subcellular regions of dendritic arbors with implications for information processing within neurons. Cell-cell interactions are widely important for circuit wiring; however, their role in subcellular specificity is not well understood. We studied the role of axon-axon interactions in precise targeting and subcellular wiring of Drosophila somatosensory circuitry. Axons of nociceptive and gentle touch neurons terminate in adjacent, non-overlapping layers in the central nervous system (CNS). Nociceptor and touch receptor axons synapse onto distinct dendritic regions of a second-order interneuron, the dendrites of which span these layers, forming touch-specific and nociceptive-specific connectivity. We found that nociceptor ablation elicited extension of touch receptor axons and presynapses into the nociceptor recipient region, supporting a role for axon-axon interactions in somatosensory wiring. Conversely, touch receptor ablation did not lead to expansion of nociceptor axons, consistent with unidirectional axon-axon interactions. Live imaging provided evidence for sequential arborization of nociceptive and touch neuron axons in the CNS. We propose that axon-axon interactions and modality-specific timing of axon targeting play key roles in subcellular connection specificity of somatosensory circuitry.

Neuromuscular Basis of Drosophila larval rolling escape behavior.

When threatened by dangerous or harmful stimuli, animals engage in diverse forms of rapid escape behaviors. In Drosophila larvae, one type of escape response involves C-shaped bending and lateral rolling followed by rapid forward crawling. The sensory circuitry that promotes larval escape has been extensively characterized; however, the motor programs underlying rolling are unknown. Here, we characterize the neuromuscular basis of rolling escape behavior. We used high-speed, volumetric, Swept Confocally-Aligned Planar Excitation (SCAPE) microscopy to image muscle activity during larval rolling. Unlike sequential peristaltic muscle contractions that progress from segment to segment during forward and backward crawling, the muscle activity progresses circumferentially during bending and rolling escape behavior. We propose that progression of muscular contraction around the larval circumference results in a transient misalignment between weight and the ground support forces, which generates a torque that induces stabilizing body rotation. Therefore, successive cycles of slight misalignment followed by reactive aligning rotation lead to continuous rolling motion. Supporting our biomechanical model, we found that disrupting the activity of muscle groups undergoing circumferential contraction progression lead to rolling defects. We use EM connectome data to identify premotor to motor connectivity patterns that could drive rolling behavior, and perform neural silencing approaches to demonstrate the crucial role of a group of glutamatergic premotor neurons in rolling. Our data reveal body-wide muscle activity patterns and putative premotor circuit organization for execution of the rolling escape response.