Abstract
Rhythmic motor patterns underlying many types of locomotion are thought to be produced by central pattern generators (CPGs). Our knowledge of how CPG networks generate motor patterns in complex nervous systems remains incomplete, despite decades of work in a variety of model organisms. Substrate borne locomotion in Drosophila larvae is driven by waves of muscular contraction that propagate through multiple body segments. We use the motor circuitry underlying crawling in larval Drosophila as a model to try to understand how segmentally coordinated rhythmic motor patterns are generated. Whereas muscles, motoneurons and sensory neurons have been well investigated in this system, far less is known about the identities and function of interneurons. Our recent study identified a class of glutamatergic premotor interneurons, PMSIs (period-positive median segmental interneurons), that regulate the speed of locomotion. Here, we report on the identification of a distinct class of glutamatergic premotor interneurons called Glutamatergic Ventro-Lateral Interneurons (GVLIs). We used calcium imaging to search for interneurons that show rhythmic activity and identified GVLIs as interneurons showing wave-like activity during peristalsis. Paired GVLIs were present in each abdominal segment A1-A7 and locally extended an axon towards a dorsal neuropile region, where they formed GRASP-positive putative synaptic contacts with motoneurons. The interneurons expressed vesicular glutamate transporter (vGluT) and thus likely secrete glutamate, a neurotransmitter known to inhibit motoneurons. These anatomical results suggest that GVLIs are premotor interneurons that locally inhibit motoneurons in the same segment. Consistent with this, optogenetic activation of GVLIs with the red-shifted channelrhodopsin, CsChrimson ceased ongoing peristalsis in crawling larvae. Simultaneous calcium imaging of the activity of GVLIs and motoneurons showed that GVLIs’ wave-like activity lagged behind that of motoneurons by several segments. Thus, GVLIs are activated when the front of a forward motor wave reaches the second or third anterior segment. We propose that GVLIs are part of the feedback inhibition system that terminates motor activity once the front of the motor wave proceeds to anterior segments.
Highlights
Rhythmic movements, such as walking, swimming, and flying, are commonly driven by neural networks known as central pattern generators (CPGs)
As interneurons that exhibit wave-like activity similar to motor activity generating muscle contraction waves are likely to play important functional roles in this locomotor network, we used calcium imaging to search for Gal4 lines which drive expression in interneurons that show such activity patterns
We focus on one of them, termed Glutamatergic Ventro-Lateral Interneurons (GVLIs), a pair of neurons in each abdominal segment in A1-A7, which were identified by two independent Gal4 lines, R26F05- and R26A08-Gal4
Summary
Rhythmic movements, such as walking, swimming, and flying, are commonly driven by neural networks known as central pattern generators (CPGs). CPG networks consist of interconnected interneurons that generate motor patterns underlying rhythmic behaviors. Since interneurons and their neurites are densely packed in the central nervous system (CNS), it has been extremely difficult in many animals to identify these interneurons and clarify their properties and function. In Drosophila, more than 1000 Gal lines are available that allow for transgene expression in small subsets of neurons [19]; these resources enable Drosophila researchers to characterize the function of single identified interneurons within CPG networks consisting of thousands of neurons
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