Cell types and coincident synapses in the ellipsoid body of Drosophila (original) (raw)

Targeted expression of tetanus toxin reveals sets of neurons involved in larval locomotion in Drosophila

Journal of Neurobiology, 2003

The Drosophila larva is widely used for studies of neuronal development and function, yet little is known about the neuronal basis of locomotion in this model organism. Drosophila larvae crawl over a plain substrate by performing repetitive waves of forward peristalsis alternated by brief episodes of head swinging and turning. To identify sets of central and peripheral neurons required for the spatial or temporal pattern of larval locomotion, we blocked neurotransmitter release from defined populations of neurons by targeted expression of tetanus toxin light chain (TeTxLC) with the GAL4/UAS system. One hundred fifty GAL4 lines were crossed to a UAS-TeTxLC strain and a motion-analysis system was used to identify larvae with abnormal movement patterns. Five lines were selected that show discrete locomotor defects (i.e., increased turning and pausing) and these defects are correlated with diverse sets of central neurons. One line, 4C-GAL4, caused an unusual circling behavior that is correlated with approximately 200 neurons, including dopaminergic and peptidergic interneurons. Expression of TeTxLC in all dopaminergic and serotonergic but not in peptidergic neurons, caused turning deficits that are similar to those of 4C-GAL4/TeTxLC larvae. The results presented here provide a basis for future genetic studies of motor control in the Drosophila larva.

Neural circuits driving larval locomotion in Drosophila

Neural development, 2018

More than 30 years of studies into Drosophila melanogaster neurogenesis have revealed fundamental insights into our understanding of axon guidance mechanisms, neural differentiation, and early cell fate decisions. What is less understood is how a group of neurons from disparate anterior-posterior axial positions, lineages and developmental periods of neurogenesis coalesce to form a functional circuit. Using neurogenetic techniques developed in Drosophila it is now possible to study the neural substrates of behavior at single cell resolution. New mapping tools described in this review, allow researchers to chart neural connectivity to better understand how an anatomically simple organism performs complex behaviors.

The Drosophila Larval Locomotor Circuit Provides a Model to Understand Neural Circuit Development and Function

Frontiers in Neural Circuits, 2021

It is difficult to answer important questions in neuroscience, such as: “how do neural circuits generate behaviour?,” because research is limited by the complexity and inaccessibility of the mammalian nervous system. Invertebrate model organisms offer simpler networks that are easier to manipulate. As a result, much of what we know about the development of neural circuits is derived from work in crustaceans, nematode worms and arguably most of all, the fruit fly, Drosophila melanogaster. This review aims to demonstrate the utility of the Drosophila larval locomotor network as a model circuit, to those who do not usually use the fly in their work. This utility is explored first by discussion of the relatively complete connectome associated with one identified interneuron of the locomotor circuit, A27h, and relating it to similar circuits in mammals. Next, it is developed by examining its application to study two important areas of neuroscience research: critical periods of developmen...

Anatomy and Neural Pathways Modulating Distinct Locomotor Behaviors in Drosophila Larva

Biology

The control of movements is a fundamental feature shared by all animals. At the most basic level, simple movements are generated by coordinated neural activity and muscle contraction patterns that are controlled by the central nervous system. How behavioral responses to various sensory inputs are processed and integrated by the downstream neural network to produce flexible and adaptive behaviors remains an intense area of investigation in many laboratories. Due to recent advances in experimental techniques, many fundamental neural pathways underlying animal movements have now been elucidated. For example, while the role of motor neurons in locomotion has been studied in great detail, the roles of interneurons in animal movements in both basic and noxious environments have only recently been realized. However, the genetic and transmitter identities of many of these interneurons remains unclear. In this review, we provide an overview of the underlying circuitry and neural pathways req...

Neuronal constituents and putative interactions within the Drosophila ellipsoid body neuropil

2018

The central complex (CX) is a midline-situated collection of neuropil compartments in the arthropod central brain, implicated in higher-order processes such as goal-directed navigation. Here, we provide a systematic genetic-neuroanatomical analysis of the ellipsoid body (EB), a compartment which represents a major afferent portal of the Drosophila CX. The neuropil volume of the EB, along with its prominent input compartment, called the bulb, is subdivided into precisely tessellated domains, distinguishable based on intensity of the global marker DN-cadherin. EB tangential elements (so-called ring neurons), most of which are derived from the DALv2 neuroblast lineage, interconnect the bulb and EB domains in a topographically-organized fashion. Using the DN-cadherin domains as a framework, we first characterized the bulb-EB connectivity by Gal4 driver lines expressed in different DALv2 ring neuron (R-neuron) subclasses. We identified 11 subclasses, 6 of which correspond to previously d...

The effects of ER morphology on synaptic structure and function in Drosophila melanogaster

Journal of cell science, 2016

Hereditary Spastic Paraplegia (HSP) is a set of genetic diseases caused by mutations in one of 72 genes that results in age-dependent corticospinal axon degeneration accompanied by spasticity and paralysis. Two genes implicated in HSPs encode proteins that regulate ER morphology. Atlastin (SPG3A) encodes an ER membrane fusion GTPase and Reticulon 2 (SPG12) helps shape ER tube formation. Here we use a new fluorescent ER marker to show that the ER within wildtype Drosophila motor nerve terminals forms a network of tubules that is fragmented and made diffuse by atl loss. atl or Rtnl1 loss decreases evoked transmitter release and increases arborization. Similarly to other HSP genes, atl inhibits bone morphogenetic protein (BMP) signaling, and loss of atl causes age-dependent locomotor deficits in adults. These results demonstrate a critical role for ER in neuronal function and identify mechanistic links between ER morphology, neuronal function, BMP signaling, and adult behavior.

A subset of interneurons required for Drosophila larval locomotion

Molecular and cellular neurosciences, 2015

Efforts to define the neural circuits generating locomotor behavior have produced an initial understanding of some of the components within the spinal cord, as well as a basic understanding of several invertebrate motor pattern generators. However, how these circuits are assembled during development is poorly understood. We are defining the neural circuit that generates larval locomotion in the genetically tractable fruit fly Drosophila melanogaster to study locomotor circuit development. Forward larval locomotion involves a stereotyped posterior-to-anterior segmental translocation of body wall muscle contraction and is generated by a relatively small number of identified muscles, motor and sensory neurons, plus an unknown number of the ~270 bilaterally-paired interneurons per segment of the 1st instar larva. To begin identifying the relevant interneurons, we have conditionally inactivated synaptic transmission of interneuron subsets and assayed for the effects on locomotion. From t...

Electrophysiological and Morphological Characterization of Identified Motor Neurons in the Drosophila Third Instar Larva Central Nervous System

Journal of Neurophysiology, 2004

Electrophysiological and morphological characterization of identified motor neurons in the Drosophila third instar larva central nervous system. . We have used dye fills and electrophysiological recordings to identify and characterize a cluster of motor neurons in the third instar larval ventral ganglion. This cluster of neurons is similar in position to the well-studied embryonic RP neurons. Dye fills of larval dorsomedial neurons demonstrate that individual neurons within the cluster can be reproducibly identified by observing their muscle targets and bouton morphology. The terminal targets of these five neurons are body wall muscles 6/7, 1, 14, and 30 and the intersegmental nerve (ISN) terminal muscles (1, 2, 3, 4, 9, 10, 19, 20). All cells except the ISN neuron, which has a type Is ending, display type Ib boutons. Two of these neurons appear to be identical to the embryonic RP3 and aCC cells, which define the most proximal and distal innervations within a hemisegment. The targets of the other neurons in the larval dorsomedial cluster do not correspond to embryonic targets of the neurons in the RP cluster, suggesting rewiring of this circuit during early larval stages. Electrophysiological studies of the five neurons in current clamp revealed that type Is neurons have a longer delay in the appearance of the first spike compared with type Ib neurons. Genetic, biophysical, and pharmacological studies in current and voltage clamp show this delay is controlled by the kinetics and voltage sensitivity of inactivation of a current whose properties suggest that it may be the Shal I A current. The combination of genetic identification and whole cell recording allows us to directly explore the cellular substrates of neural and locomotor behavior in an intact system.