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Erginkaya, M.

Publications and source records attributed to Erginkaya, M..

6 recordsLinked to original sources

A dedicated brain circuit controls forward walking in Drosophila

Neural circuits in the brain control high-level parameters of movement, including the initiation, speed, and direction of locomotion. How specific cell types are organized into circuits to compute these control signals and enable context-appropriate behavior remains unclear. Here, we identify central brain neurons in Drosophila that can initiate walking and exert graded control over walking speed. Connectome analyses position the neurons on top of a layered brain circuit, which recruits a specific population of descending neurons to control forward walking independently of turning and other parameters. As predicted by the connectome, the circuit enforces straight walking when activated unilaterally, and the activity of the central brain neurons represents a high-level walking drive. This drive is suppressed during flight but flexibly integrated with other control signals to enable complex movement sequences during obstacle negotiation. Together, our findings elucidate a dedicated brain circuit that enables efficient computation, selection, and integration of forward-walking signals for context-appropriate motor control.

neuroscience↗

Parallel neuronal ensembles control behavior across sensorimotor levels in Drosophila

Nervous systems can process information in serial or in parallel, trading off efficiency for flexibility and speed. How these network architectures are implemented across sensorimotor pathways to control behavior is unclear. We investigate this tradeoff directly in Drosophila by comparing neuronal circuits underlying landing and takeoff, behaviors transforming similar visual cues to whole-body motor output. Using a whole-CNS connectome, electrophysiology, and behavioral analysis, we reconstruct the complete feedforward pathway for landing, including visual feature detectors, a dedicated ensemble of descending neurons (DNs), and a core premotor circuit in the nerve cord. Comparison to the takeoff pathway reveals that, despite encoding the same sensory feature and engaging similar muscle groups, neuronal circuits controlling the two behaviors are separated at every sensorimotor level. Extending this analysis to the complete DN population reveals a blueprint for descending motor control: DNs across the behavioral space utilized by the fly are organized as a set of parallel, loosely-overlapping ensembles that form a continuum from command-like control, with individual DNs determining behavioral output, to population coding, with multiple DNs controlling behavior synergistically. Distinct combinations of sensory feature detectors differentially recruit DN ensembles to enable flexible, context-dependent behavioral control.

neuroscience↗

Control of walking direction by descending and dopaminergic neurons in Drosophila

Animals need to fine-control the speed and direction of locomotion to navigate complex and dynamic environments. To achieve this, they integrate multimodal sensory inputs with their internal drive to constantly adjust their motor output. This integration involves the interplay of neuronal populations across different hierarchical levels along the sensorimotor axis - from sensory, central, and modulatory neurons in the brain to descending neurons and motor networks in the nerve cord. Here, we characterize two populations of neurons that control distinct aspects of walking on different hierarchical levels in Drosophila. First, we use in-vivo electrophysiological recordings to demonstrate that moonwalker descending neurons (MDN) integrate antennal touch to drive changes in walking direction from forward to backward. Second, we establish DopaMeander as an important component in the control of forward walking through a combination of optogenetic activation, silencing, connectomics, and in-vivo recordings. These dopaminergic modulatory neurons drive forward walking with increased turning, and the activity of individual neurons is correlated with ipsiversive turning. Hence, MDN and DopaMeander control opposite regimes of walking on different hierarchical levels. Computational models reveal that their activity predicts key parameters of spontaneous walking. Moreover, we find that both MDN and DopaMeander are gated out during flight. This suggests that neuronal populations across levels of control are modulated by the behavioral state to minimize cross-talk between motor programs.

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A comprehensive neuroanatomical survey of the Drosophila Lobula Plate Tangential Neurons with predictions for their optic flow sensitivity

Flying insects exhibit remarkable navigational abilities controlled by their compact nervous systems. Optic flow, the pattern of changes in the visual scene induced by locomotion, is a crucial sensory cue for robust self-motion estimation, especially during rapid flight. Neurons that respond to specific, large-field optic flow patterns have been studied for decades, primarily in large flies, such as houseflies, blowflies, and hover flies. The best-known optic-flow sensitive neurons are the large tangential cells of the dipteran lobula plate, whose visual-motion responses, and to a lesser extent, their morphology, have been explored using single-neuron neurophysiology. Most of these studies have focused on the large, Horizontal and Vertical System neurons, yet the lobula plate houses a much larger set of optic-flow sensitive neurons, many of which have been challenging to unambiguously identify or to reliably target for functional studies. Here we report the comprehensive reconstruction and identification of the Lobula Plate Tangential Neurons in an Electron Microscopy (EM) volume of a whole Drosophila brain. This catalog of 58 LPT neurons (per brain hemisphere) contains many neurons that are described here for the first time and provides a basis for systematic investigation of the circuitry linking self-motion to locomotion control. Leveraging computational anatomy methods, we estimated the visual motion receptive fields of these neurons and compared their tuning to the visual consequence of body rotations and translational movements. We also matched these neurons, in most cases on a one-for-one basis, to stochastically labeled cells in genetic driver lines, to the mirror-symmetric neurons in the same EM brain volume, and to neurons in an additional EM data set. Using cell matches across data sets, we analyzed the integration of optic flow patterns by neurons downstream of the LPTs and find that most central brain neurons establish sharper selectivity for global optic flow patterns than their input neurons. Furthermore, we found that self-motion information extracted from optic flow is processed in distinct regions of the central brain, pointing to diverse foci for the generation of visual behaviors.

neuroscience↗

A competitive disinhibitory network for robust optic flow processing in Drosophila

Many animals rely on optic flow for navigation, using differences in eye image velocity to detect deviations from their intended direction of travel. However, asymmetries in image velocity between the eyes are often overshadowed by strong, symmetric translational optic flow during navigation. Yet, the brain efficiently extracts these asymmetries for course control. While optic flow sensitive-neurons have been found in many animal species, far less is known about the postsynaptic circuits that support such robust optic flow processing. In the fly Drosophila melanogaster, a group of neurons called the horizontal system (HS) are involved in course control during high-speed translation. To understand how HS cells facilitate robust optic flow processing, we identified central networks that connect to HS cells using full brain electron microscopy datasets. These networks comprise three layers: convergent inputs from different, optic flow-sensitive cells, a middle layer with reciprocal, and lateral inhibitory interactions among different interneuron classes, and divergent output projecting to both the ventral nerve cord (equivalent to the vertebrate spinal cord), and to deeper regions of the fly brain. By combining two-photon optical imaging to monitor free calcium dynamics, manipulating GABA receptors and modeling, we found that lateral disinhibition between brain hemispheres enhance the selectivity to rotational visual flow at the output layer of the network. Moreover, asymmetric manipulations of interneurons and their descending outputs induce drifts during high-speed walking, confirming their contribution to steering control. Together, these findings highlight the importance of competitive disinhibition as a critical circuit mechanism for robust processing of optic flow, which likely influences course control and heading perception, both critical functions supporting navigation.

neuroscience↗

Organization of an Ascending Circuit that Conveys Flight Motor State

Natural behaviors are a coordinated symphony of motor acts which drive self-induced or reafferent sensory activation. Single sensors only signal presence and magnitude of a sensory cue; they cannot disambiguate exafferent (externally-induced) from reafferent sources. Nevertheless, animals readily differentiate between these sources of sensory signals to make appropriate decisions and initiate adaptive behavioral outcomes. This is mediated by predictive motor signaling mechanisms, which emanate from motor control pathways to sensory processing pathways, but how predictive motor signaling circuits function at the cellular and synaptic level is poorly understood. We use a variety of techniques, including connectomics from both male and female electron microscopy volumes, transcriptomics, neuroanatomical, physiological and behavioral approaches to resolve the network architecture of two pairs of ascending histaminergic neurons (AHNs), which putatively provide predictive motor signals to several sensory and motor neuropil. Both AHN pairs receive input primarily from an overlapping population of descending neurons, many of which drive wing motor output. The two AHN pairs target almost exclusively non-overlapping downstream neural networks including those that process visual, auditory and mechanosensory information as well as networks coordinating wing, haltere, and leg motor output. These results support the conclusion that the AHN pairs multi-task, integrating a large amount of common input, then tile their output in the brain, providing predictive motor signals to non-overlapping sensory networks affecting motor control both directly and indirectly.

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