Descending Neurons Research Articles

Descending networks transform command signals into population motor control

To convert intentions into actions, movement instructions must pass from the brain to downstream motor circuits through descending neurons (DNs). These include small sets of command-like neurons that are sufficient to drive behaviours1—the circuit mechanisms for which remain unclear. Here we show that command-like DNs in Drosophila directly recruit networks of additional DNs to orchestrate behaviours that require the active control of numerous body parts. Specifically, we found that command-like DNs previously thought to drive behaviours alone2–4 in fact co-activate larger populations of DNs. Connectome analyses and experimental manipulations revealed that this functional recruitment can be explained by direct excitatory connections between command-like DNs and networks of interconnected DNs in the brain. Descending population recruitment is necessary for behavioural control: DNs with many downstream descending partners require network co-activation to drive complete behaviours and drive only simple stereotyped movements in their absence. These DN networks reside within behaviour-specific clusters that inhibit one another. These results support a mechanism for command-like descending control in which behaviours are generated through the recruitment of increasingly large DN networks that compose behaviours by combining multiple motor subroutines.

Azimuthal invariance to looming stimuli in the Drosophila giant fiber escape circuit.

Spatially invariant feature detection is a property of many visual systems that rely on visual information provided by two eyes. However, how information across both eyes is integrated for invariant feature detection is not fully understood. Here, we investigated spatial invariance of looming responses in descending neurons (DNs) of Drosophila melanogaster. We found that multiple looming responsive DNs integrate looming information across both eyes, even though their dendrites are restricted to a single visual hemisphere. One DN, the giant fiber (GF), responds invariantly to looming stimuli across tested azimuthal locations. We confirmed visual information propagates to the GF from the contralateral eye, through an unidentified pathway, and demonstrated that the absence of this pathway alters GF responses to looming stimuli presented to the ipsilateral eye. Our data highlight a role for bilateral visual integration in generating consistent, looming-evoked escape responses that are robust across different stimulus locations and parameters.

Distribution and Organization of Descending Neurons in the Brain of Adult Helicoverpa armigera (Insecta).

The descending neurons (DNs) of insects connect the brain and thoracic ganglia and play a key role in controlling insect behaviors. Here, a comprehensive investigation of the distribution and organization of the DNs in the brain of Helicoverpa armigera (Hübner) was made by using backfilling from the neck connective combined with immunostaining techniques. The maximum number of DN somata labeled in H. armigera was about 980 in males and 840 in females, indicating a sexual difference in DNs. All somata of DNs in H. armigera were classified into six different clusters, and the cluster of DNd was only found in males. The processes of stained neurons in H. armigera were mainly found in the ventral central brain, including in the posterior slope, ventral lateral protocerebrum, lateral accessory lobe, antennal mechanosensory and motor center, gnathal ganglion and other small periesophageal neuropils. These results indicate that the posterior ventral part of the brain is vital for regulating locomotion in insects. These findings provide a detailed description of DNs in the brain that could contribute to investigations on the neural mechanism of moth behaviors.

Descending neuron population dynamics during odor-evoked and spontaneous limb-dependent behaviors.

Deciphering how the brain regulates motor circuits to control complex behaviors is an important, long-standing challenge in neuroscience. In the fly, Drosophila melanogaster, this is coordinated by a population of ~ 1100 descending neurons (DNs). Activating only a few DNs is known to be sufficient to drive complex behaviors like walking and grooming. However, what additional role the larger population of DNs plays during natural behaviors remains largely unknown. For example, they may modulate core behavioral commands or comprise parallel pathways that are engaged depending on sensory context. We evaluated these possibilities by recording populations of nearly 100 DNs in individual tethered flies while they generated limb-dependent behaviors, including walking and grooming. We found that the largest fraction of recorded DNs encode walking while fewer are active during head grooming and resting. A large fraction of walk-encoding DNs encode turning and far fewer weakly encode speed. Although odor context does not determine which behavior-encoding DNs are recruited, a few DNs encode odors rather than behaviors. Lastly, we illustrate how one can identify individual neurons from DN population recordings by using their spatial, functional, and morphological properties. These results set the stage for a comprehensive, population-level understanding of how the brain's descending signals regulate complex motor actions.

Distributed control of motor circuits for backward walking in Drosophila

How do descending inputs from the brain control leg motor circuits to change how an animal walks? Conceptually, descending neurons are thought to function either as command-type neurons, in which a single type of descending neuron exerts a high-level control to elicit a coordinated change in motor output, or through a population coding mechanism, whereby a group of neurons, each with local effects, act in combination to elicit a global motor response. The Drosophila Moonwalker Descending Neurons (MDNs), which alter leg motor circuit dynamics so that the fly walks backwards, exemplify the command-type mechanism. Here, we identify several dozen MDN target neurons within the leg motor circuits, and show that two of them mediate distinct and highly-specific changes in leg muscle activity during backward walking: LBL40 neurons provide the hindleg power stroke during stance phase; LUL130 neurons lift the legs at the end of stance to initiate swing. Through these two effector neurons, MDN directly controls both the stance and swing phases of the backward stepping cycle. These findings suggest that command-type descending neurons can also operate through the distributed control of local motor circuits.

TwoLumps Ascending Neurons Mediate Touch-Evoked Reversal of Walking Direction in Drosophila.

External cues, including touch, enable walking animals to flexibly maneuver around obstacles and extricate themselves from dead-ends (for reviews, see [1-3]). In a screen for neurons that enable Drosophila melanogaster to retreat when it encounters a dead-end, we identified a pair of ascending neurons, the TwoLumps Ascending (TLA) neurons. Silencing TLA activity impairs backward locomotion, whereas optogenetic activation triggers backward walking. TLA-induced reversal is mediated in part by the Moonwalker Descending Neurons (MDNs) [4], which receive excitatory input from the TLAs. Silencing the TLAs decreases the extent to which freely walking flies back up upon encountering a physical barrier in the dark, and TLAs show calcium responses to optogenetic activation of neurons expressing the mechanosensory channel NOMPC. We infer that TLAs convey feedforward mechanosensory stimuli to transiently activate MDNs in response to anterior body touch.

State-dependent decoupling of sensory and motor circuits underlies behavioral flexibility in Drosophila.

An approaching predator and self-motion towards an object can generate similar looming patterns on the retina, but these situations demand different rapid responses. How central circuits flexibly process visual cues to activate appropriate, fast motor pathways remains unclear. Here, we identify two descending neuron (DN) types that control landing and contribute to visuomotor flexibility in Drosophila. For each, silencing impairs visually-evoked landing, activation drives landing, and spike rate determines leg extension amplitude. Critically, visual responses of both DNs are severely attenuated during non-flight periods, effectively decoupling visual stimuli from the landing motor pathway when landing is inappropriate. The flight-dependence mechanism differs between DN types. Octopamine exposure mimics flight effects in one, whereas the other likely receives neuronal feedback from flight motor circuits. Thus, this sensorimotor flexibility arises from distinct mechanisms for gating action-specific descending pathways, such that sensory and motor networks are coupled or decoupled according to the behavioral state.

Infra-anastomotic Innervation of Residual Aganglionic Distal Rectum After Pull-through Surgery for Hirschsprung Disease.

Descending neurons are important for intestinal reflex activities, including the recto-anal inhibitory reflex involved in normal defecation. Pull-through surgery for Hirschsprung disease results in the anastomosis of ganglionic bowel to native aganglionic rectum just superior to the internal anal sphincter, which potentially could allow for physiologically significant infra-anastomotic innervation. The density and distribution of intramuscular neuronal nitric oxide synthase (nNOS)- and mucosal calretinin-immunoreactive nerves were evaluated proximal and distal to the anastomosis in redo resection specimens after pull-through surgery for Hirschsprung disease. The findings were compared with data collected from cadaveric controls with no history of dysmotility and the distal aganglionic segments of primary rectal resections from patients with Hirschsprung disease. Native aganglionic rectum of Hirschsprung patients lacks the normal lush intramuscular nNOS- and mucosal calretinin-immunoreactive nerves present in normal bowel. In post-pull-through resection specimens obtained more than 7 months after pull-through surgery, nNOS- and calretinin-positive innervation is at least partially restored for variable distances up to 10 to 12 mm inferior to the anastomosis, respectively. Innervation of infra-anastomotic muscularis propria and mucosa in the aganglionic distal rectum occurs to a variable degree after pull-through surgery for Hirschsprung disease and may contribute to individual differences in postoperative obstructive symptoms. Strategies to enhance infra-anastomotic innervation may improve clinical outcome.

The functional organization of descending sensory-motor pathways in Drosophila.

In most animals, the brain controls the body via a set of descending neurons (DNs) that traverse the neck. DN activity activates, maintains or modulates locomotion and other behaviors. Individual DNs have been well-studied in species from insects to primates, but little is known about overall connectivity patterns across the DN population. We systematically investigated DN anatomy in Drosophila melanogaster and created over 100 transgenic lines targeting individual cell types. We identified roughly half of all Drosophila DNs and comprehensively map connectivity between sensory and motor neuropils in the brain and nerve cord, respectively. We find the nerve cord is a layered system of neuropils reflecting the fly's capability for two largely independent means of locomotion -- walking and flight -- using distinct sets of appendages. Our results reveal the basic functional map of descending pathways in flies and provide tools for systematic interrogation of neural circuits.

Descending neurons from the lateral accessory lobe and posterior slope in the brain of the silkmoth Bombyx mori

A population of descending neurons connect the brain and thoracic motor center, playing a critical role in controlling behavior. We examined the anatomical organization of descending neurons (DNs) in the brain of the silkmoth Bombyx mori. Moth pheromone orientation is a good model to investigate neuronal mechanisms of behavior. Based on mass staining and single-cell staining, we evaluated the anatomical organization of neurite distribution by DNs in the brain. Dense innervation was observed in the posterior–ventral part of the brain called the posterior slope (PS). We analyzed the morphology of DNs innervating the lateral accessory lobe (LAL), which is considered important for moth olfactory behavior. We observed that all LAL DNs also innervate the PS, suggesting the integration of signals from the LAL and PS. We also identified a set of DNs innervating the PS but not the LAL. These DNs were sensitive to the sex pheromone, suggesting a role of the PS in motor control for pheromone processing. Here we discuss the organization of descending pathways for pheromone orientation.

Organization of descending neurons in Drosophila melanogaster.

Neural processing in the brain controls behavior through descending neurons (DNs) - neurons which carry signals from the brain to the spinal cord (or thoracic ganglia in insects). Because DNs arise from multiple circuits in the brain, the numerical simplicity and availability of genetic tools make Drosophila a tractable model for understanding descending motor control. As a first step towards a comprehensive study of descending motor control, here we estimate the number and distribution of DNs in the Drosophila brain. We labeled DNs by backfilling them with dextran dye applied to the neck connective and estimated that there are ~1100 DNs distributed in 6 clusters in Drosophila. To assess the distribution of DNs by neurotransmitters, we labeled DNs in flies in which neurons expressing the major neurotransmitters were also labeled. We found DNs belonging to every neurotransmitter class we tested: acetylcholine, GABA, glutamate, serotonin, dopamine and octopamine. Both the major excitatory neurotransmitter (acetylcholine) and the major inhibitory neurotransmitter (GABA) are employed equally; this stands in contrast to vertebrate DNs which are predominantly excitatory. By comparing the distribution of DNs in Drosophila to those reported previously in other insects, we conclude that the organization of DNs in insects is highly conserved.

Activity in descending dopaminergic neurons represents but is not required for leg movements in the fruit fly Drosophila.

Modulatory descending neurons (DNs) that link the brain to body motor circuits, including dopaminergic DNs (DA-DNs), are thought to contribute to the flexible control of behavior. Dopamine elicits locomotor-like outputs and influences neuronal excitability in isolated body motor circuits over tens of seconds to minutes, but it remains unknown how and over what time scale DA-DN activity relates to movement in behaving animals. To address this question, we identified DA-DNs in the Drosophila brain and developed an electrophysiological preparation to record and manipulate the activity of these cells during behavior. We find that DA-DN spike rates are rapidly modulated during a subset of leg movements and scale with the total speed of ongoing leg movements, whether occurring spontaneously or in response to stimuli. However, activating DA-DNs does not elicit leg movements in intact flies, nor do acute bidirectional manipulations of DA-DN activity affect the probability or speed of leg movements over a time scale of seconds to minutes. Our findings indicate that in the context of intact descending control, changes in DA-DN activity are not sufficient to influence ongoing leg movements and open the door to studies investigating how these cells interact with other descending and local neuromodulatory inputs to influence body motor output.

Visual and mechanical sensory integration of descending neurons in Drosophila melanogaster

Event Abstract Back to Event Visual and mechanical sensory integration of descending neurons in Drosophila melanogaster Laiyong Mu1*, Kei Ito2, Jonathan Bacon3 and Nicholas Strausfeld1 1 University of Arizona, Neuroscience, United States 2 University of Tokyo, Japan 3 University of Sussex, United Kingdom Descending neurons from the brain either convey downstream commands or apply modulatory effect onto the thoracic motor centers, which then generate appropriate motor behaviors to varied environments including acute emergencies. They are organized as clusters in the deutocerebrum where each cluster shares a characteristic configuration of inputs from neurons relaying sensory information. Visual processing in insects involves a series of planar synaptic networks in the optic lobe, in which ensembles of lobula columnar neurons project to a deeper neuropil in deutocerebrum consisting of optic glomeruli. This region, the optic glomerular complex, is also known to contain the dendrites of many pre-motor descending neurons. However, it is still an open question how visual signals encoded by descending neurons are computed within the optic glomerular network and integrated with sensory information in other modalities. Genetic tools for Drosophila allow the expression of green fluorescent protein in certain descending neurons. Utilizing such specific GAL4 lines, we are able to record activities of those neurons in vivo with whole-cell patch clamp methods. Here, we first investigated multimodal sensory integration in the Giant Fiber (GF), which initiates jump-like escape responses and receives inputs from both mechanosensory afferents from the antennae and terminals of retinotopic neurons originating from the lobula. We then examined the responses of a number of other descending neurons labeled in different GAL4 lines to varied visual and mechanical sensory stimuli that have never been studied before. The results of these studies reveal functional characteristics of downstream signals encoded by Drosophila descending neurons and how these signals are established from the convergence of lobula outputs and relays carrying other sensory modalities. Keywords: Descending neuron, Drosophila, multimodal integration, optic glomerulus, Giant Fiber Conference: International Conference on Invertebrate Vision, Fjälkinge, Sweden, 1 Aug - 8 Aug, 2013. Presentation Type: Poster presentation preferred Topic: The visual control of flight and locomotion Citation: Mu L, Ito K, Bacon J and Strausfeld N (2019). Visual and mechanical sensory integration of descending neurons in Drosophila melanogaster. Front. Physiol. Conference Abstract: International Conference on Invertebrate Vision. doi: 10.3389/conf.fphys.2013.25.00014 Copyright: The abstracts in this collection have not been subject to any Frontiers peer review or checks, and are not endorsed by Frontiers. They are made available through the Frontiers publishing platform as a service to conference organizers and presenters. The copyright in the individual abstracts is owned by the author of each abstract or his/her employer unless otherwise stated. Each abstract, as well as the collection of abstracts, are published under a Creative Commons CC-BY 4.0 (attribution) licence (https://creativecommons.org/licenses/by/4.0/) and may thus be reproduced, translated, adapted and be the subject of derivative works provided the authors and Frontiers are attributed. For Frontiers’ terms and conditions please see https://www.frontiersin.org/legal/terms-and-conditions. Received: 15 Feb 2013; Published Online: 09 Dec 2019. * Correspondence: Dr. Laiyong Mu, University of Arizona, Neuroscience, Tucson, United States, mul@email.arizona.edu Login Required This action requires you to be registered with Frontiers and logged in. To register or login click here. Abstract Info Abstract The Authors in Frontiers Laiyong Mu Kei Ito Jonathan Bacon Nicholas Strausfeld Google Laiyong Mu Kei Ito Jonathan Bacon Nicholas Strausfeld Google Scholar Laiyong Mu Kei Ito Jonathan Bacon Nicholas Strausfeld PubMed Laiyong Mu Kei Ito Jonathan Bacon Nicholas Strausfeld Related Article in Frontiers Google Scholar PubMed Abstract Close Back to top Javascript is disabled. Please enable Javascript in your browser settings in order to see all the content on this page.

Neural network model of the lateral accessory lobe and ventral protocerebrum of Bombyx mori to generate the flip-flop activity

Experimental background The lateral accessory lobe (LAL) and the ventral protocerebrum (VPC) are known to form a premotor center of brain in insects. The present report focuses on the neural network of the LAL-VPC of Bombyx mori, which is known, from the neuroethological experiments, to generate the pheromone oriented behavior composed of a sequential activity of surge, zigzag-turn and loop [1-3]. The physiological experiments partly elucidate the information pathway which is evoked by a pheromone stimulus given to antennal lobe (AL) and finally projected to LAL-VPC to generate a motor command to thoracic motor systems. The LAL-VPC regions have been characteristically considered to be similar to the electric flip-flop circuit by the records of response from the descending neurons (DN). Moreover, electrophysiological and immunohistochemical studies enable the morphological and physiological classification of each LAL-VPC neuron, and show possible anatomical connection among the neurons [4].

Integration of Lobula Plate Output Signals by DNOVS1, an Identified Premotor Descending Neuron

Many motion-sensitive tangential cells of the lobula plate in blowflies are well described with respect to their visual response properties and the connectivity among them. They have large and complex receptive fields with different preferred directions in different parts of their receptive fields matching the optic flow that occurs during various flight maneuvers. However, much less is known about how tangential cells connect to postsynaptic neurons descending to the motor circuits in the thoracic ganglion and how optic flow is represented in these downstream neurons. Here we describe the physiology and the connectivity of a prominent descending neuron called DNOVS1 (for descending neurons of the ocellar and vertical system). We find that DNOVS1 is electrically coupled to a subset of vertical system cells. The specific wiring leads to a preference of DNOVS1 for rotational flow fields around a particular body axis. In addition, DNOVS1 receives input from interneurons connected to the ocelli.

Distribution of dendrites of descending neurons and its implications for the basic organization of the cockroach brain.

To determine precisely the brain areas from which descending neurons (DNs) originate, we examined the distribution of somata and dendrites of DNs in the cockroach brain by retrogradely filling their axons from the cervical connective. At least 235 pairs of somata of DNs were stained, and most of these were grouped into 22 clusters. Their dendrites were distributed in most brain areas, including lateral and medial protocerebra, which are major termination areas of output neurons of the mushroom body, but not in the optic and antennal lobes, the mushroom body, the central complex, or the posteroventral part of the lateral horn. The last area is the termination area of major types of olfactory projection neurons from the antennal lobe, i.e., uni- and macroglomerular projection neurons, so these neurons have no direct connections with DNs. The distribution of axon terminals of ascending neurons overlaps with that of DN dendrites. We propose, based on these findings, that there are numerous parallel processing streams from cephalic sensory areas to thoracic locomotory centers, many of which are via premotor brain areas from which DNs originate. In addition, outputs from the mushroom body, central complex, and posteroventral part of the lateral horn converge on some of the premotor areas, presumably to modulate the activity of some sensorimotor pathways. We propose, based on our results and documented findings, that many parallel processing streams function in various forms of reflexive and relatively stereotyped behaviors, whereas indirect pathways govern some forms of experience-dependent modification of behavior.

Premotor descending neurons responding selectively to local visual stimuli in flies.

The responses of dorsal descending neurons suggest great versatility of the visual system in detecting features of the visual world. Although wide-field motion-sensitive neurons respond to symmetric visual flow fields presented to both eyes, other neurons are known to respond selectively to asymmetric movement of the visual surround. The present account distinguishes yet a third class of descending neurons (DNs) that is selectively activated by local presentation of moving gratings or small contrasting objects. Excitation of these DNs in response to local motion contrasts with their inhibitory responses to wide-field motion. The described DNs invade dorsal neuropil of the pro- and mesothoracic ganglia where they converge with other morphologically and physiologically characterized descending elements. Axon collaterals of DNs visit thoracic neuropil containing the dendrites of motor neurons supplying indirect neck and flight muscles. The present results are discussed with respect to the organization of small-field retinotopic outputs from the lobula, and with respect to the parallel projection of many information channels from the brain to the neck and flight motors.

Physiology and morphology of descending neurons in pheromone-processing olfactory pathways in the male moth Manduca sexta

1. We have characterized the responses and structure of olfactory descending neurons (DNs) that reside in the protocerebrum (PC) of the brain of male sphinx moths Manduca sexta and project toward thoracic ganglia. 2. Excitatory responses of DNs to pheromone blends were of two general types: (a) brief excitation (BE) that recovered to background in less than 1 s after the stimulus, and (b) long-lasting excitation (LLE) that outlasted the stimulus by greater than or equal to 1 s and, in many cases, as long as 30 s. Individual pheromone components were ineffective in eliciting LLE. 3. Some neurons showing LLE also exhibited state-dependent responses to pheromonal stimuli. When such neurons were in a state of low background firing, stimulation with pheromone blend elicited LLE. When they were in a state of LLE, an identical stimulus reduced firing for 5-10 s after which firing gradually increased to the initial higher level. 4. Thirteen stained DNs were reconstructed from serial sections for detailed analysis of their morphology in the brain. DNs exhibiting LLE had neurites concentrated in the lateral accessory lobes (LALs) in the protocerebrum and adjacent neuropil. Most DNs exhibiting only BE to pheromonal stimuli and other DNs showing responses only to visual or mechanosensory stimuli did not have branches in the LALs.

Wide-field motion-sensitive neurons tuned to horizontal movement in the honeybee, Apis mellifera

This paper describes the morphology and response characteristics of two types of paired descending neurons (DNs) (classified as DNVII1 and DNIV1) and two lobula neurons (HR1 and HP1) in the honeybee, Apis mellifera. 1. The terminal arborizations of the lobula neurons are in juxtaposition with the dendritic branches of the DNs (Figs. 2, 3b, 5). Both of the DNs descend into the ipsilateral side of the thoracic ganglia via the dorsal intermediate tract (Fig. 6) and send out many blebbed terminal branches into the surrounding motor neuropil (Figs. 3c, 7). 2. Both the lobula and descending neurons respond in a directionally selective manner to the motion of widefield, periodic square-wave gratings. 3. The neurons have broad directional tuning curves (Figs. 10, 11). HR1 is maximally sensitive to regressive (back-to-front) motion and HP1 is maximally sensitive to progressive (front-to-back) motion over the ipsilateral eye (Fig. 11). DNVII1 is maximally sensitive when there is simultaneous regressive motion over the ipsilateral eye and progressive motion over the contralateral eye (Fig. 12a). Conversely, DNIV1 is optimally stimulated when there is simultaneous progressive motion over the ipsilateral eye and regressive motion over the contralateral eye (Fig. 12b). 4. The response of DNIV1 is shown to depend on the contrast frequency (CF) rather than the angular velocity of the periodic gratings used as stimuli. The peak responses of both regressive and progressive sensitive DNs are shown to occur at CFs of 8–10 Hz (Figs. 13, 14).

Mesothoracic interneurons involved in flight steering in the locust

1. 1. Twenty-eight interneurons with somata in the mesothoracic ganglion of the locust Locusta appear to be involved in steering in flight. All have their arborizations in the dorsal (flight) neuropil. All make directionally selective responses to visual, ocellar or wind stimuli corresponding to simulated deviations from course in flight. All are directly and/or indirectly postsynaptic to one or more sensory descending neurons (DNs) of the brain, which have been shown to produce steering behaviour when electrically stimulated. Convergence of DNs leads to complex responses by the interneurons. Some receive a variety of additional sensory information derived from thoracic receptors, especially wing proprioceptors and the ear. 2. 2. The membrane potentials of all these interneurons are modulated at flight frequency during fictive flight in deafferented preparations. Nineteen are depolarised in depressor phase (and/ or hyperpolarised in elevator phase); nine are depolarised in elevator phase (and/or hyperpolarised in depressor phase). The modulation derives in at least one case (neuron 016), and presumably in all, from synaptic drive from oscillator or oscillator-follower interneurons. None of the described cells, with the possible exception of IN 313, is thought to be part of the oscillator itself. 3. 3. The 28 ‘steering interneurons’ are characterised and named. Five (016, 035, 036, 302, 313) have been previously described in other contexts. Of these, the first 3 have been renamed; they were previously 116, 135 and 136 of Rowell and Pearson (1983). Four other previously named units are synonomized: 318 of Rowell and Pearson (1983) becomes 302 of Robertson and Pearson (1983), and 120 and 119 of Rowell and Pearson (1983), and 1AA of Elson (1987), all become 016. Two new modifications of the numbering system for locust interneurons are introduced. 4. 4. Five steering neurons are known to make monosynaptic, excitatory or inhibitory connections with flight motor neurons. Individual steering interneurons contribute between 25% and 10% of the total oscillatory drive to individual FMNs. 5. 5. The population of steering interneurons is the site of convergence of oscillator drive and sensory input prior to reaching the motor neuron: this allows sensory modulation of the strength and timing of drive to the individual motor neuron in the appropriate phase of the wing beat cycle, which is required for corrective steering. They are also a point at which the motor drive to the motor neuron is modified by proprioceptive reafference.