scholarly journals A command-like descending neuron that coordinately activates backward and inhibits forward locomotion

2018 ◽  
Author(s):  
Arnaldo Carreira-Rosario ◽  
Aref Arzan Zarin ◽  
Matthew Q. Clark ◽  
Laurina Manning ◽  
Richard Fetter ◽  
...  

AbstractCommand-like descending neurons can induce many behaviors, such as backward locomotion, escape, feeding, courtship, egg-laying, or grooming. In most animals it remains unknown how neural circuits switch between these antagonistic behaviors: via top-down activation/inhibition of antagonistic circuits or via reciprocal inhibition between antagonistic circuits. Here we use genetic screens, intersectional genetics, circuit reconstruction by electron microscopy, and functional optogenetics to identify a bilateral pair of larval “mooncrawler descending neurons” (MDNs) with command-like ability to coordinately induce backward locomotion and block forward locomotion; the former by activating a backward-specific premotor neuron, and the latter by disynaptic inhibition of a forward-specific premotor neuron. In contrast, direct reciprocal inhibition between forward and backward circuits was not observed. Thus, MDNs coordinate a transition between antagonistic larval locomotor behaviors. Interestingly, larval MDNs persist into adulthood, where they can trigger backward walking. Thus, MDNs induce backward locomotion in both limbless and limbed animals.HighlightsMDN command-like descending neuron induces backward larval locomotionMDN neurons coordinately regulate antagonistic behaviors (forward/backward locomotion)MDN-motor circuit validated at structural (TEM) and functional (optogenetic) levelsMDN neurons induce backward locomotion in both limbless larva and limbed adult

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Arnaldo Carreira-Rosario ◽  
Aref Arzan Zarin ◽  
Matthew Q Clark ◽  
Laurina Manning ◽  
Richard D Fetter ◽  
...  

Command-like descending neurons can induce many behaviors, such as backward locomotion, escape, feeding, courtship, egg-laying, or grooming (we define ‘command-like neuron’ as a neuron whose activation elicits or ‘commands’ a specific behavior). In most animals, it remains unknown how neural circuits switch between antagonistic behaviors: via top-down activation/inhibition of antagonistic circuits or via reciprocal inhibition between antagonistic circuits. Here, we use genetic screens, intersectional genetics, circuit reconstruction by electron microscopy, and functional optogenetics to identify a bilateral pair of Drosophila larval ‘mooncrawler descending neurons’ (MDNs) with command-like ability to coordinately induce backward locomotion and block forward locomotion; the former by stimulating a backward-active premotor neuron, and the latter by disynaptic inhibition of a forward-specific premotor neuron. In contrast, direct monosynaptic reciprocal inhibition between forward and backward circuits was not observed. Thus, MDNs coordinate a transition between antagonistic larval locomotor behaviors. Interestingly, larval MDNs persist into adulthood, where they can trigger backward walking. Thus, MDNs induce backward locomotion in both limbless and limbed animals.


2020 ◽  
Author(s):  
Shai Israel ◽  
Eyal Rozenfeld ◽  
Denise Weber ◽  
Wolf Huetteroth ◽  
Moshe Parnas

Abstract Although animals switch to backward walking upon sensing an obstacle or danger in their path, the initiation and execution of backward locomotion is poorly understood. The discovery of Moonwalker Descending Neurons (MDNs), made Drosophila useful to study neural circuits underlying backward locomotion. MDNs were demonstrated to receive visual and mechanosensory inputs. However, whether other modalities converge onto MDNs and what are the neural circuits activating MDNs are unknown. We show that aversive but not appetitive olfactory input triggers MDN-mediated backward locomotion. We identify in each hemisphere, a single Moonwalker Subesophageal Zone neuron (MooSEZ), which triggers backward locomotion. MooSEZs act both upstream and in parallel to MDNs. Surprisingly, MooSEZs also respond mostly to aversive odor. Contrary to MDNs, blocking MooSEZs activity has little effect on odor-evoked backward locomotion. Thus, this work reveals another important modality input to MDNs in addition to a novel olfactory pathway and MDN-independent backward locomotion pathway.


2018 ◽  
Author(s):  
Paavo Huoviala ◽  
Michael-John Dolan ◽  
Fiona M. Love ◽  
Philip Myers ◽  
Shahar Frechter ◽  
...  

AbstractEvolution has shaped nervous systems to produce stereotyped behavioural responses to ethologically relevant stimuli. For example when laying eggs, female Drosophila avoid geosmin, an odorant produced by toxic moulds. Here we identify second, third, and fourth order neurons required for this innate olfactory aversion. Connectomics data place these neurons in a complete synaptic circuit from sensory input to descending output. We find multiple levels of valence-specific convergence, including a novel form of axo-axonic input onto second order neurons conveying another danger signal, the pheromone of parasitoid wasps. However, we also observe extensive divergence: second order geosmin neurons connect with a diverse array of 80 third order cell types. We find a pattern of convergence of aversive odour channels at this level. Crossing one more synaptic layer, we identified descending neurons critical for egg-laying aversion. Our data suggest a transition from a labelled line organisation in the periphery to a highly distributed central brain representation that is then coupled to distinct descending pathways.


2018 ◽  
Author(s):  
Chin-Lin Chen ◽  
Laura Hermans ◽  
Meera C. Viswanathan ◽  
Denis Fortun ◽  
Michael Unser ◽  
...  

AbstractTo understand neural circuits that control limbs, one must measure their activity during behavior. Until now this goal has been challenging, because the portion of the nervous system that contains limb premotor and motor circuits is largely inaccessible to large-scale recording techniques in intact, moving animals – a constraint that is true for both vertebrate and invertebrate models. Here, we introduce a method for 2-photon functional imaging from the ventral nerve cord of behaving adult Drosophila melanogaster. We use this method to reveal patterns of activity across nerve cord populations during grooming and walking and to uncover the functional encoding of moonwalker ascending neurons (MANs), moonwalker descending neurons (MDNs), and a novel class of locomotion-associated descending neurons. This new approach enables the direct investigation of circuits associated with complex limb movements.


2020 ◽  
Author(s):  
Shai Israel ◽  
Eyal Rozenfeld ◽  
Denise Weber ◽  
Wolf Huetteroth ◽  
Moshe Parnas

AbstractAlthough animals switch to backward walking upon sensing an obstacle or danger in their path, the initiation and execution of backward locomotion is poorly understood. The discovery of Moonwalker Descending Neurons (MDNs), made Drosophila useful to study neural circuits underlying backward locomotion. MDNs were demonstrated to receive visual and mechanosensory inputs. However, whether other modalities converge onto MDNs and what are the neural circuits activating MDNs are unknown. We show that aversive but not appetitive olfactory input triggers MDN-mediated backward locomotion. We identify in each hemisphere, a single Moonwalker Subesophageal Zone neuron (MooSEZ), which triggers backward locomotion. MooSEZs act both upstream and in parallel to MDNs. Surprisingly, MooSEZs also respond mostly to aversive odor. Contrary to MDNs, blocking MooSEZs activity has little effect on odor-evoked backward locomotion. Thus, this work reveals another important modality input to MDNs in addition to a novel olfactory pathway and MDN-independent backward locomotion pathway.


2018 ◽  
Vol 41 (1) ◽  
pp. 349-369 ◽  
Author(s):  
Scott W. Emmons

The recently determined connectome of the Caenorhabditis elegans adult male, together with the known connectome of the hermaphrodite, opens up the possibility for a comprehensive description of sexual dimorphism in this species and the identification and study of the neural circuits underlying sexual behaviors. The C. elegans nervous system consists of 294 neurons shared by both sexes plus neurons unique to each sex, 8 in the hermaphrodite and 91 in the male. The sex-specific neurons are well integrated within the remainder of the nervous system; in the male, 16% of the input to the shared component comes from male-specific neurons. Although sex-specific neurons are involved primarily, but not exclusively, in controlling sex-unique behavior—egg-laying in the hermaphrodite and copulation in the male—these neurons act together with shared neurons to make navigational choices that optimize reproductive success. Sex differences in general behaviors are underlain by considerable dimorphism within the shared component of the nervous system itself, including dimorphism in synaptic connectivity.


1983 ◽  
Vol 49 (3) ◽  
pp. 611-626 ◽  
Author(s):  
E. L. Peterson

1. The interactions among the four pairs of interneurons (HN(1)-HN(4)) of the heartbeat timing oscillator are confined to the third and fourth ganglia (G3 and G4). In isolation, G3 and G4 each produces a rhythm essentially the same as that shown when the two ganglia are linked together. 2. The local circuits in both ganglia have the same general form. In both the oscillation centers on a bilateral pair of HN cells that are linked by reciprocal inhibition (the HN(3) pair in G3 and the HN(4) pair in G4). In addition, there is reciprocal inhibition between an HN(3) or HN(4) cell and the intersegmental processes of the ipsilateral HN(1) and HN(2) cells. 3. These connections account for the phase relationships in an isolated G3 or G4, since cells linked by reciprocal inhibition produce bursts in alternation. 4. In isolated ganglia, reciprocal inhibition not only coordinates the activity of the HN cells but also appears to help generate their bursts. 5. Yet reciprocal inhibition alone cannot account for the activity of the network. An endogenous property of the HN(3) and HN(4) cells appears to create the instability necessary for oscillation.


Author(s):  
Robert W. Fernandez ◽  
Kimberly Wei ◽  
Erin Y. Wang ◽  
Deimante Mikalauskaite ◽  
Andrew Olson ◽  
...  

SummaryMaps of the synapses made and neurotransmitters released by all neurons in model systems such as C. elegans have left still unresolved how neural circuits integrate and respond to neurotransmitter signals. Using the egg-laying circuit of C. elegans as a model, we mapped which cells express each of the 26 neurotransmitter G protein coupled receptors (GPCRs) of this organism and also genetically analyzed the functions of all 26 GPCRs. We found that individual neurons express many distinct receptors, epithelial cells often express neurotransmitter receptors, and receptors are often positioned to receive extrasynaptic signals. The egg-laying circuit appears to use redundancy and compensation to achieve functional robustness, as receptor knockouts reveal few defects; however, increasing receptor signaling through overexpression more efficiently reveals receptor functions. This map of neurotransmitter GPCR expression and function in the egg-laying circuit provides a model for understanding GPCR signaling in other neural circuits.


2019 ◽  
Author(s):  
Caroline Zanchi ◽  
Yannick Moret ◽  
Mark A. F. Gillingham

AbstractBody condition can be defined as the amount of energetic reserves present within an individual after structural size had been accounted for (i.e. relative amounts of energetic reserves), and estimated by Body Condition indices (BCIs)Several methods have been proposed to calculate BCIs. However, they have traditionally been validated in vertebrate studies and evidence of their power to predict fitness in invertebrates is scarce. Ideally, the use of a particular BCI in an animal population should be validated based on its ability to accurately reflect the relative amount of reserves available to the animal as well as its relationship to fitness.We aimed at increasing the variance in female body condition of Tenebrio molitor beetles by subjecting them to restricted or optimal food conditions at both the larval and/or adult stage. We then explored the predictive power of several BCIs on both the absolute and relative amount of lipids and sugars present in the insect’s body, and their link with adult fitness. Using an iteroparous income breeder allowed us to assess the relative effects of larval vs. adult access to nutritional resources on fecundity along several reproductive events.Simple measurements of phenotypically plastic traits (i.e. mass and volume) correlated well with absolute, but poorly with relative, measures of body reserves. Conversely, we found that BCIs that corrected for the interdependence between phenotypically plastic traits and structural size strongly correlated with relative amounts of body components.We found that even though the adult feeding treatment had a stronger effect, body condition at emergence, but not larval feeding treatment, also affected fecundity. Moreover, while the effect of the adult feeding treatment varied along time (i.e. egg laying rank), the effect of body condition at emergence remained constant.These results show that by carefully using simple morphometric measures and BCIs, it is possible to distinguish between the effects of structural size and body condition on fitness traits in invertebrates, and to show that an iteroparous income breeder can partially rely on its early energetic state for its later fecundity.


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