scholarly journals MDN brain descending neurons coordinately activate backward and inhibit forward locomotion

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Arnaldo Carreira-Rosario ◽  
Aref Arzan Zarin ◽  
Matthew Q Clark ◽  
Laurina Manning ◽  
Richard D Fetter ◽  
...  
Keyword(s):  
Neural Circuits ◽  
Reciprocal Inhibition ◽  
Egg Laying ◽  
Genetic Screens ◽  
Specific Behavior ◽  
Descending Neurons ◽  
Forward Locomotion ◽  
Bilateral Pair ◽  
Disynaptic Inhibition ◽  
Locomotor Behaviors

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.

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 ◽  
...  
Keyword(s):  
Neural Circuits ◽  
Reciprocal Inhibition ◽  
Egg Laying ◽  
List Type ◽  
Genetic Screens ◽  
Descending Neurons ◽  
Forward Locomotion ◽  
Bilateral Pair ◽  
Disynaptic Inhibition ◽  
Locomotor Behaviors

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

scholarly journals Two Parallel Pathways Mediate Olfactory-Driven Backward Locomotion

2020 ◽  
Author(s):  
Shai Israel ◽  
Eyal Rozenfeld ◽  
Denise Weber ◽  
Wolf Huetteroth ◽  
Moshe Parnas
Keyword(s):  
Neural Circuits ◽  
Olfactory Pathway ◽  
Backward Walking ◽  
Parallel Pathways ◽  
Descending Neurons ◽  
Olfactory Input ◽  
To Receive

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.

scholarly journals Neural circuit basis of aversive odour processing in Drosophila from sensory input to descending output

2018 ◽  
Author(s):  
Paavo Huoviala ◽  
Michael-John Dolan ◽  
Fiona M. Love ◽  
Philip Myers ◽  
Shahar Frechter ◽  
...  
Keyword(s):  
Sensory Input ◽  
Neural Circuit ◽  
Cell Types ◽  
Second Order ◽  
Egg Laying ◽  
Descending Pathways ◽  
Third Order ◽  
Descending Neurons ◽  
Central Brain ◽  
Multiple Levels

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.

scholarly journals Imaging neural activity in the ventral nerve cord of behaving adult Drosophila

2018 ◽  
Author(s):  
Chin-Lin Chen ◽  
Laura Hermans ◽  
Meera C. Viswanathan ◽  
Denis Fortun ◽  
Michael Unser ◽  
...  
Keyword(s):  
Nerve Cord ◽  
Large Scale ◽  
Ventral Nerve Cord ◽  
Neural Circuits ◽  
New Approach ◽  
Motor Circuits ◽  
Descending Neurons ◽  
Invertebrate Models ◽  
Adult Drosophila ◽  
Direct Investigation

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.

scholarly journals Targeted manipulation of neuronal activity in behaving adult flies

2016 ◽  
Author(s):  
Stefanie Hampel ◽  
Andrew Michael Seeds
Keyword(s):  
Drosophila Melanogaster ◽  
Neuronal Activity ◽  
Neural Circuits ◽  
Neural Circuit ◽  
Fruit Fly ◽  
Specific Behavior ◽  
Freely Behaving ◽  
The Rich ◽  
Circuit Function

The ability to control the activity of specific neurons in freely behaving animals provides an effective way to probe the contributions of neural circuits to behavior. Wide interest in studying principles of neural circuit function using the fruit fly Drosophila melanogaster has fueled the construction of an extensive transgenic toolkit for performing such neural manipulations. Here we describe approaches for using these tools to manipulate the activity of specific neurons and assess how those manipulations impact the behavior of flies. We also describe methods for examining connectivity among multiple neurons that together form a neural circuit controlling a specific behavior. This work provides a resource for researchers interested in examining how neurons and neural circuits contribute to the rich repertoire of behaviors performed by flies.

scholarly journals Two Parallel Pathways Mediate Olfactory-Driven Backward Locomotion

2020 ◽  
Author(s):  
Shai Israel ◽  
Eyal Rozenfeld ◽  
Denise Weber ◽  
Wolf Huetteroth ◽  
Moshe Parnas
Keyword(s):  
Neural Circuits ◽  
Olfactory Pathway ◽  
Backward Walking ◽  
Parallel Pathways ◽  
Descending Neurons ◽  
Olfactory Input ◽  
To Receive

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.

scholarly journals Activity-dependent visualization and control of neural circuits for courtship behavior in the flyDrosophila melanogaster

2019 ◽  
Vol 116 (12) ◽  
pp. 5715-5720 ◽  
Author(s):  
Seika Takayanagi-Kiya ◽  
Taketoshi Kiya
Keyword(s):  
Neural Circuits ◽  
Courtship Behavior ◽  
Sensory Information ◽  
Male Courtship ◽  
Specific Behavior ◽  
Genetic Tool ◽  
Mapping System ◽  
Full Picture ◽  
And Control ◽  
Activity Dependent

Males ofDrosophila melanogasterexhibit stereotypic courtship behavior through which they assess potential mates by processing multimodal sensory information. Although previous studies revealed important neural circuits involved in this process, the full picture of circuits that participate in male courtship remains elusive. Here, we established a genetic tool to visualize or optogenetically reactivate neural circuits activated upon specific behavior, exploiting promoter activity of a neural activity-induced geneHr38. With this approach, we visualized neural circuits activated in the male brain and the ventral nerve cord when a male interacted with a female. The labeling of neural circuits was additively dependent on inputs from antennae and foreleg tarsi. In addition, neural circuits that express the sex-determining genefruitlessordoublesexwere extensively labeled by interaction with a female. Furthermore, optogenetic reactivation of the labeled neural circuits induced courtship posture. With this mapping system, we found that afruitless-positive neural cluster aSP2 was labeled when a male interacted with a female, in addition to previously characterized neurons. Silencing of neurons including aSP2 led to frequent interruption of courtship and significant reduction of mating success rate without affecting latency to start courtship, suggesting that these neurons are required for courtship persistency important for successful copulation. Overall, these results demonstrate that activity-dependent labeling can be used as a powerful tool not only in vertebrates, but also in invertebrates, to identify neural circuits regulating innate behavior.

Neural Circuits of Sexual Behavior inCaenorhabditis elegans

2018 ◽  
Vol 41 (1) ◽  
pp. 349-369 ◽  
Author(s):  
Scott W. Emmons
Keyword(s):  
Nervous System ◽  
Sex Differences ◽  
Sexual Behaviors ◽  
Neural Circuits ◽  
Egg Laying ◽  
Synaptic Connectivity ◽  
Comprehensive Description ◽  
C Elegans ◽  
Shared Component ◽  
Male Specific

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.

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