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 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.

Convergence of Olfactory Inputs within the Central Nervous System of a Cartilaginous and a Bony Fish: An Anatomical Indicator of Olfactory Sensitivity

2020 ◽  
Vol 95 (3-4) ◽  
pp. 139-161 ◽  
Author(s):  
Victoria Camilieri-Asch ◽  
Kara E. Yopak ◽  
Alethea Rea ◽  
Jonathan D. Mitchell ◽  
Julian C. Partridge ◽  
...  
Keyword(s):  
Olfactory Nerve ◽  
Axon Diameter ◽  
Olfactory Pathway ◽  
Transmission Electron ◽  
Depth Analysis ◽  
The Central Nervous System ◽  
Olfactory Input ◽  
Bamboo Shark ◽  
The Brain

The volume of the olfactory bulbs (OBs) relative to the brain has been used previously as a proxy for olfactory capabilities in many vertebrate taxa, including fishes. Although this gross approach has predictive power, a more accurate assessment of the number of afferent olfactory inputs and the convergence of this information at the level of the telencephalon is critical to our understanding of the role of olfaction in the behaviour of fishes. In this study, we used transmission electron microscopy to assess the number of first-order axons within the olfactory nerve (ON) and the number of second-order axons in the olfactory peduncle (OP) in established model species within cartilaginous (brownbanded bamboo shark, <i>Chiloscyllium punctatum</i> [CP]) and bony (common goldfish, <i>Carassius auratus</i> [CA]) fishes. The total number of axons varied from a mean of 18.12 ± 7.50 million in the ON to a mean of 0.38 ± 0.21 million in the OP of CP, versus 0.48 ± 0.16 million in the ON and 0.09 ± 0.02 million in the OP of CA. This resulted in a convergence ratio of approximately 50:1 and 5:1, respectively, for these two species. Based on astroglial ensheathing, axon type (unmyelinated [UM] and myelinated [M]) and axon size, we found no differentiated tracts in the OP of CP, whereas a lateral and a medial tract (both of which could be subdivided into two bundles or areas) were identified for CA, as previously described. Linear regression analyses revealed significant differences not only in axon density between species and locations (nerves and peduncles), but also in axon type and axon diameter (<i>p</i> &#x3c; 0.05). However, UM axon diameter was larger in the OPs than in the nerve in both species (<i>p</i> = 0.005), with no significant differences in UM axon diameter in the ON (<i>p</i> = 0.06) between species. This study provides an in-depth analysis of the neuroanatomical organisation of the ascending olfactory pathway in two fish taxa and a quantitative anatomical comparison of the summation of olfactory information. Our results support the assertion that relative OB volume is a good indicator of the level of olfactory input and thereby a proxy for olfactory capabilities.

scholarly journals Cannabinoids Regulate Sensory Processing in Early Olfactory and Visual Neural Circuits

2021 ◽  
Vol 15 ◽  
Author(s):  
Thomas Heinbockel ◽  
Alex Straiker
Keyword(s):  
Visual System ◽  
Sensory Processing ◽  
Neural Circuits ◽  
Endocannabinoid System ◽  
Sensory Receptors ◽  
Signaling System ◽  
Olfactory Pathway ◽  
Chemical Substances ◽  
Early Processing ◽  
The Brain

Our sensory systems such as the olfactory and visual systems are the target of neuromodulatory regulation. This neuromodulation starts at the level of sensory receptors and extends into cortical processing. A relatively new group of neuromodulators includes cannabinoids. These form a group of chemical substances that are found in the cannabis plant. Δ9-tetrahydrocannabinol (THC) and cannabidiol (CBD) are the main cannabinoids. THC acts in the brain and nervous system like the chemical substances that our body produces, the endogenous cannabinoids or endocannabinoids, also nicknamed the brain’s own cannabis. While the function of the endocannabinoid system is understood fairly well in limbic structures such as the hippocampus and the amygdala, this signaling system is less well understood in the olfactory pathway and the visual system. Here, we describe and compare endocannabinoids as signaling molecules in the early processing centers of the olfactory and visual system, the olfactory bulb, and the retina, and the relevance of the endocannabinoid system for synaptic plasticity.

scholarly journals Nonlinear convergence boosts information coding in circuits with parallel outputs

2019 ◽  
Author(s):  
Gabrielle J. Gutierrez ◽  
Fred Rieke ◽  
Eric T. Shea-Brown
Keyword(s):  
Nonlinear Response ◽  
Single Neuron ◽  
Neural Circuits ◽  
Response Functions ◽  
Information Coding ◽  
Efficient Coding ◽  
Coding Efficiency ◽  
Parallel Pathways ◽  
Simultaneous Impact ◽  
Circuit Structure

Neural circuits are structured with layers of converging and diverging connectivity, and selectivity-inducing nonlinearities at neurons and synapses. These components have the potential to hamper an accurate encoding of the circuit inputs. Past computational studies have optimized the nonlinearities of single neurons, or connection weights in networks, to maximize encoded information, but have not grappled with the simultaneous impact of convergent circuit structure and nonlinear response functions for efficient coding. Our approach is to compare model circuits with different combinations of convergence, divergence, and nonlinear neurons to discover how interactions between these components affect coding efficiency. We find that a convergent circuit with divergent parallel pathways can encode more information with nonlinear subunits than with linear subunits, despite the compressive loss induced by the convergence and the nonlinearities when considered individually. These results show that the combination of selective nonlinearities and a convergent architecture - both elements that reduce information when acting separately - can promote efficient coding.Significance StatementComputation in neural circuits relies on a common set of motifs, including divergence of common inputs to parallel pathways, convergence of multiple inputs to a single neuron, and nonlinearities that select some signals over others. Convergence and circuit nonlinearities, considered individually, can lead to a loss of information about inputs. Past work has detailed how optimized nonlinearities and circuit weights can maximize information, but here, we show that incorporating non-invertible nonlinearities into a circuit with divergence and convergence, can enhance encoded information despite the suboptimality of these components individually. This study extends a broad literature on efficient coding to convergent circuits. Our results suggest that neural circuits may preserve more information using suboptimal components than one might expect.

scholarly journals Distributed control of motor circuits for backward walking in Drosophila

2020 ◽  
Vol 11 (1) ◽  
Author(s):  
Kai Feng ◽  
Rajyashree Sen ◽  
Ryo Minegishi ◽  
Michael Dübbert ◽  
Till Bockemühl ◽  
...  
Keyword(s):  
Distributed Control ◽  
Population Coding ◽  
Power Stroke ◽  
Single Type ◽  
Level Control ◽  
Backward Walking ◽  
Motor Circuits ◽  
Descending Neurons ◽  
High Level ◽  
The Brain

AbstractHow 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.

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.

Neuronal Control of Drosophila Walking Direction

Science ◽  
2014 ◽  
Vol 344 (6179) ◽  
pp. 97-101 ◽  
Author(s):  
Salil S. Bidaye ◽  
Christian Machacek ◽  
Yang Wu ◽  
Barry J. Dickson
Keyword(s):  
Muscle Activation ◽  
Command Neurons ◽  
Backward Walking ◽  
Motor Circuits ◽  
Neuronal Control ◽  
Descending Neurons ◽  
Leg Muscle ◽  
The Brain ◽  
Local Motor

Most land animals normally walk forward but switch to backward walking upon sensing an obstacle or danger in the path ahead. A change in walking direction is likely to be triggered by descending “command” neurons from the brain that act upon local motor circuits to alter the timing of leg muscle activation. Here we identify descending neurons for backward walking in Drosophila—the MDN neurons. MDN activity is required for flies to walk backward when they encounter an impassable barrier and is sufficient to trigger backward walking under conditions in which flies would otherwise walk forward. We also identify ascending neurons, MAN, that promote persistent backward walking, possibly by inhibiting forward walking. These findings provide an initial glimpse into the circuits and logic that control walking direction in Drosophila.

scholarly journals Cellular expression and functional roles of all 26 neurotransmitter GPCRs in the C. elegans egg-laying circuit

2020 ◽  
Author(s):  
Robert W. Fernandez ◽  
Kimberly Wei ◽  
Erin Y. Wang ◽  
Deimante Mikalauskaite ◽  
Andrew Olson ◽  
...  
Keyword(s):  
Neural Circuits ◽  
Egg Laying ◽  
G Protein Coupled Receptors ◽  
Model Systems ◽  
Functional Roles ◽  
C Elegans ◽  
Cellular Expression ◽  
And Function ◽  
To Receive ◽  
G Protein Coupled

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.

scholarly journals Structured sampling of olfactory input by the fly mushroom body

2020 ◽  
Author(s):  
Zhihao Zheng ◽  
Feng Li ◽  
Corey Fisher ◽  
Iqbal J. Ali ◽  
Nadiya Sharifi ◽  
...  
Keyword(s):  
Network Structure ◽  
Mushroom Body ◽  
Sensory Information ◽  
Fruit Fly ◽  
Projection Neurons ◽  
Large Numbers ◽  
Unified View ◽  
Olfactory Input ◽  
To Receive ◽  
Random Connectivity

AbstractAssociative memory formation and recall in the adult fruit fly Drosophila melanogaster is subserved by the mushroom body (MB). Upon arrival in the MB, sensory information undergoes a profound transformation. Olfactory projection neurons (PNs), the main MB input, exhibit broadly tuned, sustained, and stereotyped responses to odorants; in contrast, their postsynaptic targets in the MB, the Kenyon cells (KCs), are nonstereotyped, narrowly tuned, and only briefly responsive to odorants. Theory and experiment have suggested that this transformation is implemented by random connectivity between KCs and PNs. However, this hypothesis has been challenging to test, given the difficulty of mapping synaptic connections between large numbers of neurons to achieve a unified view of neuronal network structure. Here we used a recent whole-brain electron microscopy (EM) volume of the adult fruit fly to map large numbers of PN- to-KC connections at synaptic resolution. Comparison of the observed connectome to precisely defined null models revealed unexpected network structure, in which a subset of food-responsive PN types converge on individual downstream KCs more frequently than expected. The connectivity bias is consistent with the neurogeometry: axons of the overconvergent PNs tend to arborize near one another in the MB main calyx, making local KC dendrites more likely to receive input from those types. Computational modeling of the observed PN-to-KC network showed that input from the overconvergent PN types is better discriminated than input from other types. These results suggest an ‘associative fovea’ for olfaction, in that the MB is wired to better discriminate more frequently occurring and ethologically relevant combinations of food-related odors.

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.

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