scholarly journals A neural circuit basis for context-modulation of individual locomotor behavior

2019 ◽  
Author(s):  
Kyobi Skutt-Kakaria ◽  
Pablo Reimers ◽  
Timothy A. Currier ◽  
Zach Werkhoven ◽  
Benjamin L. de Bivort
Keyword(s):  
Neural Circuit ◽  
Locomotor Behavior ◽  
Context Dependence ◽  
Central Complex ◽  
Ambient Illumination ◽  
Behavioral Characteristic ◽  
Illumination Changes ◽  
Output Neurons ◽  
Context Specific ◽  
Innate Behaviors

AbstractDefying the cliche that biological variation arises from differences in nature or nurture, genetically identical animals reared in the same environment exhibit striking differences in their behaviors. Innate behaviors can be surprisingly flexible, for example by exhibiting context-dependence. The intersection of behavioral individuality and context-dependence is largely unexplored, particularly at the neural circuit level. Here, we show that individual flies’ tendencies to turn left or right (locomotor handedness) changes when ambient illumination changes. This change is itself a stable individual behavioral characteristic. Silencing output neurons of the central complex (a premotor area that mediates goal-directed navigation) blocks this change. These neurons respond to light with idiosyncratic changes to their baseline calcium levels, and idiosyncratic morphological variation in their presynaptic arbors correlates with idiosyncratic sensory-context-specific turn biases. These findings provide a circuit mechanism by which individual locomotor biases arise and are modulated by sensory context.

scholarly journals A locomotor neural circuit persists and functions similarly in larvae and adult Drosophila

2021 ◽  
Author(s):  
Kristen M. Lee ◽  
Chris Q. Doe
Keyword(s):  
Molecular Markers ◽  
Structural Changes ◽  
Neural Circuit ◽  
Structural Plasticity ◽  
Locomotor Behavior ◽  
Input Output ◽  
Neuronal Remodeling ◽  
Forward Locomotion ◽  
Output Neurons ◽  
Adult Drosophila

AbstractIndividual neurons can undergo drastic structural changes, known as neuronal remodeling or structural plasticity. One example of this is in response to hormones, such as during puberty in mammals or metamorphosis in insects. However, in each of these examples it remains unclear whether the remodeled neuron resumes prior patterns of connectivity, and if so, whether the persistent circuits drive similar behaviors. Here, we utilize a well-characterized neural circuit in the Drosophila larva: the Moonwalking Descending Neuron (MDN) circuit. We previously showed that larval MDN induces backward crawling, and synapses onto the Pair1 interneuron to inhibit forward crawling (Carreira-Rosario et al., 2018). MDN is remodeled during metamorphosis and regulates backward walking in the adult fly. We investigated whether Pair1 is remodeled during metamorphosis and functions within the MDN circuit during adulthood. We assayed morphology and molecular markers to demonstrate that Pair1 is remodeled during metamorphosis and persists in the adult fly. In the adult, optogenetic activation of Pair1 resulted in arrest of forward locomotion, similar to what is observed in larvae. MDN and Pair1 are also synaptic partners in the adult, showing that the MDN-Pair1 interneuron circuit is retained in the adult following hormone-driven pupal remodeling. Thus, the MDN-Pair1 neurons are an interneuronal circuit – i.e. a pair of synaptically connected interneurons – that persists through metamorphosis, taking on new input/output neurons, yet generating similar locomotor behavior at both stages.

scholarly journals A neural model for insect steering applied to olfaction and path integration

2020 ◽  
Author(s):  
Andrea Adden ◽  
Terrence C. Stewart ◽  
Barbara Webb ◽  
Stanley Heinze
Keyword(s):  
Neural Network ◽  
Computational Model ◽  
Motor Neurons ◽  
Spatial Orientation ◽  
Path Integration ◽  
Neural Circuit ◽  
Central Complex ◽  
Flip Flop ◽  
Descending Neurons ◽  
Output Neurons

AbstractMany animal behaviours require orientation and steering with respect to the environment. For insects, a key brain area involved in spatial orientation and navigation is the central complex. Activity in this neural circuit has been shown to track the insect’s current heading relative to its environment, and has also been proposed to be the substrate of path integration. However, it remains unclear how the output of the central complex is integrated into motor commands. Central complex output neurons project to the lateral accessory lobes (LAL), from which descending neurons project to thoracic motor centres. Here, we present a computational model of a simple neural network that has been described anatomically and physiologically in the LALs of male silkworm moths, in the context of odour-mediated steering. We present and analyze two versions of this network, both implemented in the Nengo framework, one rate-based and one based on spiking neurons. The modelled network consists of an inhibitory local interneuron and a bistable descending neuron (‘flip-flop’), which both receive input in the LAL. The flip-flop neuron projects onto neck motor neurons to induce steering. We show that this simple computational model not only replicates the basic parameters of male silkworm moth behaviour in a simulated odour plume, but can also take input from a computational model of path integration in the central complex and use it to steer back to a point of origin. Furthermore, we find that increasing the level of detail within the model improves the realism of the model’s behaviour. Our results suggest that descending neurons originating in the lateral accessory lobes, such as flip-flop neurons, are sufficient to mediate multiple steering behaviours. This study is therefore a first step to close the gap between orientation circuits in the central complex and downstream motor centres.Author summaryTargeted movements and steering within an environment are essential for many behaviours. In insects, the brain’s center for spatial orientation and navigation is the central complex, which processes information about the configuration of the local environment as well as global orientation cues such as the Sun position. Neural networks in the central complex also compute the insect’s heading direction, and are thought to be involved in generating steering commands. However, it is unclear how these steering commands are transmitted to downstream motor centers. Output neurons from the central complex project to the lateral accessory lobes, a neuropil which also gives rise to descending pre-motor neurons that are involved in steering in the silkworm moth Bombyx mori. In this study, we provide a computational model of a pre-motor neural network in the lateral accessory lobes. We show that this network can steer an agent towards the source of a simulated odor plume, but that it can also steer efficiently when getting input from an anatomically constrained network model of the central complex. This model is therefore a first step to close the gap between the central complex and thoracic motor circuits.

Neural circuit control of innate behaviors

2021 ◽  
Author(s):  
Wei Xiao ◽  
Zhuo-Lei Jiao ◽  
Esra Senol ◽  
Jiwei Yao ◽  
Miao Zhao ◽  
...  
Keyword(s):  
Neural Circuit ◽  
Innate Behaviors

scholarly journals A locomotor neural circuit persists and functions similarly in larvae and adult Drosophila

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Kristen Lee ◽  
Chris Q Doe
Keyword(s):  
Molecular Markers ◽  
Structural Changes ◽  
Neural Circuit ◽  
Structural Plasticity ◽  
Locomotor Behavior ◽  
Backward Walking ◽  
Neuronal Remodeling ◽  
Forward Locomotion ◽  
Adult Drosophila

Individual neurons can undergo drastic structural changes, known as neuronal remodeling or structural plasticity. One example of this is in response to hormones, such as during puberty in mammals or metamorphosis in insects. However, in each of these examples it remains unclear whether the remodeled neuron resumes prior patterns of connectivity, and if so, whether the persistent circuits drive similar behaviors. Here, we utilize a well-characterized neural circuit in the Drosophila larva: the Moonwalking Descending Neuron (MDN) circuit. We previously showed that larval MDN induces backward crawling, and synapses onto the Pair1 interneuron to inhibit forward crawling (Carreira-Rosario et al., 2018). MDN is remodeled during metamorphosis and regulates backward walking in the adult fly. We investigated whether Pair1 is remodeled during metamorphosis and functions within the MDN circuit during adulthood. We assayed morphology and molecular markers to demonstrate that Pair1 is remodeled during metamorphosis and persists in the adult fly. MDN-Pair1 connectivity is lost during early pupal stages, when both neurons are severely pruned back, but connectivity is re-established at mid-pupal stages and persist into the adult. In the adult, optogenetic activation of Pair1 resulted in arrest of forward locomotion, similar to what is observed in larvae. Thus, the MDN-Pair1 neurons are an interneuronal circuit - a pair of synaptically connected interneurons – that is re-established during metamorphosis, yet generates similar locomotor behavior at both larval and adult stages.

scholarly journals The connectome of the adult Drosophila mushroom body: implications for function

2020 ◽  
Author(s):  
Feng Li ◽  
Jack Lindsey ◽  
Elizabeth C. Marin ◽  
Nils Otto ◽  
Marisa Dreher ◽  
...  
Keyword(s):  
Dopaminergic Neurons ◽  
Mushroom Body ◽  
Experimental Studies ◽  
Central Complex ◽  
Sensory Inputs ◽  
Descending Neurons ◽  
Sensory Modalities ◽  
Output Neurons ◽  
Transfer Of Information ◽  
Adult Drosophila

AbstractMaking inferences about the computations performed by neuronal circuits from synapse-level connectivity maps is an emerging opportunity in neuroscience. The mushroom body (MB) is well positioned for developing and testing such an approach due to its conserved neuronal architecture, recently completed dense connectome, and extensive prior experimental studies of its roles in learning, memory and activity regulation. Here we identify new components of the MB circuit in Drosophila, including extensive visual input and MB output neurons (MBONs) with direct connections to descending neurons. We find unexpected structure in sensory inputs, in the transfer of information about different sensory modalities to MBONs, and in the modulation of that transfer by dopaminergic neurons (DANs). We provide insights into the circuitry used to integrate MB outputs, connectivity between the MB and the central complex and inputs to DANs, including feedback from MBONs. Our results provide a foundation for further theoretical and experimental work.

scholarly journals Idiosyncratic learning performance in flies generalizes across modalities

2021 ◽  
Author(s):  
Matthew Smith ◽  
Kyle S. Honegger ◽  
Glenn Turner ◽  
Benjamin de Bivort
Keyword(s):  
Individual Differences ◽  
Neural Circuit ◽  
Bitter Taste ◽  
Model Organism ◽  
Fruit Fly ◽  
Learning Performance ◽  
Suitable Model ◽  
Mechanistic Basis ◽  
Innate Behaviors ◽  
Stimulus Modalities

AbstractIndividuals vary in their innate behaviors, even when they have the same genome and have been reared in the same environment. The extent of individuality in plastic behaviors, like learning, is less well characterized. Also unknown is the extent to which intragenotypic differences in learning generalize: if an individual performs well in one assay, will it perform well in other assays? We investigated this using the fruit fly Drosophila melanogaster, an organism long-used to study the mechanistic basis of learning and memory. We found that isogenic flies, reared in identical lab conditions, and subject to classical conditioning that associated odorants with electric shock, exhibit clear individuality in their learning responses. Flies that performed well when an odor was paired with shock tended to perform well when other odors were paired with shock, or when the original odor was paired with bitter taste. Thus, individuality in learning performance appears to be prominent in isogenic animals reared identically, and individual differences in learning performance generalize across stimulus modalities. Establishing these results in flies opens up the possibility of studying the genetic and neural circuit basis of individual differences in learning in a highly suitable model organism.

scholarly journals A Conditional Glutamatergic Synaptic Vesicle Marker for Drosophila

2022 ◽  
Author(s):  
Sarah J Certel ◽  
Evelyne Ruchti ◽  
Brian D McCabe ◽  
R Steven Stowers
Keyword(s):  
Nervous System ◽  
Synaptic Vesicles ◽  
Neural Circuit ◽  
Glutamate Release ◽  
Nervous System Development ◽  
Central Complex ◽  
Excitatory Neurotransmitter ◽  
Glutamatergic Neurons ◽  
Brain Functions ◽  
Conditional Expression

Abstract Glutamate is a principal neurotransmitter used extensively by the nervous systems of all vertebrate and invertebrate animals. It is primarily an excitatory neurotransmitter that has been implicated in nervous system development as well as a myriad of brain functions from the simple transmission of information between neurons to more complex aspects of nervous system function including synaptic plasticity, learning, and memory. Identification of glutamatergic neurons and their sites of glutamate release are thus essential for understanding the mechanisms of neural circuit function and how information is processed to generate behavior. Here we describe and characterize smFLAG-vGlut, a conditional marker of glutamatergic synaptic vesicles for the Drosophila model system. smFLAG-vGlut is validated for functionality, conditional expression, and specificity for glutamatergic neurons and synaptic vesicles. The utility of smFLAG-vGlut is demonstrated by glutamatergic neurotransmitter phenotyping of 26 different central complex neuron types of which nine were established to be glutamatergic. This illumination of glutamate neurotransmitter usage will enhance the modeling of central complex neural circuitry and thereby our understanding of information processing by this region of the fly brain. The use of smFLAG for glutamatergic neurotransmitter phenotyping and identification of glutamate release sites can be extended to any Drosophila neuron(s) represented by a binary transcription system driver.

scholarly journals Astrocytes close a critical period of motor circuit plasticity

2020 ◽  
Author(s):  
Sarah D. Ackerman ◽  
Nelson A. Perez-Catalan ◽  
Marc R. Freeman ◽  
Chris Q. Doe
Keyword(s):  
Motor Neuron ◽  
Critical Period ◽  
Large Scale ◽  
Sensory Input ◽  
Neural Circuit ◽  
Locomotor Behavior ◽  
Neuron Activity ◽  
Critical Periods ◽  
Dendrite Morphology ◽  
Motor Circuit

AbstractCritical periods – brief intervals where neural circuits can be modified by sensory input – are necessary for proper neural circuit assembly. Extended critical periods are associated with neurodevelopmental disorders, including schizophrenia and autism; however, the mechanisms that ensure timely critical period closure remain unknown. Here, we define the extent of a critical period in the developing Drosophila motor circuit, and identify astrocytes as essential for proper critical period termination. During the critical period, decreased activity produces larger motor dendrites with fewer inhibitory inputs; conversely, increased motor neuron activity produces smaller motor dendrites with fewer excitatory inputs. Importantly, activity has little effect on dendrite morphology after critical period closure. Astrocytes invade the neuropil just prior to critical period closure, and astrocyte ablation prolongs the critical period. Finally, we use a genetic screen to identify astrocyte-motor neuron signaling pathways that close the critical period, including Neuroligin-Neurexin signaling. Reduced signaling destabilizes dendritic microtubules, increases dendrite dynamicity, and impairs locomotor behavior, underscoring the importance of critical period closure. Previous work defines astroglia as regulators of plasticity at individual synapses; here, we show that astrocytes also regulate large-scale structural plasticity to motor dendrite, and thus, circuit architecture to ensure proper locomotor behavior.

scholarly journals The connectome of the adult Drosophila mushroom body provides insights into function

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Feng Li ◽  
Jack W Lindsey ◽  
Elizabeth C Marin ◽  
Nils Otto ◽  
Marisa Dreher ◽  
...  
Keyword(s):  
Dopaminergic Neurons ◽  
Mushroom Body ◽  
Experimental Studies ◽  
Central Complex ◽  
Sensory Inputs ◽  
Descending Neurons ◽  
Sensory Modalities ◽  
Output Neurons ◽  
Transfer Of Information ◽  
Adult Drosophila

Making inferences about the computations performed by neuronal circuits from synapse-level connectivity maps is an emerging opportunity in neuroscience. The mushroom body (MB) is well positioned for developing and testing such an approach due to its conserved neuronal architecture, recently completed dense connectome, and extensive prior experimental studies of its roles in learning, memory and activity regulation. Here we identify new components of the MB circuit in Drosophila, including extensive visual input and MB output neurons (MBONs) with direct connections to descending neurons. We find unexpected structure in sensory inputs, in the transfer of information about different sensory modalities to MBONs, and in the modulation of that transfer by dopaminergic neurons (DANs). We provide insights into the circuitry used to integrate MB outputs, connectivity between the MB and the central complex and inputs to DANs, including feedback from MBONs. Our results provide a foundation for further theoretical and experimental work.

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