Regulation of sensory motor circuits used in C. elegans male intromission behavior

AbstractAnimal behaviors are commonly organized into long-lasting states that coordinately impact the generation of diverse motor outputs such as feeding, locomotion, and grooming. However, the neural mechanisms that coordinate these diverse motor programs remain poorly understood. Here, we examine how the distinct motor programs of the nematode C. elegans are coupled together across behavioral states. We describe a new imaging platform that permits automated, simultaneous quantification of each of the main C. elegans motor programs over hours or days. Analysis of these whole-organism behavioral profiles shows that the motor programs coordinately change as animals switch behavioral states. Utilizing genetics, optogenetics, and calcium imaging, we identify a new role for dopamine in coupling locomotion and egg-laying together across states. These results provide new insights into how the diverse motor programs throughout an organism are coordinated and suggest that neuromodulators like dopamine can couple motor circuits together in a state-dependent manner.

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A conserved neuropeptide system links head and body motor circuits to enable adaptive behavior

10.1101/2020.04.27.064550 ◽

2020 ◽

Author(s):

Shankar Ramachandran ◽

Navonil Banerjee ◽

Raja Bhattacharya ◽

Denis Touroutine ◽

Christopher M. Lambert ◽

...

Keyword(s):

Motor Neurons ◽

Adaptive Behavior ◽

Environmental Conditions ◽

Body Wall ◽

Behavioral Responses ◽

Physiological Changes ◽

C Elegans ◽

Motor Circuits ◽

Concerted Activity ◽

Stimulation Of

SUMMARYNeuromodulators promote adaptive behaviors in response to either environmental or internal physiological changes. These responses are often complex and may involve concerted activity changes across circuits that are not physically connected. It is not well understood how neuromodulatory systems act across circuits to elicit complex behavioral responses. Here we show that the C. elegans NLP-12 neuropeptide system shapes responses to food availability by selectively modulating the activity of head and body wall motor neurons. NLP-12 modulation of the head and body wall motor circuits is generated through conditional involvement of alternate GPCR targets. The CKR-1 GPCR is highly expressed in the head motor circuit, and functions to enhance head bending and increase trajectory reorientations during local food searching, primarily through stimulatory actions on SMD head motor neurons. In contrast, NLP-12 activation of CKR-1 and CKR-2 GPCRs regulates body bending under basal conditions, primarily through actions on body wall motor neurons. Thus, locomotor responses to changing environmental conditions emerge from conditional NLP-12 stimulation of head or body wall motor neuron targets.

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Training sensory–motor behavior in the connectome of an artificial C. elegans

Neurocomputing ◽

10.1016/j.neucom.2015.06.007 ◽

2015 ◽

Vol 168 ◽

pp. 128-134 ◽

Cited By ~ 6

Author(s):

Thomas E. Portegys

Keyword(s):

Motor Behavior ◽

C Elegans ◽

Sensory Motor

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Multilevel Modulation of a Sensory Motor Circuit during C. elegans Sleep and Arousal

Cell ◽

10.1016/j.cell.2013.11.036 ◽

2014 ◽

Vol 156 (1-2) ◽

pp. 249-260 ◽

Cited By ~ 56

Author(s):

Julie Y. Cho ◽

Paul W. Sternberg

Keyword(s):

Motor Circuit ◽

C Elegans ◽

Sensory Motor ◽

Multilevel Modulation

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Modulatory Action by the Serotonergic System: Behavior and Neurophysiology inDrosophila melanogaster

Neural Plasticity ◽

10.1155/2016/7291438 ◽

2016 ◽

Vol 2016 ◽

pp. 1-23 ◽

Cited By ~ 24

Author(s):

Zana R. Majeed ◽

Esraa Abdeljaber ◽

Robin Soveland ◽

Kristin Cornwell ◽

Aubrey Bankemper ◽

...

Keyword(s):

Motor Activity ◽

Tryptophan Hydroxylase ◽

Neural Circuit ◽

Receptor Activation ◽

Receptor Subtype ◽

Receptor Subtypes ◽

Feeding Behaviors ◽

Pharmacological Agents ◽

Motor Circuits ◽

Sensory Motor

Serotonin modulates various physiological processes and behaviors. This study investigates the role of 5-HT in locomotion and feeding behaviors as well as in modulation of sensory-motor circuits. The 5-HT biosynthesis was dysregulated by feedingDrosophilalarvae 5-HT, a 5-HT precursor, or an inhibitor of tryptophan hydroxylase during early stages of development. The effects of feeding fluoxetine, a selective serotonin reuptake inhibitor, during early second instars were also examined. 5-HT receptor subtypes were manipulated using RNA interference mediated knockdown and 5-HT receptor insertional mutations. Moreover, synaptic transmission at 5-HT neurons was blocked or enhanced in both larvae and adult flies. The results demonstrate that disruption of components within the 5-HT system significantly impairs locomotion and feeding behaviors in larvae. Acute activation of 5-HT neurons disrupts normal locomotion activity in adult flies. To determine which 5-HT receptor subtype modulates the evoked sensory-motor activity, pharmacological agents were used. In addition, the activity of 5-HT neurons was enhanced by expressing and activating TrpA1 channels or channelrhodopsin-2 while recording the evoked excitatory postsynaptic potentials (EPSPs) in muscle fibers. 5-HT2 receptor activation mediates a modulatory role in a sensory-motor circuit, and the activation of 5-HT neurons can suppress the neural circuit activity, while fluoxetine can significantly decrease the sensory-motor activity.

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Ebf Activates Expression of a Cholinergic Locus in a Multipolar Motor Ganglion Interneuron Subtype in Ciona

Frontiers in Neuroscience ◽

10.3389/fnins.2021.784649 ◽

2021 ◽

Vol 15 ◽

Author(s):

Sydney Popsuj ◽

Alberto Stolfi

Keyword(s):

Motor Neurons ◽

Terminal Differentiation ◽

Cholinergic Neuron ◽

Gene Products ◽

Exact Role ◽

C Elegans ◽

Motor Circuits ◽

Functional Identities ◽

Type Specification ◽

Differentiation Gene

Conserved transcription factors termed “terminal selectors” regulate neuronal sub-type specification and differentiation through combinatorial transcriptional regulation of terminal differentiation genes. The unique combinations of terminal differentiation gene products in turn contribute to the functional identities of each neuron. One well-characterized terminal selector is COE (Collier/Olf/Ebf), which has been shown to activate cholinergic gene batteries in C. elegans motor neurons. However, its functions in other metazoans, particularly chordates, is less clear. Here we show that the sole COE ortholog in the non-vertebrate chordate Ciona robusta, Ebf, controls the expression of the cholinergic locus VAChT/ChAT in a single dorsal interneuron of the larval Motor Ganglion, which is presumed to be homologous to the vertebrate spinal cord. We propose that, while the function of Ebf as a regulator of cholinergic neuron identity conserved across bilaterians, its exact role may have diverged in different cholinergic neuron subtypes (e.g., interneurons vs. motor neurons) in chordate-specific motor circuits.

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Whole-organism behavioral profiling reveals a role for dopamine in state-dependent motor program coupling in C. elegans

eLife ◽

10.7554/elife.57093 ◽

2020 ◽

Vol 9 ◽

Cited By ~ 4

Author(s):

Nathan Cermak ◽

Stephanie K Yu ◽

Rebekah Clark ◽

Yung-Chi Huang ◽

Saba N Baskoylu ◽

...

Keyword(s):

Motor Program ◽

Egg Laying ◽

Neural Mechanisms ◽

Dependent Manner ◽

Motor Programs ◽

C Elegans ◽

Motor Circuits ◽

State Dependent ◽

Behavioral States ◽

Behavioral Profiling

Animal behaviors are commonly organized into long-lasting states that coordinately impact the generation of diverse motor outputs such as feeding, locomotion, and grooming. However, the neural mechanisms that coordinate these distinct motor programs remain poorly understood. Here, we examine how the distinct motor programs of the nematode C. elegans are coupled together across behavioral states. We describe a new imaging platform that permits automated, simultaneous quantification of each of the main C. elegans motor programs over hours or days. Analysis of these whole-organism behavioral profiles shows that the motor programs coordinately change as animals switch behavioral states. Utilizing genetics, optogenetics, and calcium imaging, we identify a new role for dopamine in coupling locomotion and egg-laying together across states. These results provide new insights into how the diverse motor programs throughout an organism are coordinated and suggest that neuromodulators like dopamine can couple motor circuits together in a state-dependent manner.

Download Full-text