Electric shock causes fear-like persistent behavioral response in the nematode Caenorhabditis elegans

Electricity is widely utilized as environmental stimulus to sense the world by many animal species. Despite its importance, however, molecular and physiological mechanisms for responding to electrical stimulus have been far less understood compared to other sensory stimuli. Here we report novel behavioral responses to electrical stimulus of the nematode C. elegans. When the animals on food are stimulated by alternating current, their movement speed suddenly increases more than 2-fold, which persists for a few minutes even after the electrical stimulation is terminated. Genetic analyses reveal that voltage-gated channels are required for the response, possibly as the sensors, and neuropeptide signaling suppresses the persistent response. Additional behavioral analysis reveals that, in addition to the persistence, the animal's response to electrical shock is scalable and has a negative valence, which are recently regarded as emotion primitives, suggesting that the response may reflect a primitive form of "fear" of animals.

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Auditory effects to complement the absence of visual information

Seeing and Perceiving ◽

10.1163/187847612x647991 ◽

2012 ◽

Vol 25 (0) ◽

pp. 169

Author(s):

Tomoaki Nakamura ◽

Yukio P. Gunji

Keyword(s):

Visual Information ◽

Visual Stimuli ◽

Movement Speed ◽

Auditory Stimuli ◽

Perceptual Similarity ◽

Main Interest ◽

Sensory Stimuli ◽

Visual Interaction ◽

Spatio Temporal ◽

Expected Position

The majority of research on audio–visual interaction focused on spatio-temporal factors and synesthesia-like phenomena. Especially, research on synesthesia-like phenomena has been advanced by Marks et al., and they found synesthesia-like correlation between brightness and size of visual stimuli and pitch of auditory stimuli (Marks, 1987). It seems that main interest of research on synesthesia-like phenomena is what perceptual similarity/difference between synesthetes and non-synesthetes is. We guessed that cross-modal phenomena of non-synesthetes on perceptual level emerge as a function to complement the absence or ambiguity of a certain stimulus. To verify the hypothesis, we investigated audio–visual interaction using movement (speed) of an object as visual stimuli and sine-waves as auditory stimuli. In this experiment objects (circles) moved at a fixed speed in one trial and the objects were masked in arbitrary positions, and auditory stimuli (high, middle, low pitch) were given simultaneously with the disappearance of objects. Subject reported the expected position of the objects when auditory stimuli stopped. Result showed that correlation between the position, i.e., the movement speed, of the object and pitch of sound was found. We conjecture that cross-modal phenomena on non-synesthetes tend to occur when one of sensory stimuli are absent/ambiguous.

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C. elegans G Protein Regulator RGS-3 Controls Sensitivity to Sensory Stimuli

Neuron ◽

10.1016/j.neuron.2006.11.015 ◽

2007 ◽

Vol 53 (1) ◽

pp. 39-52 ◽

Cited By ~ 38

Author(s):

Denise M. Ferkey ◽

Rhonda Hyde ◽

Gal Haspel ◽

Heather M. Dionne ◽

Heather A. Hess ◽

...

Keyword(s):

G Protein ◽

Sensory Stimuli ◽

C Elegans

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Chaperone biomarkers of lifespan and penetrance track the dosages of many other proteins

Nature Communications ◽

10.1038/s41467-019-13664-7 ◽

2019 ◽

Vol 10 (1) ◽

Cited By ~ 5

Author(s):

Nikolay Burnaevskiy ◽

Bryan Sands ◽

Soo Yun ◽

Patricia M. Tedesco ◽

Thomas E. Johnson ◽

...

Keyword(s):

Animal Model ◽

Intrinsic Noise ◽

Effective Dosage ◽

Major Contributor ◽

In Vivo Microscopy ◽

Physiological Mechanisms ◽

C Elegans ◽

Protein Chaperone ◽

Cell Variation

AbstractMany traits vary among isogenic individuals in homogeneous environments. In microbes, plants and animals, variation in the protein chaperone system affects many such traits. In the animal model C. elegans, the expression level of hsp-16.2 chaperone biomarkers correlates with or predicts the penetrance of mutations and lifespan after heat shock. But the physiological mechanisms causing cells to express different amounts of the biomarker were unknown. Here, we used an in vivo microscopy approach to dissect different contributions to cell-to-cell variation in hsp-16.2 expression in the intestines of young adult animals, which generate the most lifespan predicting signal. While we detected both cell autonomous intrinsic noise and signaling noise, we found both contributions were relatively unimportant. The major contributor to cell-to-cell variation in biomarker expression was general differences in protein dosage. The hsp-16.2 biomarker reveals states of high or low effective dosage for many genes.

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A gate-and-switch model for head orientation behaviors in C. elegans

10.1101/291005 ◽

2018 ◽

Cited By ~ 1

Author(s):

Marie-Hélène Ouellette ◽

Melanie J. Desrochers ◽

Ioana Gheta ◽

Ryan Ramos ◽

Michael Hendricks

Keyword(s):

Motor Neurons ◽

Head Orientation ◽

Sensory Stimuli ◽

C Elegans ◽

Gating Mechanism ◽

Reciprocal Connections ◽

Stable Representation ◽

Odor Removal ◽

Sensory Encoding ◽

Head Responses

SummaryThe nervous system seamlessly integrates perception and action. This ability is essential for stable representation of and appropriate responses to the external environment. How the sensorimotor integration underlying this ability occurs at the level of individual neurons is of keen interest. In Caenorhabditis elegans, RIA interneurons receive input from sensory pathways and have reciprocal connections with head motor neurons. Through separate physiological mechanisms, RIA simultaneously encodes both head orientation and sensory stimuli. Based on these observations, we proposed a model for how RIA may integrate these two signals to detect the spatial distribution of stimuli across head sweeps and generate directional head responses. Here, we show that blocking synaptic release from RIA disrupts head orientation behaviors in response to unilaterally presented stimuli. We found that sensory encoding in RIA is gated according to head orientation. This dependence on head orientation is independent of motor encoding in RIA, suggesting a second, posture-dependent pathway upstream of RIA. This gating mechanism may allow RIA to selectively attend to stimuli that are asymmetric across head sweeps. Attractive odor removal during head bends triggers rapid head withdrawal in the opposite direction. Unlike sensory encoding, this directional response is dependent on motor inputs to and synaptic output from RIA. Together, these results suggest that RIA is part of a sensorimotor pathway that is dynamically regulated according to head orientation at two levels: the first is a gate that filters sensory representations in RIA, and the second is a switch that routes RIA synaptic output to dorsal or ventral head motor neurons.

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Simultaneous optogenetic manipulation and calcium imaging in freely movingC. elegans

10.1101/000943 ◽

2013 ◽

Author(s):

Frederick B. Shipley ◽

Christopher M. Clark ◽

Mark J. Alkema ◽

Andrew M. Leifer

Keyword(s):

Neural Activity ◽

Calcium Imaging ◽

Neural Circuits ◽

Neural Response ◽

Sensory Stimuli ◽

Systems Neuroscience ◽

C Elegans ◽

Fundamental Goal ◽

Freely Moving ◽

Interneuron Activity

A fundamental goal of systems neuroscience is to probe the dynamics of neural activity that drive behavior. Here we present an instrument to simultaneously manipulate neural activity via Channelrhodopsin, monitor neural response via GCaMP3, and observes behavior in freely moving C. elegans. We use the instrument to directly observe the relation between sensory stimuli, interneuron activity and locomotion in the mechanosensory circuit. Now published as: Front Neural Circuits 8:28, doi:10.3389/fncir.2014.00028

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Distinct ensembles of medial prefrontal cortex neurons are activated by threatening stimuli that elicit excitation vs. inhibition of movement

Journal of Neurophysiology ◽

10.1152/jn.00656.2014 ◽

2015 ◽

Vol 114 (2) ◽

pp. 793-807 ◽

Cited By ~ 31

Author(s):

Lindsay R. Halladay ◽

Hugh T. Blair

Keyword(s):

Prefrontal Cortex ◽

Medial Prefrontal Cortex ◽

Conditioned Fear ◽

Flight Behavior ◽

Movement Speed ◽

Sensory Stimuli ◽

Firing Rates ◽

Motor Circuits ◽

The Us ◽

Before And After

Neural circuits controlling defensive behavior were investigated by recording single units in medial prefrontal cortex (mPFC) and dorsolateral periaqueductal gray (dlPAG) while rats expressed conditioned fear responses to an auditory conditioned stimulus (CS; 20-s train of white noise pips) previously paired with an aversive unconditioned stimulus (US; 2-s train of periorbital shocks). The CS elicited conditioned movement inhibition (CMI; characterized by decreased movement speed and freezing) when rats had not recently encountered the US, whereas the CS elicited conditioned movement excitation (CME; characterized by increased movement speed and flight behavior) after recent US encounters. Many mPFC neurons were “strategy-selective” cells that changed their firing rates only when the CS elicited CME (15/71) or CMI (13/71) responses, whereas few mPFC cells (4/71) responded nonselectively to the CS during either response. By contrast, many dlPAG neurons (20/74) responded nonselectively to the CS, but most (40/74) were excited by the CS selectively during CME trials (and none during CMI trials). CME-selective neurons in dlPAG responded phasically after CS pips that elicited CME responses, whereas CME-selective neurons in mPFC showed tonically elevated activity before and after pips that evoked CME responses. These findings suggest that, at the time when the CS occurs, tonic firing rates of CME- and CMI-selective mPFC neurons may bias the rat's choice of whether to express CME vs. CMI responses, perhaps via projections to downstream structures (such as amygdala and PAG) that influence how sensory stimuli are mapped onto motor circuits that drive the expression of competing behaviors.

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The C. elegans homeodomain gene unc-42 regulates chemosensory and glutamate receptor expression

Development ◽

10.1242/dev.126.10.2241 ◽

1999 ◽

Vol 126 (10) ◽

pp. 2241-2251 ◽

Cited By ~ 2

Author(s):

R. Baran ◽

R. Aronoff ◽

G. Garriga

Keyword(s):

Axon Guidance ◽

Cell Fate ◽

Glutamate Receptor ◽

Sensory Neurons ◽

Motor Neurons ◽

Neural Circuits ◽

Receptor Expression ◽

Homeodomain Protein ◽

Sensory Stimuli ◽

C Elegans

Genes that specify cell fate can influence multiple aspects of neuronal differentiation, including axon guidance, target selection and synapse formation. Mutations in the unc-42 gene disrupt axon guidance along the C. elegans ventral nerve cord and cause distinct functional defects in sensory-locomotory neural circuits. Here we show that unc-42 encodes a novel homeodomain protein that specifies the fate of three classes of neurons in the Caenorhabditis elegans nervous system: the ASH polymodal sensory neurons, the AVA, AVD and AVE interneurons that mediate repulsive sensory stimuli to the nematode head and anterior body, and a subset of motor neurons that innervate head and body-wall muscles. unc-42 is required for the expression of cell-surface receptors that are essential for the mature function of these neurons. In mutant animals, the ASH sensory neurons fail to express SRA-6 and SRB-6, putative chemosensory receptors. The AVA, AVD and AVE interneurons and RME and RMD motor neurons of unc-42 mutants similarly fail to express the GLR-1 glutamate receptor. These results show that unc-42 performs an essential role in defining neuron identity and contributes to the establishment of neural circuits in C. elegans by regulating the transcription of glutamate and chemosensory receptor genes.

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A cyclic nucleotide-gated channel inhibits sensory axon outgrowth in larval and adult Caenorhabditis elegans: a distinct pathway for maintenance of sensory axon structure

Development ◽

10.1242/dev.125.2.249 ◽

1998 ◽

Vol 125 (2) ◽

pp. 249-258 ◽

Cited By ~ 4

Author(s):

C.M. Coburn ◽

I. Mori ◽

Y. Ohshima ◽

C.I. Bargmann

Keyword(s):

Cyclic Nucleotide ◽

Developmental Process ◽

Adult Stage ◽

Axon Outgrowth ◽

Late Time ◽

Sensory Axon ◽

Sensory Stimuli ◽

C Elegans ◽

Dauer Larva ◽

Gated Channel

The tax-2 and tax-4 genes of C. elegans encode two subunits of a cyclic nucleotide-gated channel that is required for chemosensation, thermosensation and normal axon outgrowth of some sensory neurons. Here we show that, in tax-2 and tax-4 mutants, young larvae have superficially normal axons, but axon outgrowth resumes in inappropriate regions in late larval stages. Using a temperature-sensitive mutation in tax-2, we find that tax-2 activity is required during the adult stage to preserve normal axon morphology. These results indicate that tax-2 and tax-4 are required for the maintenance of correct axon structure, and reveal an unexpected plasticity that allows C. elegans axons to be remodeled long after their initial connections have been established. TAX-2 and TAX-4 have been proposed to form a transduction channel for chemosensation and thermosensation, and tax-2 activity is required in the adult stage for normal chemotaxis to NaCl and odorants. Animals mutant for the daf-11 gene have axon phenotypes that are similar to those of tax-2 and tax 4 mutants; this axon phenotype also has a late time of action. daf-11 regulates a developmental process called dauer larva formation that is controlled by sensory stimuli, and tax-2 and tax-4 can either stimulate or inhibit dauer larva formation in different contexts.

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hsp-16.2 chaperone biomarkers track physiological states of proteome dosage

10.1101/431643 ◽

2018 ◽

Cited By ~ 1

Author(s):

Nikolay Burnaevskiy ◽

Bryan Sands ◽

Soo Yun ◽

Patricia M Tedesco ◽

Thomas E Johnson ◽

...

Keyword(s):

Gene Expression ◽

Natural Variation ◽

Phenotypic Expression ◽

Major Axis ◽

Intrinsic Noise ◽

Physiological Mechanisms ◽

C Elegans ◽

Protein Chaperone ◽

Cell Variation

ABSTRACTPhenotypic expression of many traits varies among isogenic individuals in homogeneous environments. Intrinsic variation in the protein chaperone system affects a wide variety of traits in diverse biological systems. In C. elegans, expression of hsp-16.2 chaperone biomarkers predicts the penetrance of mutations and lifespan after heat shock. But the physiological mechanisms by which cells express different amounts of the biomarker were unknown. Here, we used an in vivo microscopy approach to dissect the mechanisms of cell-to-cell variation in hsp-16.2 biomarker expression, focusing on the intestines, which generate most signal. We found both intrinsic noise and signaling noise are low. The major axis of cell-to-cell variation in gene expression is composed of general differences in protein dosage. Thus, hsp-16.2 biomarkers reveal states of high or low effective dosages for many genes. It is possible that natural variation in protein dosage or chaperone activity may account for missing heritability of some traits.

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A high-resolution morphological and ultrastructural map of anterior sensory cilia and glia in Caenorhabditis elegans

eLife ◽

10.7554/elife.01948 ◽

2014 ◽

Vol 3 ◽

Cited By ~ 99

Author(s):

David B Doroquez ◽

Cristina Berciu ◽

James R Anderson ◽

Piali Sengupta ◽

Daniela Nicastro

Keyword(s):

High Resolution ◽

Protein Trafficking ◽

Three Dimensional ◽

Structural Features ◽

Microtubule Organization ◽

Sensory Stimuli ◽

C Elegans ◽

Sensory Cilia ◽

Adult Hermaphrodite ◽

Neuronal Functions

Many primary sensory cilia exhibit unique architectures that are critical for transduction of specific sensory stimuli. Although basic ciliogenic mechanisms are well described, how complex ciliary structures are generated remains unclear. Seminal work performed several decades ago provided an initial but incomplete description of diverse sensory cilia morphologies in C. elegans. To begin to explore the mechanisms that generate these remarkably complex structures, we have taken advantage of advances in electron microscopy and tomography, and reconstructed three-dimensional structures of fifty of sixty sensory cilia in the C. elegans adult hermaphrodite at high resolution. We characterize novel axonemal microtubule organization patterns, clarify structural features at the ciliary base, describe new aspects of cilia–glia interactions, and identify structures suggesting novel mechanisms of ciliary protein trafficking. This complete ultrastructural description of diverse cilia in C. elegans provides the foundation for investigations into underlying ciliogenic pathways, as well as contributions of defined ciliary structures to specific neuronal functions.

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