scholarly journals Presynaptic MAST Kinase Controls Bidirectional Post-Synaptic Responses to Convey Stimulus Valence in C. elegans

2019 ◽  
Author(s):  
Shunji Nakano ◽  
Muneki Ikeda ◽  
Yuki Tsukada ◽  
Xianfeng Fei ◽  
Takamasa Suzuki ◽  
...  
Keyword(s):  
Inhibitory Response ◽  
Thermal Gradients ◽  
Presynaptic Neuron ◽  
C Elegans ◽  
Presynaptic Plasticity ◽  
Freely Behaving ◽  
Stimulus Valence ◽  
Presynaptic Regulation ◽  
Thermal Stimuli ◽  
Synaptic Responses

AbstractPresynaptic plasticity is known to modulate the strength of synaptic transmission. However, it remains unknown whether regulation in presynaptic neurons alters the directionality –positive or negative-of postsynaptic responses. We report here that the C. elegans homologs of MAST kinase, Stomatin and Diacylglycerol kinase act in a thermosensory neuron to elicit in its postsynaptic neuron an excitatory or inhibitory response that correlates with the valence of thermal stimuli. By monitoring neural activity of the valence-coding interneuron in freely behaving animals, we show that the alteration between excitatory and inhibitory responses of the interneuron is mediated by controlling the balance of two opposing signals released from the presynaptic neuron. These alternative transmissions further generate opposing behavioral outputs necessary for the navigation on thermal gradients. Our findings reveal the previously unrecognized capability of presynaptic regulation to evoke bidirectional postsynaptic responses and suggest a molecular mechanism of determining stimulus valence.

scholarly journals Presynaptic MAST kinase controls opposing postsynaptic responses to convey stimulus valence in Caenorhabditis elegans

2020 ◽  
Vol 117 (3) ◽  
pp. 1638-1647 ◽  
Author(s):  
Shunji Nakano ◽  
Muneki Ikeda ◽  
Yuki Tsukada ◽  
Xianfeng Fei ◽  
Takamasa Suzuki ◽  
...  
Keyword(s):  
Caenorhabditis Elegans ◽  
Diacylglycerol Kinase ◽  
Inhibitory Response ◽  
Thermal Gradients ◽  
Postsynaptic Neuron ◽  
Presynaptic Neuron ◽  
Presynaptic Plasticity ◽  
Freely Behaving ◽  
Stimulus Valence ◽  
Thermal Stimuli

Presynaptic plasticity is known to modulate the strength of synaptic transmission. However, it remains unknown whether regulation in presynaptic neurons can evoke excitatory and inhibitory postsynaptic responses. We report here that the Caenorhabditis elegans homologs of MAST kinase, Stomatin, and Diacylglycerol kinase act in a thermosensory neuron to elicit in its postsynaptic neuron an excitatory or inhibitory response that correlates with the valence of thermal stimuli. By monitoring neural activity of the valence-coding interneuron in freely behaving animals, we show that the alteration between excitatory and inhibitory responses of the interneuron is mediated by controlling the balance of two opposing signals released from the presynaptic neuron. These alternative transmissions further generate opposing behavioral outputs necessary for the navigation on thermal gradients. Our findings suggest that valence-encoding interneuronal activity is determined by a presynaptic mechanism whereby MAST kinase, Stomatin, and Diacylglycerol kinase influence presynaptic outputs.

scholarly journals Calcium imaging of multiple neurons in freely behaving C. elegans

2012 ◽  
Vol 206 (1) ◽  
pp. 78-82 ◽  
Author(s):  
Maohua Zheng ◽  
Pengxiu Cao ◽  
Jiong Yang ◽  
X.Z. Shawn Xu ◽  
Zhaoyang Feng
Keyword(s):  
Calcium Imaging ◽  
C Elegans ◽  
Freely Behaving

scholarly journals Pan-neuronal screening in Caenorhabditis elegans reveals asymmetric dynamics of AWC neurons is critical for thermal avoidance behavior

eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Ippei Kotera ◽  
Nhat Anh Tran ◽  
Donald Fu ◽  
Jimmy HJ Kim ◽  
Jarlath Byrne Rodgers ◽  
...  
Keyword(s):  
Avoidance Behavior ◽  
Calcium Imaging ◽  
Functional Screening ◽  
Noxious Heat ◽  
Thermal Nociception ◽  
C Elegans ◽  
Low Efficiency ◽  
Behavioral Transition ◽  
Thermal Stimuli

Understanding neural functions inevitably involves arguments traversing multiple levels of hierarchy in biological systems. However, finding new components or mechanisms of such systems is extremely time-consuming due to the low efficiency of currently available functional screening techniques. To overcome such obstacles, we utilize pan-neuronal calcium imaging to broadly screen the activity of the C. elegans nervous system in response to thermal stimuli. A single pass of the screening procedure can identify much of the previously reported thermosensory circuitry as well as identify several unreported thermosensory neurons. Among the newly discovered neural functions, we investigated in detail the role of the AWCOFF neuron in thermal nociception. Combining functional calcium imaging and behavioral assays, we show that AWCOFF is essential for avoidance behavior following noxious heat stimulation by modifying the forward-to-reversal behavioral transition rate. We also show that the AWCOFF signals adapt to repeated noxious thermal stimuli and quantify the corresponding behavioral adaptation.

scholarly journals Recurrent Neural Networks with Interpretable Cells Predict and Classify Worm Behaviour

2017 ◽  
Author(s):  
Kezhi Li ◽  
Avelino Javer ◽  
Eric E. Keaveny ◽  
Andre E.X. Brown
Keyword(s):  
Generative Models ◽  
Sensor Technology ◽  
Test Analysis ◽  
Artificial Neuron ◽  
C Elegans ◽  
Large Databases ◽  
Artificial Neurons ◽  
Mutant Strains ◽  
Freely Behaving ◽  
Nematode Worm

AbstractAn important goal in behaviour analytics is to connect disease state or genome variation with observable differences in behaviour. Despite advances in sensor technology and imaging, informative behaviour quantification remains challenging. The nematode worm C. elegans provides a unique opportunity to test analysis approaches because of its small size, compact nervous system, and the availability of large databases of videos of freely behaving animals with known genetic differences. Despite its relative simplicity, there are still no reports of generative models that can capture essential differences between even well-described mutant strains. Here we show that a multilayer recurrent neural network (RNN) can produce diverse behaviours that are difficult to distinguish from real worms’ behaviour and that some of the artificial neurons in the RNN are interpretable and correlate with observable features such as body curvature, speed, and reversals. Although the RNN is not trained to perform classification, we find that artificial neuron responses provide features that perform well in worm strain classification.

Seizures Induce Simultaneous GABAergic and Glutamatergic Transmission in the Dentate Gyrus-CA3 System

2000 ◽  
Vol 84 (6) ◽  
pp. 3088-3090 ◽  
Author(s):  
Rafael Gutiérrez
Keyword(s):  
Dentate Gyrus ◽  
Mossy Fibers ◽  
Pyramidal Cells ◽  
Inhibitory Response ◽  
Excitatory Postsynaptic Potential ◽  
Postsynaptic Potential ◽  
Ca3 Pyramidal Cells ◽  
Neuronal Sprouting ◽  
Kindled Seizures ◽  
Synaptic Responses

Monosynaptic and polysynaptic responses of CA3 pyramidal cells (PC) to stimulation of the dentate gyrus (DG) are normally blocked by glutamate receptor antagonists (GluRAs). However, after kindled seizures, GluRAs block the monosynaptic excitatory postsynaptic potential (EPSP) and isolate a monosynaptic inhibitory postsynaptic potential (IPSP), suggesting that mossy fibers release GABA. However, kindling epilepsy induces neuronal sprouting, which can underlie this fast inhibitory response. To explore this possibility, the synaptic responses of PC to DG stimulation were analyzed in kindled epileptic rats, with and without seizures, and in nonepileptic rats, immediately after a single pentylenetetrazol (PTZ)-induced seizure, in which sprouting is unlikely to have occurred. Excitatory and inhibitory synaptic responses of PC to DG stimulation were blocked by GluRAs in control cells and in cells from kindled nonseizing rats, confirming that inhibitory potentials are disynaptically mediated. However, a fast IPSP could be evoked in kindled epileptic rats and in nonepileptic rats after a single PTZ-induced seizure. The same response was induced after rekindling the epileptic nonseizing rats. This IPSP has an onset latency that parallels that of the control EPSP and is not altered under low Ca2+ medium or halothane perfusion. In addition, it was reversibly depressed byl(+)-2-amino-4-phosphonobutyric acid (l-AP4), which is known to inhibit transmitter release from mossy fibers. These results demonstrate that seizures, and not the synaptic rearrangement due to an underlying epileptic state, induce the emergence of fast inhibition in the DG-CA3 system, and suggest that the mossy fibers underlie this plastic change.

scholarly journals Integration of plasticity mechanisms within a single sensory neuron of C. elegans actuates a memory

2017 ◽  
Author(s):  
Josh D. Hawk ◽  
Ana C. Calvo ◽  
Agustin Almoril-Porras ◽  
Ahmad Aljobeh ◽  
Maria Luisa Torruella-Suárez ◽  
...  
Keyword(s):  
Single Cell ◽  
Sensory Neuron ◽  
Neural Plasticity ◽  
Sensory Information ◽  
Sensory Adaptation ◽  
Sensory Stimuli ◽  
C Elegans ◽  
Presynaptic Plasticity ◽  
Behavioral Preference

SummaryNeural plasticity—the ability of a neuron to change its cellular properties in response to past experiences—underpins the nervous system’s capacity to form memories and actuate behaviors. How different plasticity mechanisms act together in vivo and at a cellular level to transform sensory information into behavior is not well understood. Here we show that in the nematode C. elegans two plasticity mechanisms—sensory adaptation and presynaptic plasticity—act within a single cell to encode thermosensory information and actuate a temperature-preference memory. Sensory adaptation enables the primary thermosensory neuron, AFD, to adjust the temperature range of its sensitivity to the local environment, thereby optimizing its ability to detect temperature fluctuations associated with migration. Presynaptic plasticity transforms this thermosensory information into a behavioral preference by gating synaptic communication between sensory neuron AFD and its postsynaptic partner, AIY. The gating of synaptic communication is regulated at AFD presynaptic sites by the conserved kinase nPKCε. Bypassing or altering AFD presynaptic plasticity predictably changes the learned behavioral preferences without affecting sensory responses. Our findings indicate that two distinct and modular neuroplasticity mechanisms function together within a single sensory neuron to encode multiple components of information required to enact thermotactic behavior. The integration of these plasticity mechanisms result in a single-cell logic system that can both represent sensory stimuli and guide memory-based behavioral preference.

Dopamine Activates Two Different Receptors to Produce Variability in Sign at an Identified Synapse

1999 ◽  
Vol 81 (3) ◽  
pp. 1330-1340 ◽  
Author(s):  
Neil S. Magoski ◽  
Andrew G. M. Bulloch
Keyword(s):  
Lymnaea Stagnalis ◽  
Freshwater Snail ◽  
Inhibitory Response ◽  
Postsynaptic Neuron ◽  
Presynaptic Neuron ◽  
Postsynaptic Potential ◽  
Bath Application ◽  
Continuous Bath ◽  
Two Populations ◽  
Reversal Potentials

Dopamine activates two different receptors to produce variability in sign at an identified synapse. Chemical synaptic transmission was investigated at a central synapse between identified neurons in the freshwater snail, Lymnaea stagnalis. The presynaptic neuron was the dopaminergic cell, Right Pedal Dorsal one (RPeD1). The postsynaptic neuron was Visceral Dorsal four (VD4). These neurons are components of the respiratory central pattern generator. The synapse from RPeD1 to VD4 showed variability of sign, i.e., it was either inhibitory (monophasic and hyperpolarizing), biphasic (depolarizing followed by hyperpolarizing phases), or undetectable. Both the inhibitory and biphasic synapse were eliminated by low Ca2+/high Mg2+ saline and maintained in high Ca2+/high Mg2+ saline, indicating that these two types of connections were chemical and monosynaptic. The latency of the inhibitory postsynaptic potential (IPSP) in high Ca2+/high Mg2+ saline was ∼43 ms, whereas the biphasic postsynaptic potential (BPSP) had ∼12-ms latency in either normal or high Ca2+/high Mg2+ saline. For a given preparation, when dopamine was pressured applied to the soma of VD4, it always elicited the same response as the synaptic input from RPeD1. Thus, for a VD4 neuron receiving an IPSP from RPeD1, pressure application of dopamine to the soma of VD4 produced an inhibitory response similar to the IPSP. The reversal potentials of the IPSP and the inhibitory dopamine response were both approximately −90 mV. For a VD4 neuron with a biphasic input from RPeD1, pressure-applied dopamine produced a biphasic response similar to the BPSP. The reversal potentials of the depolarizing phase of the BPSP and the biphasic dopamine response were both approximately −44 mV, whereas the reversal potentials for the hyperpolarizing phases were both approximately −90 mV. The hyperpolarizing but not the depolarizing phase of the BPSP and the biphasic dopamine response was blocked by the d-2 dopaminergic antagonist (±) sulpiride. Previously, our laboratory demonstrated that both IPSP and the inhibitory dopamine response are blocked by (±) sulpiride. Conversely, the depolarizing phase of both the BPSP and the biphasic dopamine response was blocked by the Cl− channel antagonist picrotoxin. Finally, both phases of the BPSP and the biphasic dopamine response were desensitized by continuous bath application of dopamine. These results indicate that the biphasic RPeD1 → VD4 synapse is dopaminergic. Collectively, these data suggest that the variability in sign (inhibitory vs. biphasic) at the RPeD1 → VD4 synapse is due to activation of two different dopamine receptors on the postsynaptic neuron VD4. This demonstrates that two populations of receptors can produce two different forms of transmission, i.e., the inhibitory and biphasic forms of the single RPeD1 → VD4 synapse.

Intestinal Ca2+ wave dynamics in freely moving C. elegans coordinate execution of a rhythmic motor program

2008 ◽  
Vol 294 (1) ◽  
pp. C333-C344 ◽  
Author(s):  
K. Nehrke ◽  
Jerod Denton ◽  
William Mowrey
Keyword(s):  
Model Organism ◽  
Motor Program ◽  
Wave Dynamics ◽  
C Elegans ◽  
Plasmic Reticulum ◽  
Rhythmic Behavior ◽  
Freely Behaving ◽  
Trisphosphate Receptor ◽  
Nematode Worm ◽  
Worm Caenorhabditis Elegans

Defecation in the nematode worm Caenorhabditis elegans is a highly rhythmic behavior that is regulated by a Ca2+ wave generated in the 20 epithelial cells of the intestine, in part through activation of the inositol 1,4,5-trisphosphate receptor. Execution of the defecation motor program (DMP) can be modified by external cues such as nutrient availability or mechanical stimulation. To address the likelihood that environmental regulation of the DMP requires integrating distinct cellular and organismal processes, we have developed a method for studying coordinate Ca2+ oscillations and defecation behavior in intact, freely behaving animals. We tested this technique by examining how mutations in genes known to alter Ca2+ handling [including egl-8/phospholipase C (PLC)-β, kqt-3/KCNQ1, sca-1/sarco(endo)plasmic reticulum Ca2+ ATPase, and unc-43/Ca2+-CaMKII] contribute to shaping the Ca2+ wave and asked how Ca2+ wave dynamics in the mutant backgrounds altered execution of the DMP. Notably, we find that Ca2+ waves in the absence of PLCβ initiate ectopically, often traveling in reverse, and fail to trigger a complete DMP. These results suggest that the normal supremacy of the posterior intestinal cells is not obligatory for Ca2+ wave occurrence but instead helps to coordinate the DMP. Furthermore, we present evidence suggesting that an underlying pacemaker appears to oscillate at a faster frequency than the defecation cycle and that arrhythmia may result from uncoupling the pacemaker from the DMP rather than from disrupting the pacemaker itself. We also show that chronic elevations in Ca2+ have limited influence on the defecation period but instead alter the interval between successive steps of the DMP. Finally, our results demonstrate that it is possible to assess Ca2+ dynamics and muscular contractions in a completely unrestrained model organism.

Short-Term Adaptation and Temporal Processing in the Cryophilic Response of Caenorhabditis elegans

2007 ◽  
Vol 97 (3) ◽  
pp. 1903-1910 ◽  
Author(s):  
Damon A. Clark ◽  
Christopher V. Gabel ◽  
Timothy M. Lee ◽  
Aravinthan D. T. Samuel
Keyword(s):  
Temporal Dynamics ◽  
Time Derivative ◽  
Neural Mechanisms ◽  
Thermal Gradients ◽  
Short Term ◽  
Forward Movement ◽  
Operating Range ◽  
C Elegans ◽  
Biased Random Walk ◽  
Short Term Adaptation

When navigating spatial thermal gradients, the nematode C. elegans migrates toward colder temperatures until it reaches its previous cultivation temperature, exhibiting cryophilic movement. The strategy for effecting cryophilic movement is the biased random walk: C. elegans extends (shortens) periods of forward movement that are directed down (up) spatial thermal gradients by modulating the probability of reorientation. Here, we analyze the temporal sensory processor that enables cryophilic movement by quantifying the movements of individual worms subjected to defined temperature waveforms. We show that step increases in temperature as small as 0.05°C lead to transient increases in the probability of reorientation followed by gradual adaptation to the baseline level; temperature downsteps leads to similar but inverted responses. Short-term adaptation is a general property of sensory systems, allowing organisms to maintain sensitivity to sensory variations over broad operating ranges. During cryophilic movement C. elegans also uses the temporal dynamics of its adaptive response to compute the time derivative of gradual temperature variations with exquisite sensitivity. On the basis of the time derivative, the worm determines how it is oriented in spatial thermal gradients during each period of forward movement. We show that the operating range of the cryophilic response extends to lower temperatures in ttx-3 mutants, which affects the development of the AIY interneurons. We show that the temporal sensory processor for the cryophilic response is affected by mutation in the EAT-4 glutamate vesicular transporter. Regulating the operating range of the cryophilic response and executing the cryophilic response may have separate neural mechanisms.

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