scholarly journals The C.elegans AWA Olfactory Neuron Fires Calcium-Mediated All-or-None Action Potentials

2018 ◽  
Author(s):  
Qiang Liu ◽  
Philip B. Kidd ◽  
May Dobosiewicz ◽  
Cornelia I. Bargmann
Keyword(s):  
Calcium Imaging ◽  
Action Potentials ◽  
Neural Coding ◽  
Patch Clamp Recording ◽  
Olfactory Neurons ◽  
C Elegans ◽  
Coding Schemes ◽  
Current Voltage ◽  
Ion Substitution ◽  
Specialized Function

SummaryWe find, unexpectedly, that C. elegans neurons can encode information through regenerative all-or-none action potentials. In a survey of current-voltage relationships in C. elegans neurons, we discovered that AWA olfactory neurons generate membrane potential spikes with defining characteristics of action potentials. Ion substitution experiments, pharmacology, and mutant analysis identified a voltage-gated CaV1 calcium channel and a Shaker-type potassium channel that underlie action potential dynamics in AWA. Simultaneous patch-clamp recording and calcium imaging in AWA revealed spike-associated calcium signals that were also observed after odor stimulation of intact animals, suggesting that natural odor stimuli induce AWA action potentials. The stimulus regimes that elicited action potentials match AWA’s proposed specialized function in climbing odor gradients. Our results provide evidence that C. elegans can use digital as well as analog coding schemes, expand the computational repertoire of its nervous system, and inform future modeling of its neural coding and network dynamics.

Na+ and Ca2+ currents of acutely isolated adult rat nodose ganglion cells

1986 ◽  
Vol 55 (3) ◽  
pp. 527-539 ◽  
Author(s):  
S. R. Ikeda ◽  
G. G. Schofield ◽  
F. F. Weight
Keyword(s):  
Action Potentials ◽  
Time Course ◽  
Ganglion Cells ◽  
Input Resistance ◽  
Potential Range ◽  
Patch Clamp Recording ◽  
Maximal Conductance ◽  
Pharmacological Agents ◽  
Inward Current ◽  
Ion Substitution

The electrical properties of nodose ganglion cells acutely isolated from adult rats were studied using the whole-cell patch-clamp recording method. Current-clamp recordings revealed a mean resting membrane potential of -54.3 mV and an input resistance of 527 M omega. Depolarizing current steps evoked action potentials with the following properties (mean): amplitude 111 mV, threshold -36 mV, and rate of rise 117 V/s. Two types of action potentials were observed, short and long duration. These properties, with the exception of input resistance (527 M omega cf. 50 M omega), are similar to those reported previously using intracellular recording methods in intact nodose ganglia (11, 20, 28). Brief application of 10 microM 5-hydroxytryptamine resulted in a rapid depolarization and burst of action potentials in the majority of cells. With voltage-clamp recording, step depolarizations to potentials positive to -10 mV elicited a transient inward current that was followed by a sustained outward current. Inward Na+ current was isolated by ion substitution and pharmacological agents. Two types of Na+ current were observed. One current was completely abolished by 3-15 microM tetrodotoxin (TTX), had a rapid time course, activated over the potential range -60 to -10 mV, and attained half-maximal conductance at -30 mV. The other current persisted in the presence of 15 microM TTX, had a slower time course, activated over the potential range -30 to 0 mV, and attained half-maximal conductance at -15 mV. In addition, 500 microM Cd2+ and 5.0 mM Co2+ reduced the TTX-insensitive current to 53 and 42% of control, respectively. Inward Ca2+ current was isolated by ion substitution and pharmacological agents and was identified by a dependence on external Ca2+. Cd2+ (500 microM) and Co2+ (5 mM) reduced the maximal inward current to 5 and 20% of control, respectively. When Ba2+ was substituted for Ca2+ as the charge carrier, the maximal inward current increased to 175% of control. Some cells had two Ca2+ current components, an inactivating component that activated near -60 mV and a large sustained current that activated near -40 mV. The initial inactivating current appeared as a "hump" on the current-voltage (I-V) curve over the potential range of -60 to -30 mV. The results indicate that, following isolation of these adult mammalian neurons, the membrane surfaces are sufficiently clean to allow patch-clamp recording.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Transcriptomic profiling of sex-specific olfactory neurons reveals subset-specific receptor expression in C. elegans

2021 ◽  
Author(s):  
Douglas K Reilly ◽  
Erich M Schwarz ◽  
Caroline S Muirhead ◽  
Annalise N Robidoux ◽  
Igor Antoscheckin ◽  
...  
Keyword(s):  
Neural Coding ◽  
Radial Symmetry ◽  
Receptor Expression ◽  
Double Knockout ◽  
Olfactory Neurons ◽  
Transcriptomic Profiling ◽  
C Elegans ◽  
Expression Of Genes ◽  
Gfp Reporter ◽  
Male Specific

The nematode Caenorhabditis elegans utilizes chemosensation to navigate an ever-changing environment for its survival. A class of secreted small-molecule pheromones, termed ascarosides, play an important role in olfactory perception by affecting a host of biological function ranging from development to behavior. The ascaroside ascr#8 mediates sex-specific behaviors, driving avoidance in hermaphrodites and attraction in males. Males sense ascr#8 via the ciliated male-specific cephalic sensory (CEM) neurons, which exhibit radial symmetry along dorsal-ventral and left-right axes. Calcium imaging studies suggest a complex neural coding mechanism that translates stochastic physiological responses in these neurons to reliable behavioral outputs. To test the hypothesis that the neurophysiological complexity arises from differential expression of genes within subsets of these neurons, we performed cell-specific transcriptomic profiling of these sensory neurons. Expression profiling revealed between 20 and 639 genes enriched at least two-fold per CEM neuron and identified multiple G protein coupled receptor (GPCR) candidates enriched in non-overlapping subsets of CEM neurons. GFP reporter analysis confirmed that RNA expression of two of the GPCR genes, srw-97 and dmsr-12, is enriched in specific subsets of the CEM neurons. Single CRISPR-Cas9 knockouts of either srw-97 or dmsr-12 resulted in partial defects, while a double knockout of both srw-97 and dmsr-12 completely abolished the attractive response to ascr#8, suggesting that each receptor acts in a non-redundant manner in discrete olfactory neurons. Together, our results suggest that the evolutionarily distinct GPCRs SRW-97 and DMSR-12 act to facilitate male-specific sensation of ascr#8 through discrete subsets of CEM neurons.

scholarly journals C. elegans AWA Olfactory Neurons Fire Calcium-Mediated All-or-None Action Potentials

Cell ◽  
2018 ◽  
Vol 175 (1) ◽  
pp. 57-70.e17 ◽  
Author(s):  
Qiang Liu ◽  
Philip B. Kidd ◽  
May Dobosiewicz ◽  
Cornelia I. Bargmann
Keyword(s):  
Action Potentials ◽  
Olfactory Neurons ◽  
C Elegans

Ionic Basis of the Resting Membrane Potential and Action Potential in the Pharyngeal Muscle of Caenorhabditis elegans

2002 ◽  
Vol 87 (2) ◽  
pp. 954-961 ◽  
Author(s):  
Christopher J. Franks ◽  
Darrel Pemberton ◽  
Irina Vinogradova ◽  
Alan Cook ◽  
Robert J. Walker ◽  
...  
Keyword(s):  
Membrane Potential ◽  
Action Potential ◽  
Action Potentials ◽  
Resting Membrane Potential ◽  
Channel Blockers ◽  
Voltage Gated ◽  
C Elegans ◽  
Current Voltage ◽  
Prolongation Of Action Potential ◽  
Ionic Basis

The pharynx of C. elegans is a rhythmically active muscle that pumps bacteria into the gut of the nematode. This activity is maintained by action potentials, which qualitatively bear a resemblance to vertebrate cardiac action potentials. Here, the ionic basis of the resting membrane potential and pharyngeal action potential has been characterized using intracellular recording techniques. The resting membrane potential is largely determined by a K+permeability, and a ouabain-sensitive, electrogenic pump. As previously suggested, the action potential is at least partly dependent on voltage-gated Ca2+ channels, as the amplitude was increased as extracellular Ca2+ was increased, and decreased by L-type Ca2+ channel blockers verapamil and nifedipine. Barium caused a marked prolongation of action potential duration, suggesting that a calcium-activated K+ current may contribute to repolarization. Most notably, however, we found that action potentials were abolished in the absence of external Na+. This may be due, at least in part, to a Na+-dependent pacemaker potential. In addition, the persistence of action potentials in nominally free Ca2+, the inhibition by Na+ channel blockers procaine and quinidine, and the increase in action potential frequency caused by veratridine, a toxin that alters activation of voltage-gated Na+channels, point to the involvement of a voltage-gated Na+ current. Voltage-clamp analysis is required for detailed characterization of this current, and this is in progress. Nonetheless, these observations are quite surprising in view of the lack of any obvious candidate genes for voltage-gated Na+ channels in the C. elegans genome. It would therefore be informative to re-evaluate the data from these homology searches, with the aim of identifying the gene(s) conferring this Na+, quinidine, and veratridine sensitivity to the pharynx.

The Caenorhabditis elegans odr-2 Gene Encodes a Novel Ly-6-Related Protein Required for Olfaction

Genetics ◽  
2001 ◽  
Vol 157 (1) ◽  
pp. 211-224 ◽  
Author(s):  
Joseph H Chou ◽  
Cornelia I Bargmann ◽  
Piali Sengupta
Keyword(s):  
Caenorhabditis Elegans ◽  
Motor Neurons ◽  
Amino Terminus ◽  
Signaling Proteins ◽  
Related Protein ◽  
Olfactory Neurons ◽  
Unique Role ◽  
C Elegans ◽  
Founding Member ◽  
High Concentrations

Abstract Caenorhabditis elegans odr-2 mutants are defective in the ability to chemotax to odorants that are recognized by the two AWC olfactory neurons. Like many other olfactory mutants, they retain responses to high concentrations of AWC-sensed odors; we show here that these residual responses are caused by the ability of other olfactory neurons (the AWA neurons) to be recruited at high odor concentrations. odr-2 encodes a membrane-associated protein related to the Ly-6 superfamily of GPI-linked signaling proteins and is the founding member of a C. elegans gene family with at least seven other members. Alternative splicing of odr-2 yields three predicted proteins that differ only at the extreme amino terminus. The three isoforms have different promoters, and one isoform may have a unique role in olfaction. An epitope-tagged ODR-2 protein is expressed at high levels in sensory neurons, motor neurons, and interneurons and is enriched in axons. The AWC neurons are superficially normal in their development and structure in odr-2 mutants, but their function is impaired. Our results suggest that ODR-2 may regulate AWC signaling within the neuronal network required for chemotaxis.

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 Action Potentials in Rhodnius Oocytes: Repolarization is Sensitive to Potassium Channel Blockers

1986 ◽  
Vol 126 (1) ◽  
pp. 119-132
Author(s):  
M. J. O'DONNELL
Keyword(s):  
Potassium Channel ◽  
Action Potentials ◽  
Potassium Conductance ◽  
Channel Blockers ◽  
Calcium Dependent ◽  
Outward Rectification ◽  
Current Voltage ◽  
Potassium Channel Blockers ◽  
Potassium Conductances ◽  
Voltage Dependent

Depolarization of Rhodnius oocytes evokes action potentials (APs) whose rising phase is calcium-dependent. The ionic basis for the repolarizing (i.e. falling) phase of the AP was examined. Addition of potassium channel blockers (tetraethylammonium, tetrabutylammonium, 4-aminopyridine, atropine) to the bathing saline increased the duration and overshoot of APs. Intracellular injection of tetraethyl ammonium had similar effects. These results suggest that a voltage-dependent potassium conductance normally contributes to repolarization. Repolarization does not require a chloride influx, because substitution of impermeant anions for chloride did not increase AP duration. AP duration and overshoot actually decreased progressively when chloride levels were reduced. Current/voltage curves show inward and outward rectification, properties often associated with potassium conductances. Outward rectification was largely blocked by external tetraethylammonium. Possible functions of the rectifying properties of the oocyte membrane are discussed.

scholarly journals Progressive recruitment of distal MEC-4 channels determines touch response strength in C. elegans

2019 ◽  
Author(s):  
S. Katta ◽  
A. Sanzeni ◽  
A. Das ◽  
M. Vergassola ◽  
M.B. Goodman
Keyword(s):  
Temporal Dynamics ◽  
Mechanical Strain ◽  
Tissue Mechanics ◽  
Mechanical Stimuli ◽  
Patch Clamp Recording ◽  
Open Probability ◽  
C Elegans ◽  
Somatosensory Neurons ◽  
Touch Response

AbstractTouch deforms, or strains, the skin beyond the immediate point of contact. The spatiotemporal nature of the touch-induced strain fields depend on the mechanical properties of the skin and the tissues below. Somatosensory neurons that sense touch branch out within the skin and rely on a set of mechano-electrical transduction channels distributed within their dendrites to detect mechanical stimuli. Here, we sought to understand how tissue mechanics shape touch-induced mechanical strain across the skin over time and how individual channels located in different regions of the strain field contribute to the overall touch response. We leveraged C. elegans’ touch receptor neurons (TRNs) as a simple model amenable to in vivo whole-cell patch clamp recording and an integrated experimental-computational approach to dissect the mechanisms underlying the spatial and temporal dynamics that we observed. Consistent with the idea that strain is produced at a distance, we show that delivering strong stimuli outside the anatomical extent of the neuron is sufficient to evoke MRCs. The amplitude and kinetics of the MRCs depended on both stimulus displacement and speed. Finally, we found that the main factor responsible for touch sensitivity is the recruitment of progressively more distant channels by stronger stimuli, rather than modulation of channel open probability. This principle may generalize to somatosensory neurons with more complex morphologies.SummaryThrough experiment and simulation, Katta et al. reveal that pushing faster and deeper recruits more and more distant mechano-electrical transduction channels during touch. The net result is a dynamic receptive field whose size and shape depends on tissue mechanics, stimulus parameters, and channel distribution within sensory neurons.

scholarly journals The quest for action potentials in C. elegans neurons hits a plateau

2009 ◽  
Vol 12 (4) ◽  
pp. 377-378 ◽  
Author(s):  
Shawn R Lockery ◽  
Miriam B Goodman
Keyword(s):  
Action Potentials ◽  
C Elegans
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