Elegans Touch Receptor Neurons Research Articles

C. elegans touch receptor neurons direct mechanosensory complex organization via repurposing conserved basal lamina proteins

The sense of touch is conferred by the conjoint function of somatosensory neurons and skin cells. These cells meet across a gap filled by a basal lamina, an ancient structure found in metazoans. Using Caenorhabditis elegans, we investigate the composition and ultrastructure of the extracellular matrix at the epidermis and touch receptor neuron (TRN) interface. We show that membrane-matrix complexes containing laminin, nidogen, and the MEC-4 mechano-electrical transduction channel reside at this interface and are central to proper touch sensation. Interestingly, the dimensions and spacing of these complexes correspond with the discontinuous beam-like extracellular matrix structures observed in serial-section transmission electron micrographs. These complexes fail to coalesce in touch-insensitive extracellular matrix mutants and in dissociated neurons. Loss of nidogen reduces the density of mechanoreceptor complexes and the amplitude of the touch-evoked currents they carry. Thus, neuron-epithelium cell interfaces are instrumental in mechanosensory complex assembly and function. Unlike the basal lamina ensheathing the pharynx and body wall muscle, nidogen recruitment to the puncta along TRNs is not dependent upon laminin binding. MEC-4, but not laminin or nidogen, is destabilized by point mutations in the C-terminal Kunitz domain of the extracellular matrix component, MEC-1. These findings imply that somatosensory neurons secrete proteins that actively repurpose the basal lamina to generate special-purpose mechanosensory complexes responsible for vibrotactile sensing.

Tracking Mitochondrial Density and Positioning along a Growing Neuronal Process in Individual C. elegans Neuron Using a Long-Term Growth and Imaging Microfluidic Device.

The long cellular architecture of neurons requires regulation in part through transport and anchoring events to distribute intracellular organelles. During development, cellular and subcellular events such as organelle additions and their recruitment at specific sites on the growing axons occur over different time scales and often show interanimal variability thus making it difficult to identify specific phenomena in population averages. To measure the variability in subcellular events such as organelle positions, we developed a microfluidic device to feed and immobilize Caenorhabditis elegans for high-resolution imaging over several days. The microfluidic device enabled long-term imaging of individual animals and allowed us to investigate organelle density using mitochondria as a testbed in a growing neuronal process in vivo Subcellular imaging of an individual neuron in multiple animals, over 36 h in our microfluidic device, shows the addition of new mitochondria along the neuronal process and an increase in the accumulation of synaptic vesicles (SVs) at synapses. Long-term imaging of individual C. elegans touch receptor neurons (TRNs) shows that the addition of new mitochondria takes place along the entire neuronal process length at a rate of ∼0.6 mitochondria/h. The threshold for the addition of a new mitochondrion occurs when the average separation between the two preexisting mitochondria exceeds 24 μm. Our assay provides a new opportunity to move beyond simple observations obtained from in vitro assays to allow the discovery of genes that regulate positioning of mitochondria in neurons.

Cargo crowding at actin-rich regions along axons causes local traffic jams.

Steady axonal cargo flow is central to the functioning of healthy neurons. However, a substantial fraction of cargo in axons remains stationary up to several minutes. We examine the transport of precursors of synaptic vesicles (pre-SVs), endosomes and mitochondria in Caenorhabditis elegans touch receptor neurons, showing that stationary cargo are predominantly present at actin-rich regions along the neuronal process. Stationary vesicles at actin-rich regions increase the propensity of moving vesicles to stall at the same location, resulting in traffic jams arising from physical crowding. Such local traffic jams at actin-rich regions are likely to be a general feature of axonal transport since they also occur in Drosophila neurons. Repeated touch stimulation of C. elegans reduces the density of stationary pre-SVs, indicating that these traffic jams can act as both sources and sinks of vesicles. This suggests that vesicles trapped in actin-rich regions are functional reservoirs that may contribute to maintaining robust cargo flow in the neuron. A video abstract of this article can be found at: Video S1; Video S2.

Distinct effects of tubulin isotype mutations on neurite growth in Caenorhabditis elegans.

Tubulins, the building block of microtubules (MTs), play a critical role in both supporting and regulating neurite growth. Eukaryotic genomes contain multiple tubulin isotypes, and their missense mutations cause a range of neurodevelopmental defects. Using the Caenorhabditis elegans touch receptor neurons, we analyzed the effects of 67 tubulin missense mutations on neurite growth. Three types of mutations emerged: 1) loss-of-function mutations, which cause mild defects in neurite growth; 2) antimorphic mutations, which map to the GTP binding site and intradimer and interdimer interfaces, significantly reduce MT stability, and cause severe neurite growth defects; and 3) neomorphic mutations, which map to the exterior surface, increase MT stability, and cause ectopic neurite growth. Structure-function analysis reveals a causal relationship between tubulin structure and MT stability. This stability affects neuronal morphogenesis. As part of this analysis, we engineered several disease-associated human tubulin mutations into C. elegans genes and examined their impact on neuronal development at the cellular level. We also discovered an α-tubulin (TBA-7) that appears to destabilize MTs. Loss of TBA-7 led to the formation of hyperstable MTs and the generation of ectopic neurites; the lack of potential sites for polyamination and polyglutamination on TBA-7 may be responsible for this destabilization.

Activation of the Caenorhabditis elegans Degenerin Channel by Shear Stress Requires the MEC-10 Subunit

Mechanotransduction in Caenorhabditis elegans touch receptor neurons is mediated by an ion channel formed by MEC-4, MEC-10, and accessory proteins. To define the role of these subunits in the channel's response to mechanical force, we expressed degenerin channels comprising MEC-4 and MEC-10 in Xenopus oocytes and examined their response to laminar shear stress (LSS). Shear stress evoked a rapid increase in whole cell currents in oocytes expressing degenerin channels as well as channels with a MEC-4 degenerin mutation (MEC-4d), suggesting that C. elegans degenerin channels are sensitive to LSS. MEC-10 is required for a robust LSS response as the response was largely blunted in oocytes expressing homomeric MEC-4 or MEC-4d channels. We examined a series of MEC-10/MEC-4 chimeras to identify specific domains (amino terminus, first transmembrane domain, and extracellular domain) and sites (residues 130-132 and 134-137) within MEC-10 that are required for a robust response to shear stress. In addition, the LSS response was largely abolished by MEC-10 mutations encoded by a touch-insensitive mec-10 allele, providing a correlation between the channel's responses to two different mechanical forces. Our findings suggest that MEC-10 has an important role in the channel's response to mechanical forces.

A Novel MitoTimer Reporter Gene for Mitochondrial Content, Structure, Stress, and Damage in Vivo

Mitochondrial dysfunction plays important roles in many diseases, but there is no satisfactory method to assess mitochondrial health in vivo. Here, we engineered a MitoTimer reporter gene from the existing Timer reporter gene. MitoTimer encodes a mitochondria-targeted green fluorescent protein when newly synthesized, which shifts irreversibly to red fluorescence when oxidized. Confocal microscopy confirmed targeting of the MitoTimer protein to mitochondria in cultured cells, Caenorhabditis elegans touch receptor neurons, Drosophila melanogaster heart and indirect flight muscle, and mouse skeletal muscle. A ratiometric algorithm revealed that conditions that cause mitochondrial stress led to a significant shift toward red fluorescence as well as accumulation of pure red fluorescent puncta of damaged mitochondria targeted for mitophagy. Long term voluntary exercise resulted in a significant fluorescence shift toward green, in mice and D. melanogaster, as well as significantly improved structure and increased content in mouse FDB muscle. In contrast, high-fat feeding in mice resulted in a significant shift toward red fluorescence and accumulation of pure red puncta in skeletal muscle, which were completely ameliorated by voluntary wheel running. Hence, MitoTimer allows for robust analysis of multiple parameters of mitochondrial health under both physiological and pathological conditions and will be highly useful for future research of mitochondrial health in multiple disciplines in vivo.

Omega 6 Polyunsaturated Fatty Acid-Containing Phospholipids Enhance Neuronal Cell Mechanics and Touch in C. Elegans

Mechano-electrical transduction (MeT) channels embedded in neuronal cell membranes are essential for touch and proprioception. Little is understood about the interplay between native MeT channels and membrane phospholipids, in part because few techniques are available for altering plasma membrane composition in vivo. Here, we leverage genetic dissection, chemical complementation, and optogenetics to establish that arachidonic acid (AA), an omega 6 polyunsaturated fatty acid (PUFA), enhances touch sensation and mechanoelectrical transduction activity while incorporated into membrane phospholipids in C. elegans touch receptor neurons (TRNs). We found that arachidonic acid acts cell autonomously, since we show that enzymes needed for its synthesis are expressed in TRNs. We also established that the membrane viscoelastic properties of TRNs lacking omega 6 PUFAs are altered (i.e., membrane bending and viscosity), yielding less flexible membranes than wild type, as determined by atomic force microscopy (AFM) based single-tether extrusion. Our data suggest that the defect in touch sensation likely reflects a loss of mechanotransduction rather than lack of excitability or downstream signaling. These findings establish that polyunsaturated phospholipids are crucial determinants of both the biochemistry and mechanics of mechanoreceptor neurons and reinforce the idea that sensory mechanotransduction in animals relies on a cellular machine composed of both proteins and membrane lipids.

Posttranslational Acetylation of α-Tubulin Constrains Protofilament Number in Native Microtubules

Microtubules are built from linear polymers of α-β tubulin dimers (protofilaments) that form a tubular quinary structure. Microtubules assembled from purified tubulin in vitro contain between 10 and 16 protofilaments; however, such structural polymorphisms are not found in cells. This discrepancy implies that factors other than tubulin constrain microtubule protofilament number, but the nature of these constraints is unknown. Here, we show that acetylation of MEC-12 α-tubulin constrains protofilament number in C. elegans touch receptor neurons (TRNs). Whereas the sensory dendrite of wild-type TRNs is packed with a cross-linked bundle of long, 15-protofilament microtubules, mec-17;atat-2 mutants lacking α-tubulin acetyltransferase activity have short microtubules, rampant lattice defects, and variable protofilament number both between and within microtubules. All-atom molecular dynamics simulations suggest a model in which acetylation of lysine 40 promotes the formation of interprotofilament salt bridges, stabilizing lateral interactions between protofilaments and constraining quinary structure to produce stable, structurally uniform microtubules in vivo. Acetylation of α-tubulin is an essential constraint on protofilament number in vivo. We propose a structural model in which this posttranslational modification promotes the formation of lateral salt bridges that fine-tune the association between adjacent protofilaments and enable the formation of uniform microtubule populations in vivo.

C. elegans model of neuronal aging

Aging of the nervous system underlies the behavioral and cognitive decline associated with senescence. Understanding the molecular and cellular basis of neuronal aging will therefore contribute to the development of effective treatments for aging and age-associated neurodegenerative disorders. Despite this pressing need, there are surprisingly few animal models that aim at recapitulating neuronal aging in a physiological context. We recently developed a C. elegans model of neuronal aging, and showed that age-dependent neuronal defects are regulated by insulin signaling. We identified electrical activity and epithelial attachment as two critical factors in the maintenance of structural integrity of C. elegans touch receptor neurons. These findings open a new avenue for elucidating the molecular mechanisms that maintain neuronal structures during the course of aging.

Microtubule depolymerization in Caenorhabditis elegans touch receptor neurons reduces gene expression through a p38 MAPK pathway.

Microtubules are integral to neuronal development and function. They endow cells with polarity, shape, and structure, and their extensive surface area provides substrates for intracellular trafficking and scaffolds for signaling molecules. Consequently, microtubule polymerization dynamics affect not only structural features of the cell but also the subcellular localization of proteins that can trigger intracellular signaling events. In the nematode Caenorhabditis elegans, the processes of touch receptor neurons are filled with a bundle of specialized large-diameter microtubules. We find that conditions that disrupt these microtubules (loss of either the MEC-7 β-tubulin or MEC-12 α-tubulin or growth in 1 mM colchicine) cause a general reduction in touch receptor neuron (TRN) protein levels. This reduction requires a p38 MAPK pathway (DLK-1, MKK-4, and PMK-3) and the transcription factor CEBP-1. Cells may use this feedback pathway that couples microtubule state and MAPK activation to regulate cellular functions.

Conditional gene expression and RNAi using MEC-8–dependent splicing in C. elegans

SummaryWe describe a method for conditional regulation of gene expression based on the processing of an intron cassette by a splicing factor. The RNA processing factor MEC-8 is necessary for the function of the Caenorhabditis elegans touch receptor neurons; mec-8 mutants are touch insensitive. We show here that this insensitivity involves the loss of MEC-8-dependent splicing of mec-2, which encodes a component of the mechanosensory transduction complex. MEC-8 is needed to remove the ninth intron in mec-2 pre-mRNA to form the longest of three mRNAs, mec-2a. Without MEC-8, splicing causes the termination of the transcript. Inclusion of mec-2 intron 9 is sufficient to convey mec-8-dependent regulation on other genes and, in mec-8(u218ts) mutants, resulted in their temperature-dependent expression. Because mec-8 is expressed ubiquitously in embryos and extensively in larvae, this system should produce temperature-sensitive expression for most genes. We report a strain that exhibits temperature-dependent RNA interference.

Mec-15 Encodes an F-Box Protein Required for Touch Receptor Neuron Mechanosensation, Synapse Formation and Development

Selective protein degradation is a key regulator of neuronal development and synaptogenesis. Complexes that target proteins for degradation often contain F-box proteins. Here we characterize MEC-15, an F-box protein with WD repeats, which is required for the development and function of Caenorhabditis elegans touch receptor neurons (TRNs). Mutations in mec-15 produce defects in TRN touch sensitivity, chemical synapse formation, and cell-body morphology. All mec-15 mutant phenotypes are enhanced by mutations in a MAP kinase pathway composed of the MAPKKK DLK-1, the MAPKK MKK-4, and the p38 MAPK PMK-3. A mutation of the rpm-1 gene, which encodes an E3 ubiquitin ligase that negatively regulates this pathway to promote synaptogenesis, suppresses only the mec-15 cell-body defect. Thus, MEC-15 acts in parallel with RPM-1, implicating a second protein degradation pathway in TRN development. In addition, all mec-15 phenotypes can be dominantly suppressed by mutations in mec-7, which encodes a beta-tubulin, and dominantly enhanced by mutations in mec-12, which encodes an alpha-tubulin. Since mec-15 phenotypes depend on the relative levels of these tubulins, MEC-15 may target proteins whose function is affected by these levels.

Deciphering the Neural and Molecular Mechanisms of C. elegans Behavior

Because of its small and well-characterized nervous system and amenability to genetic manipulation, the nematode Caenorhabditis elegans offers the promise of understanding the mechanisms underlying a whole animal's behavior at the molecular and cellular levels. In fact, this goal was a primary motivation behind the development of C. elegans as an experimental organism 40 years ago. Yet it has proven surprisingly difficult to obtain a mechanistic understanding of how the C. elegans nervous system generates behavior, despite the existence of a 'wiring diagram' that contains a degree of information about neural connectivity unparalleled in any organism. This review describes three types of information--molecular data on cellular neurochemistry, temporal information about neural activity patterns, and behavioral data on the consequences of neural ablation and manipulation--that, along with genetic analysis, may ultimately lead to a complete functional map of the C. elegans nervous system.

Metazoan mechanotransduction mystery finally solved

In a technical tour de force, whole-cell patch clamp in tiny C. elegans touch receptor neurons in vivo is used to directly record currents in response to mechanical force, providing the first direct evidence that specific proteins are mechanotransducers.

Organizing Synapses

Two articles this week suggest that interactions with extracellular matrix proteins and channels may underlie synaptic organization. Nishimune et al . report that laminin β2, which is concentrated in the basal lamina that extends through the synaptic cleft at the skeletal neuromuscular junction (NMJ), interacted with the voltage-gated calcium channel (VGCC) pore-forming subunits in the presynaptic nerve terminal. VGCC and laminin 9 (a laminin α4,β2,γ1 heterotrimer) coimmunoprecipitated from and could be cross-linked in Torpedo electric organ, a source of concentrated NMJ-like synapses. The interaction was confirmed with the use of cells transfected to express rat VGCC, which bound to laminin 9-coated beads. Beads coated with laminin 9 or the fragment of laminin β2 that bound to VGCC stimulated VGCC clustering of cultured motor neurons. In addition to the clustered VGCC, these were also sites enriched in vesicles and other factors associated with presynaptic differentiation. Examination of mice deficient for β2 laminin ( Lamb2 –/– ) or the Cav2.1 subunit showed decreased NMJ active zones. Emtage et al. examined Caenorhabditis elegans touch receptor neuron organization and touch sensitivity in animals with mutations in genes encoding several extracellular matrix proteins. One of the genes that produced touch-insensitive animals encoded MEC-1, which the authors characterized and determined to be an extracellular matrix protein with multiple epidermal growth factor (EGF) domains and Kunitz domains. MEC-1 and the collagen MEC-5 colocalized with subunits of the degenerin mechanosensory channel complex (MEC-2, MEC-4, and MEC-6) along the touch receptor process. The punctate distribution of the mechanosensory channel complex required MEC-1, because mec-1 null animals had uniform distribution of MEC-4. Furthermore, MEC-1, MEC-4, and MEC-5 positive puncta correspond to positions of attachment of the touch receptor process to the body wall. These extracellular matrix proteins may also play a role in gating of the channel, an idea that requires further analysis. H. Nishimune, J. R. Sanes, S. S. Carlson, A synaptic laminin-calcium channel interaction organizes active zones in motor nerve terminals. Nature 432 , 580-587 (2004). [Online Journal] L. Emtage, G. Gu, E. Hartwieg, M. Chalfie, Extracellular proteins organize the mechanosensory channel complex in C. elegans touch receptor neurons. Neuron 44 , 795-807 (2004). [Online Journal]

The MEC-4 DEG/ENaC channel of Caenorhabditis elegans touch receptor neurons transduces mechanical signals

Transformation of mechanical energy into ionic currents is essential for touch, hearing and nociception. Although DEG/ENaC proteins are believed to form sensory mechanotransduction channels, the evidence for this role remains indirect. By recording from C. elegans touch receptor neurons in vivo, we found that external force evokes rapidly activating mechanoreceptor currents (MRCs) carried mostly by Na(+) and blocked by amiloride-characteristics consistent with direct mechanical gating of a DEG/ENaC channel. Like mammalian Pacinian corpuscles, these neurons depolarized with both positive and negative changes in external force but not with sustained force. Null mutations in the DEG/ENaC gene mec-4 and in the accessory ion channel subunit genes mec-2 and mec-6 eliminated MRCs. In contrast, the genetic elimination of touch neuron-specific microtubules reduced, but did not abolish, MRCs. Our findings link the application of external force to the activation of a molecularly defined metazoan sensory transduction channel.

Extracellular Proteins Organize the Mechanosensory Channel Complex in C. elegans Touch Receptor Neurons

Specialized extracellular matrix (ECM) is associated with virtually every mechanosensory system studied. C. elegans touch receptor neurons have specialized ECM and attach to the surrounding epidermis. The mec-1 gene encodes an ECM protein with multiple EGF and Kunitz domains. MEC-1 is needed for the accumulation of the collagen MEC-5 and other ECM components, attachment, and, separately, for touch sensitivity. MEC-1 and MEC-5 bind to touch processes uniformly and in puncta. These puncta colocalize with and localize the mechanosensory channel complex in the touch neurons. In turn, the production of the MEC-1 and MEC-5 puncta appears to rely on interactions with the neighboring epidermal tissue. These and other observations lead us to propose that extracellular, but not cytoskeletal, tethering of the degenerin channel is needed for mechanosensory transduction. Additionally, our experiments demonstrate an important role of the ECM in organizing the placement of the channel complex.

MEC-2 Is Recruited to the Putative Mechanosensory Complex in C. elegans Touch Receptor Neurons through Its Stomatin-like Domain

The response to gentle body touch in C. elegans requires a degenerin channel complex containing four proteins (MEC-2, MEC-4, MEC-6, and MEC-10). The central portion of the integral membrane protein MEC-2 contains a stomatin-like region that is highly conserved from bacteria to mammals. The molecular function of this domain in MEC-2, however, is unknown. Here, we show that MEC-2 colocalizes with the degenerin MEC-4 in regular puncta along touch receptor neuron processes. This punctate localization requires the other channel complex proteins. The stomatin-like region of MEC-2 interacts with the intracellular cytoplasmic portion of MEC-4. Missense mutations in this region that destroy the interaction also disrupt the punctate localization and degenerin-regulating function of MEC-2. Missense mutations outside this region apparently have no effect on the punctate localization but significantly reduce the regulatory effect of MEC-2 on the MEC-4 degenerin channel. A second stomatin-like protein, UNC-24, colocalizes with MEC-2 in vivo and coimmunoprecipitates with MEC-2 and MEC-4 in Xenopus oocytes; unc-24 enhances the touch insensitivity of temperature-sensitive alleles of mec-4 and mec-6. Two stomatin homologs, MEC-2 and UNC-24, interact with the MEC-4 degenerin through their stomatin-like regions, which act as protein binding domains. At least in the case of MEC-2, this binding allows its nonstomatin domains to regulate channel activity. Stomatin-like regions in other proteins may serve a similar protein binding function.

Identification of genes expressed in C. elegans touch receptor neurons.

The extent of gene regulation in cell differentiation is poorly understood. We previously used saturation mutagenesis to identify 18 genes that are needed for the development and function of a single type of sensory neuron--the touch receptor neuron for gentle touch in Caenorhabditis elegans. One of these genes, mec-3, encodes a transcription factor that controls touch receptor differentiation. By culturing and isolating wild-type and mec-3 mutant cells from embryos and applying their amplified RNA to DNA microarrays, here we have identified genes that are known to be expressed in touch receptors, a previously uncloned gene (mec-17) that is needed for maintaining touch receptor differentiation, and more than 50 previously unknown mec-3-dependent genes. These genes are randomly distributed in the genome and under-represented both for genes that are co-expressed in operons and for multiple members of gene families. Using regions 5' of the start codon of the first 20 genes, we have also identified an over-represented heptanucleotide, AATGCAT, that is needed for the expression of touch receptor genes.

Local responses in Pacinian corpuscles.

ArticleLocal Responses in Pacinian CorpusclesR. Alvarez-Buylla, and J. Ramirez de ArellanoR. Alvarez-BuyllaFrom the Department of Physiology, Instituto N. de Cardiologia, México, Distrito Federal, and J. Ramirez de ArellanoFrom the Department of Physiology, Instituto N. de Cardiologia, México, Distrito FederalPublished Online:31 Dec 1952https://doi.org/10.1152/ajplegacy.1952.172.1.237MoreSectionsPDF (914 KB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInWeChat Previous Back to Top Next Download PDF FiguresReferencesRelatedInformation Cited ByThe mechanosensory neurons of touch and their mechanisms of activation26 July 2021 | Nature Reviews Neuroscience, Vol. 22, No. 9The Form and Function of PIEZO2Annual Review of Biochemistry, Vol. 90, No. 1Computational Model of a Pacinian Corpuscle for Hybrid-Stimuli: Spike-Rate and Threshold Characteristics12 May 2021Sensation, mechanoreceptor, and nerve fiber function after nerve regeneration7 December 2017 | Annals of Neurology, Vol. 82, No. 6Mechanosensory Transduction: Focus on Ion Channels ☆Insight into DEG/ENaC Channel Gating from Genetics and StructureAmy L. Eastwood, and Miriam B. Goodman1 October 2012 | Physiology, Vol. 27, No. 5How We Feel: Ion Channel Partnerships that Detect Mechanical Inputs and Give Rise to Touch and Pain PerceptionNeuron, Vol. 74, No. 4Perceived timing of vestibular stimulation relative to touch, light and sound8 April 2009 | Experimental Brain Research, Vol. 198, No. 2-3Observations on the Neurohistology of Cutaneous Blood Vessels27 May 2008Initiation of Impulses by Mechanosensory Nerve Terminals27 May 2008The MEC-4 DEG/ENaC channel of Caenorhabditis elegans touch receptor neurons transduces mechanical signals5 December 2004 | Nature Neuroscience, Vol. 8, No. 1Representation of Multiple Kinematic Parameters of the Cat Hindlimb in Spinocerebellar ActivityG. Bosco, and R. E. Poppele1 September 1997 | Journal of Neurophysiology, Vol. 78, No. 3Compound sensory action potentials evoked by tactile and by electrical stimulation in normal median and sural nervesMuscle & Nerve, Vol. 17, No. 7The structure and function of pacinian corpuscles: A reviewProgress in Neurobiology, Vol. 42, No. 1Dynamic and static hysteresis in crayfish stretch receptorsBiological Cybernetics, Vol. 52, No. 5A micro-electrode study of peripheral neuropathy in manJournal of the Neurological Sciences, Vol. 34, No. 2The Pacinian CorpuscleAn ultrastructural study of the inner core of the Pacinian corpuscleJournal of Neurocytology, Vol. 2, No. 2Cutaneous Mechanoreceptors and NociceptorsCardiovascular ReceptorsRATE SENSITIVITY OF A BIOLOGICAL TRANSDUCERAnnals of the New York Academy of Sciences, Vol. 156, No. 2 Rein Control,Properties of reptilian cutaneous mechanoreceptorsExperimental Neurology, Vol. 20, No. 3Sense organs - transducers of the environment5 August 2002 | Reports on Progress in Physics, Vol. 30, No. 2Bibliography on muscle receptors; Their morphology, pathology and physiologyExperimental Neurology, Vol. 18ReferencesThe discharge from vibration-sensitive receptors in the monkey footExperimental Neurology, Vol. 15, No. 4Excitation processes in a receptor membraneActa Neurovegetativa, Vol. 24, No. 1-4Physiologie der HautsinneEXCITATION AND INACTIVATION IN A RECEPTOR MEMBRANE*15 December 2006 | Annals of the New York Academy of Sciences, Vol. 94, No. 2Toward Cutaneous Electro-Pulse Communication2 July 2010 | The Journal of Psychology, Vol. 52, No. 1Initiation of spike potentials in contact chemosensory hairs of insects. III. D.C. stimulation and generator potential of labellar chemoreceptor of calliphoraJournal of Cellular and Comparative Physiology, Vol. 54, No. 2THE GENERATION OF ELECTRIC ACTIVITY IN A NERVE ENDING*15 December 2006 | Annals of the New York Academy of Sciences, Vol. 81, No. 2Mechanical into Electrical Energy in Certain MechanoreceptorsProgress in Biophysics and Biophysical Chemistry, Vol. 9REFERENCESActa Physiologica Scandinavica, Vol. 44Generation and Propagation of Impulses during Refractoriness in a Pacinian CorpuscleNature, Vol. 181, No. 4602 More from this issue > Volume 172Issue 1December 1952Pages 237-244 Copyright & PermissionsCopyright © 1952 by American Physiological Societyhttps://doi.org/10.1152/ajplegacy.1952.172.1.237History Received 20 August 1952 Published online 31 December 1952 Published in print 31 December 1952 Metrics