Ectopic excitability of injured nerves in monkey: entrained responses to vibratory stimuli

Koschorke, G. M.; Meyer, Richard A.; Tillman, D B; Campbell, James N.

doi:10.1152/jn.1991.65.3.693

Cited by 52 publications

(26 citation statements)

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“…Trains of vibration stimuli were applied to identify neurons specifically tuned to this type of stimulus in vivo (17,18): 21 ± 3% of mechanosensitive neurons reliably responded to vibration stimuli (henceforth termed "vibration neurons") ( Fig. 1A′).…”

Section: Resultsmentioning

confidence: 99%

En masse in vitro functional profiling of the axonal mechanosensitivity of sensory neurons

Usoskin

Zilberter²,

Linnarsson³

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

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Perception of the environment relies on somatosensory neurons. Mechanosensory, proprioceptor and many nociceptor subtypes of these neurons have specific mechanosensitivity profiles to adequately differentiate stimulus patterns. Nevertheless, the cellular basis of differential mechanosensation remains largely elusive. Successful transduction of sensory information relies on the recruitment of sensory neurons and mechanosensation occurring at their peripheral axonal endings in vivo. Conspicuously, existing in vitro models aimed to decipher molecular mechanisms of mechanosensation test single sensory neuron somata at any one time. Here, we introduce a compartmental in vitro chamber design to deliver precisely controlled mechanical stimulation of sensory axons with synchronous real-time imaging of Ca 2+ transients in neuronal somata that reliably reflect action potential firing patterns. We report of three previously not characterized types of mechanosensitive neuron subpopulations with distinct intrinsic axonal properties tuned specifically to static indentation or vibration stimuli, showing that different classes of sensory neurons are tuned to specific types of mechanical stimuli. Primary receptor currents of vibration neurons display rapidly adapting conductance reliably detected for every single stimulus during vibration and are consistently converted into action potentials. This result allows for the characterization of two critical steps of mechanosensation in vivo: primary signal detection and signal conversion into specific action potential firing patterns in axons.compartmentalized chamber | dorsal root ganglion | neurite | end-organ | vibration C ontinuous sensing of the surrounding environment is an absolute requirement for any organism to ensure its survival through adaptation. Recently, significant progress has been made in understanding the molecular mechanisms underpinning the perception of temperature and chemical stimuli in both vertebrates and invertebrates (1-3). In contrast, the molecular and cellular requirements for mechanoreception during sensations of touch and pain have yet to be elucidated.The application of mechanical force is believed to activate ion channels in sensory nerve endings, resulting in membrane depolarization and peripheral action potential (AP) generation (4, 5). Nociceptors contain free nerve endings acting as high-threshold mechanotransducers. Vibration, touch, and pressure sensations are mediated by low-threshold myelinated sensory afferents with their unmyelinated terminals located within specialized accessory structures, the sensory end-organs (6). Our ability to discriminate fine modalities of mechanical stimuli is thought to be underlain by multiple subtypes of myelinated sensory neurons, each associated with corresponding sensory end-organs. However, the relative importance of sensory end-organs vs. intrinsic mechanoreceptive properties of neurons themselves remains elusive, largely because of the lack of models to resolve neuronal responses to diverse stimuli in the...

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Section: Resultsmentioning

confidence: 99%

En masse in vitro functional profiling of the axonal mechanosensitivity of sensory neurons

Usoskin

Zilberter²,

Linnarsson³

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

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“…These sensory properties included the development of spontaneous ectopic discharge (Michaelis et al, 1995), axonal sensitivity to a variety of algesic agents such as bradykinin (BK), prostaglandin E2, acidic pH, and capsaicin (Michaelis et al, 1997;Moalem et al, 2005), and the appearance of mechanosensitivity and thermosensitivity along the axon itself at the developing neuroma site (Koschorke et al, 1991;Michaelis et al, 1995Michaelis et al, , 1997Blenk et al, 1996). The common hypothesis explaining these observations is that anterograde axonal transport of sensory transducer molecules such as heatactivated channels or of voltage-gated ion channels causes an accumulation of these membrane proteins at the lesioned site.…”

Section: Introductionmentioning

confidence: 99%

“…The common hypothesis explaining these observations is that anterograde axonal transport of sensory transducer molecules such as heatactivated channels or of voltage-gated ion channels causes an accumulation of these membrane proteins at the lesioned site. Translocation of the receptors and channels to the axonal membrane could provide the regenerating axonal sprouts with the same properties their sensory nerve endings possessed before axotomy (Devor and Govrin-Lippmann, 1983;Guharay and Sachs, 1984;Koschorke et al, 1991Koschorke et al, , 1994Blenk et al, 1996;Michaelis et al, 1999).…”

Section: Introductionmentioning

confidence: 99%

Sensory Transduction in Peripheral Nerve Axons Elicits Ectopic Action Potentials

Hoffmann¹,

Sauer²,

Horch³

et al. 2008

Journal of Neuroscience

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Sensory properties of unmyelinated axons in the isolated rat sciatic nerve have been revealed previously by measuring stimulated neuropeptide release in response to noxious stimuli. In addition, axonal sensitization by inflammatory mediators has been demonstrated and shown to depend on the heat-and proton-activated ion channel transient receptor potential vanilloid receptor-1. It was unclear whether this responsiveness is accompanied by ectopic generation of action potentials, which may play a crucial role in painful neuropathies. We explored this hypothesis using the isolated mouse skin-nerve preparation. This method enabled us to directly compare the sensory properties of axons in the peripheral nerve with their characterized cutaneous terminals in the receptive field using propagated action potentials as an index of axonal activation. Single-fiber recordings from 51 mechanosensitive mouse C-fibers revealed that a majority of the polymodal nociceptors responded with an encoding discharge rate to graded heating of the cutaneous receptive field (n ϭ 38) as well as of the saphenous nerve carrying the fiber under investigation (n ϭ 25; 66%). Axonal heat responses paralleled those of the receptive fields with regard to thresholds and discharge rates (41.5 Ϯ 4.3°C; 7.7 Ϯ 9.6 spikes in a 20 s 32-48°C ranged stimulation). In contrast, axonal mechanosensitivity was poor and noxious cold sensitivity more rarely encountered. In conclusion, peripheral nerve axons exhibit sensory transduction capacities similar to their nociceptive terminals in the skin with respect to noxious heat, although not to mechanical and cold sensitivity. This may become a source of ectopic discharge and pain if axonal heat threshold drops to body temperature, as may be the case during inflammation-like processes in peripheral nerves.

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“…In other words, the adaptation to a prolonged suprathreshold stimulus appeared to be an intrinsic property of the neurones and not a function of the nerve ending-tissue interaction. Also supporting this concept is the observation that a neuroma created by nerve crush experiments, therefore removed from the environment it normally innervates, maintains its activation-response characteristics to mechanical stimulation (Koschorke et al 1991). In contrast in the airways, experiments using antidromic electrical stimulation have led to the suggestion that the adaptation of sensory nerves to mechanical stimulation is not a function of the neurone per se, but a function of visco-elastic elements within the airway wall (Davenport et al 1981).…”

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confidence: 99%

Adaptation of guinea‐pig vagal airway afferent neurones to mechanical stimulation

McAlexander

Myers

Undem

1999

The Journal of Physiology

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The sensory nerve fibres supplying the guinea-pig trachea and main-stem bronchi are mainly vagal fibres with somata located within the nodose and jugular ganglia (Kummer et al. 1992;Riccio et al. 1996b). While subpopulations of these nerve endings can be excited by chemical and non-isoosmotic stimuli, the majority of them respond to mechanical stimuli (Riccio et al. 1996a;Pedersen et al. 1998). Of the fibres that respond to a von Frey fibre mechanical stimulus, there are both low threshold and high threshold mechanoreceptors. Previous studies from our laboratory have shown that the low threshold mechanoreceptors originate from somata within the nodose ganglion and the high threshold mechanoreceptors originate from somata within the jugular ganglion (Riccio et al. 1996a). Two types of mechanoreceptors have been characterized based on their response pattern to the mechanical forces imposed upon lung inflation, namely slowly adapting receptors (SARs) and rapidly adapting receptors (RARs).RARs, which discharge during lung inflation and then become refractory during maintained inflation, were first discovered in the airways by Knowlton & Larrabee (1946). Later, Widdicombe (1954) described RARs as irritant receptors that were largely located in the conducting airways and SARs as stretch receptors located primarily within the lung. Although this dichotomy has been established for some time, relatively little is known regarding the mechanism of adaptation to mechanical stimuli. A central question regarding the adaptation of sensory nerves to mechanical stimulation is whether the electrophysiological properties of the neurone per se can support the adaptive response, or whether the adaptation is secondary to the manner in which the nerve ending interacts with the airway tissue. Harper (1991) observed that the adaptation of somata within the dorsal root ganglia to prolonged suprathreshold depolarizing current steps mimicked the adaptation of the nerve endings arising from these somata to

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Ectopic excitability of injured nerves in monkey: entrained responses to vibratory stimuli

Cited by 52 publications

References 0 publications

En masse in vitro functional profiling of the axonal mechanosensitivity of sensory neurons

En masse in vitro functional profiling of the axonal mechanosensitivity of sensory neurons

Sensory Transduction in Peripheral Nerve Axons Elicits Ectopic Action Potentials

Adaptation of guinea‐pig vagal airway afferent neurones to mechanical stimulation

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