Sympathetic Responses to Noxious Stimulation of Muscle and Skin

Burton, Amy L.; Fazalbhoy, Azharuddin; Macefield, Vaughan G.

doi:10.3389/fneur.2016.00109

Cited by 63 publications

(48 citation statements)

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“…That is, cutaneous pain elicits fight/flight behaviors, coupled with increases in heart rate, blood pressure and sympathetic vasoconstrictor drive, whereas muscle and visceral pain bring about quiescence and decreases in heart rate, blood pressure and vasoconstrictor drive . Although some clinical observations in humans suggested similar divergent responses [Lewis, 1942;Feinstein et al, 1954], we found that acute cutaneous or muscle pain, induced by bolus subcutaneous or intramuscular injection of hypertonic saline, both evoked transient (30 s) increases in skin sympathetic nerve activity (SSNA) and heart rate, with small sustained increases in blood pressure and muscle sympathetic nerve activity (MSNA) that matched the duration of pain [Burton et al, 2009a,b;Hall et al, 2012; for review see Burton et al, 2016]. These data demonstrate that, in humans, differential sympathetic responses to acute cutaneous and muscle pain do not occur.…”

Section: Introductionmentioning

confidence: 74%

“…We recently found that prolonged muscle pain, induced by intramuscular infusion of hypertonic saline, is accompanied by two patterns of change in MSNA, with subjects showing either a sustained increase or a sustained decrease in MSNA [Fazalbhoy et al, , 2014Kobuch et al, 2015Kobuch et al, , 2016 for review see Burton et al, 2016]. These divergent patterns of MSNA are reproducible over time [Fazalbhoy et al, 2014], and not based on sex, or differences in resting MSNA, blood pressure, or heart rate [Kobuch et al, 2015].…”

Section: Introductionmentioning

confidence: 99%

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Central circuitry responsible for the divergent sympathetic responses to tonic muscle pain in humans

et al. 2016

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Experimentally induced tonic muscle pain evokes divergent muscle vasoconstrictor responses, with some individuals exhibiting a sustained increase in muscle sympathetic nerve activity (MSNA), and others a sustained decrease. These patterns cannot be predicted from an individual's baseline physiological or psychological measures. The aim of this study was to investigate whether the different muscle sympathetic responses to tonic muscle pain were associated with differential changes in regional brain activity. Functional magnetic resonance imaging (fMRI) of the brain was performed concurrently with microelectrode recording of MSNA from the peroneal nerve during a 40-min infusion of hypertonic saline into the ipsilateral tibialis anterior muscle. MSNA increased in 26 and decreased in 11 of 37 subjects during tonic muscle pain. Within the prefrontal and cingulate cortices, precuneus, nucleus accumbens, caudate nucleus, and dorsomedial hypothalamus, blood oxygen level dependent (BOLD) signal intensity increased in the increasing-MSNA group and remained at baseline or decreased in the decreasing-MSNA group. Similar responses occurred in the dorsolateral pons and in the region of the rostral ventrolateral medulla. By contrast, within the region of the dorsolateral periaqueductal gray (dlPAG) signal intensity initially increased in both groups but returned to baseline levels only in the increasing-MSNA group. These results suggest that the divergent sympathetic responses to muscle pain result from activation of a neural pathway that includes the dlPAG, an area thought to be responsible for the behavioral and cardiovascular responses to psychological rather than physical stressors. Hum Brain Mapp 38:869-881, 2017. © 2016 Wiley Periodicals, Inc.

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Section: Introductionmentioning

confidence: 74%

Section: Introductionmentioning

confidence: 99%

Central circuitry responsible for the divergent sympathetic responses to tonic muscle pain in humans

et al. 2016

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“…; Person, ; Burton et al . ). Moreover, a mechanical stimulus to tissues such as the skin and skeletal muscle evokes sympathoexcitation, no matter whether the stimulation is noxious or not (e.g.…”

Section: Introductionmentioning

confidence: 97%

“…; Burton et al . ). Recent studies have demonstrated that insulin activates some ion channels reported as molecular candidates for mechanosensitive receptors in the peripheral terminals of primary sensory neurons for which the cell bodies are in the dorsal root ganglion (DRG) (Uchida & Tominaga, ; Colsoul et al .…”

Section: Introductionmentioning

confidence: 97%

Insulin potentiates the response to mechanical stimuli in small dorsal root ganglion neurons and thin fibre muscle afferents in vitro

Hotta

Katanosaka

Mizumura

et al. 2019

The Journal of Physiology

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Key points Insulin is known to activate the sympathetic nervous system centrally. A mechanical stimulus to tissues activates the sympathetic nervous system via thin fibre afferents. Evidence suggests that insulin modulates putative mechanosensitive channels in the dorsal root ganglion neurons of these afferents. In the present study, we report the novel finding that insulin augments the mechanical responsiveness of thin fibre afferents not only at dorsal root ganglion, but also at muscle tissue levels. Our data suggest that sympathoexcitation is mediated via the insulin‐induced mechanical sensitization peripherally. The present study proposes a novel physiological role of insulin in the regulation of mechanical sensitivity in somatosensory thin fibre afferents. Abstract Insulin activates the sympathetic nervous system, although the mechanism underlying insulin‐induced sympathoexcitation remains to be determined. A mechanical stimulus to tissues such as skin and/or skeletal muscle, no matter whether the stimulation is noxious or not, activates the sympathetic nervous system via thin fibre afferents. Evidence suggests that insulin modulates putative mechanosensitive channels in the dorsal root ganglion (DRG) neurons of these afferents. Accordingly, we investigated whether insulin augments whole‐cell current responses to mechanical stimuli in small DRG neurons of normal healthy mice. We performed whole‐cell patch clamp recordings using cultured DRG neurons and observed mechanically‐activated (MA) currents induced by mechanical stimuli applied to the cell surface. Local application of vehicle solution did not change MA currents or mechanical threshold in cultured DRG neurons. Insulin (500 mU mL−1) significantly augmented the amplitude of MA currents (P < 0.05) and decreased the mechanical threshold (P < 0.05). Importantly, pretreatment with the insulin receptor antagonist, GSK1838705, significantly suppressed the insulin‐induced potentiation of the mechanical response. We further examined the impact of insulin on thin fibre muscle afferent activity in response to mechanical stimuli in normal healthy rats in vitro. Using a muscle–nerve preparation, we recorded single group IV fibre activity to a ramp‐shaped mechanical stimulation. Insulin significantly decreased mechanical threshold (P < 0.05), although it did not significantly increase the response magnitude to the mechanical stimulus. In conclusion, these data suggest that insulin augments the mechanical responsiveness of small DRG neurons and potentially sensitizes group IV afferents to mechanical stimuli at the muscle tissue level, possibly contributing to insulin‐induced sympathoexcitation.

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“…Clear evidence exists that stimulation of high threshold skin mechanoreceptors sensitive to noxious stimuli can influence heart rate, blood pressure, and efferent sympathetic outflow to skeletal muscle (Burton et al, 2016). Although pain and touch are known to be intricately related (Abraira and Ginty, 2013), the relationship between low threshold cutaneous mechanoreceptor afferent feedback and reflex efferent sympathetic (or parasympathetic) activity is not well-studied.…”

Section: Introductionmentioning

confidence: 99%

Cutaneous Mechanoreceptor Feedback from the Hand and Foot Can Modulate Muscle Sympathetic Nerve Activity

et al. 2016

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Stimulation of high threshold mechanical nociceptors on the skin can modulate efferent sympathetic outflow. Whether low threshold mechanoreceptors from glabrous skin are similarly capable of modulating autonomic outflow is unclear. Therefore, the purpose of this study was to examine the effects of cutaneous afferent feedback from the hand palm and foot sole on efferent muscle sympathetic nerve activity (MSNA). Fifteen healthy young participants (9 male; 25 ± 3 years [range: 22–29]) underwent microneurographic recording of multi-unit MSNA from the right fibular nerve during 2 min of baseline and 2 min of mechanical vibration (150 Hz, 220 μm peak-to-peak) applied to the left hand or foot. Each participant completed three trials of both hand and foot stimulation, each separated by 5 min. MSNA burst frequency decreased similarly during the 2 min of both hand (20.8 ± 8.9 vs. 19.3 ± 8.6 bursts/minute [Δ −8%], p = 0.035) and foot (21.0 ± 8.3 vs. 19.5 ± 8.3 bursts/minute [Δ −8%], p = 0.048) vibration but did not alter normalized mean burst amplitude or area (All p > 0.05). Larger reductions in burst frequency were observed during the first 10 s (onset) of both hand (20.8 ± 8.9 vs. 17.0 ± 10.4 [Δ −25%], p < 0.001) and foot (21.0 ± 8.3 vs. 18.3 ± 9.4 [Δ −16%], p = 0.035) vibration, in parallel with decreases in normalized mean burst amplitude (hand: 0.45 ± 0.06 vs. 0.36 ± 0.14% [Δ −19%], p = 0.03; foot: 0.47 ± 0.07 vs. 0.34 ± 0.19% [Δ −27%], p = 0.02) and normalized mean burst area (hand: 0.42 ± 0.05 vs. 0.32 ± 0.12% [Δ −25%], p = 0.003; foot: 0.47 ± 0.05 vs. 0.34 ± 0.16% [Δ −28%], p = 0.01). These results demonstrate that tactile feedback from the hands and feet can influence efferent sympathetic outflow to skeletal muscle.

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Sympathetic Responses to Noxious Stimulation of Muscle and Skin

Cited by 63 publications

References 65 publications

Central circuitry responsible for the divergent sympathetic responses to tonic muscle pain in humans

Central circuitry responsible for the divergent sympathetic responses to tonic muscle pain in humans

Insulin potentiates the response to mechanical stimuli in small dorsal root ganglion neurons and thin fibre muscle afferents in vitro

Cutaneous Mechanoreceptor Feedback from the Hand and Foot Can Modulate Muscle Sympathetic Nerve Activity

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