Abstract
There is evidence in experimental animals that deep and superficial pain exert differential effects on cutaneous sympathetic activity. Skin sympathetic nerve activity (SSNA) was recorded from the common peroneal nerve of awake human subjects and injections of 0.5 ml hypertonic saline was made into the tibialis anterior muscle (causing a deep, dull ache) or 0.2 ml into the overlying skin (causing a sharp burning pain) at unexpected times. Both deep and superficial pain caused increases in SSNA immediately on injection and preceding the onset of pain for both muscle and skin pain (10.1 ± 2.4 vs. 15.3 ± 5.3 s; muscle versus skin, respectively). SSNA increases were short lasting (104.2 ± 13.4 vs. 81.8 ± 11.7 s; muscle versus skin pain) and did not follow muscle and skin pain profiles. Sweat release occurred following both intramuscular and subcutaneous injections of hypertonic saline. While muscle or skin pain invariably caused changes in skin blood flow as well as increases in sweat release, skin blood flow increased in females and decreased in males. We conclude that both acute muscle and skin pain cause an increase in SSNA, sweat release and gender-dependent changes in skin blood flow.
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References
Berkley KJ (1997) Sex differences in pain. Behav Brain Sci 20:371–380
Burton AR, Brown R, Macefield VG (2008) Selective activation of muscle and skin nociceptors does not trigger exaggerated sympathetic responses in spinal-injured subjects. Spinal Cord 46:660–665
Burton AR, Birznieks I, Bolton PS et al (2009) Effects of deep and superficial experimentally induced acute pain on muscle sympathetic nerve activity in human subjects. J Physiol 587:183–193
Cankar K, Finderle Ž, Štrucl M (2000) Gender differences in cutaneous laser Doppler flow response to local direct and contralateral cooling. J Vasc Res 37:183–188
Cooke J, Creager M, Osmundson P et al (1990) Sex differences in control of cutaneous blood flow. Circulation 82:1607–1615
Dart AM, Du X, Kingwell BA (2002) Gender, sex hormones and autonomic nervous control of the cardiovascular system. Cardiovasc Res 53:678–687
Depaulis A, Keay KA, Bandler R (1992) Longitudinal neuronal organization of defensive reactions in the midbrain periaqueductal gray region of the rat. Exp Brain Res 90:307–318
Drevets WC, Price JL, Simpson JR et al (1997) Subgenual prefrontal cortex abnormalities in mood disorders. Nature 386:824–827
Drummond PD (2004) Involvement of the sympathetic nervous system in complex regional pain syndrome. Int J Low Extrem Wounds 3:335–342
Henderson LA, Gandevia SC, Macefield VG (2008) Gender differences in brain activity evoked by muscle and cutaneous pain: a retrospective study of single-trial fMRI data. NeuroImage 39:1867–1876
Horeyseck G, Jänig W (1972) Response patterns in vasoconstrictors to the skin and muscles upon stimulation of skin receptors in chronically spinalized cats. Pflugers Arch 332:R64
Horeyseck G, Jänig W (1974) Reflexes in postganglionic fibres within skin and muscle nerves after noxious stimulation of skin. Exp Brain Res 20:125–134
Jänig W, Häbler HJ (2000) Specificity in the organization of the autonomic nervous system: a basis for precise neural regulation of homeostatic and protective body functions. Prog Brain Res 122:351–367
Keay KA, Bandler R (1993) Deep and superficial noxious stimulation increases Fos-like immunoreactivity in different regions of the midbrain periaqueductal grey of the rat. Neurosci Lett 154:23–26
Keay KA, Clement CI, Owler B et al (1994) Convergence of deep somatic and visceral nociceptive information onto a discrete ventrolateral midbrain periaqueductal gray region. Neuroscience 61:727–732
Macefield VG, Wallin BG (1999) Respiratory and cardiac modulation of single sympathetic vasoconstrictor and sudomotor neurones to human skin. J Physiol 516:303–314
Macefield VG, Wallin BG, Vallbo AB (1994) The discharge behaviour of single vasoconstrictor motoneurones in human muscle nerves. J Physiol 481:799–809
Macefield VG, Gandevia SC, Henderson LA (2007) Discrete changes in cortical activation during experimentally induced referred muscle pain: a single-trial fMRI study. Cereb Cortex 17:2050–2059
Mayberg HS, Brannan SK, Mahurin RK et al (1997) Cingulate function in depression: a potential predictor of treatment response. NeuroReport 8:1057–1061
Morrison SF (2001) Differential control of sympathetic outflow. Am J Physiol Regul Integr Comp Physiol 281:R683–R698
Procacci P, Zoppi M, Maresca M (1979) Experimental pain in man. Pain 6:123–140
Shoemaker JK, Hogeman CS, Khan M et al (2001) Gender affects sympathetic and hemodynamic response to postural stress. Am J Physiol Heart Circ Physiol 281:H2028–H2035
Wallin BG (1990) Neural control of human skin blood flow. J Auton Nerv Syst 30:S185–S190
Wong SW, Kimmerly DS, Massé N (2007) Sex differences in forebrain and cardiovagal responses at the onset of isometric handgrip exercise: a retrospective fMRI study. J Appl Physiol 103:1402–1411
Acknowledgment
This work was supported by grant 350889 to V. G. Macefield and L. A. Henderson from the National Health and Medical Research Council of Australia.
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Burton, A.R., Birznieks, I., Spaak, J. et al. Effects of deep and superficial experimentally induced acute pain on skin sympathetic nerve activity in human subjects. Exp Brain Res 195, 317–324 (2009). https://doi.org/10.1007/s00221-009-1790-9
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DOI: https://doi.org/10.1007/s00221-009-1790-9