Convergence of cutaneous and pelvic visceral nociceptive inputs onto primate spinothalamic neurons

R. J. Milne, R. D. Foreman, G. J. Giesler, W. D. Willis

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146 Scopus citations

Abstract

The responses of 66 primate spinothalamic neurons to natural stimulation of the urinary bladder and testicle were studied with extracellular recording techniques in order to elucidate the neural basis for referral of visceral pain. Thirty-eight out of 53 cells located at the thoraco-lumbar junction or in sacral segments responded to noxious cutaneous stimuli, and 84% of these also exhibited phasic and/or tonic excitatory responses to distension of the urinary bladder. Seventeen out of 20 of these units, all located at the thoraco-lumbar junction, were excited by compression of the ipsilateral testicle. The response was graded with the compressive force. Excitatory responses to noxious heat and an irritant chemical (KCl) applied to the exposed testicular surface were also observed. Twelve sacral units having inputs from deep receptors of the tail exhibited mixed excitatory and inhibitory responses to bladder distension. A further 2 cells located at the thoracolumbar junction responded only to cutaneous tactile stimuli, and 13 cells located at the lumbosacral enlargement were tonically inhibited by bladder distension. It is concluded that spinothalamic neurons that convey nociceptive input from the skin may also respond to noxious visceral stimuli. Such viscerosomatic convergence provides a neural substrate for the phenomenon of cutaneous referral of visceral pain.

Original languageEnglish (US)
Pages (from-to)163-183
Number of pages21
JournalPain
Volume11
Issue number2
DOIs
StatePublished - Oct 1981

Bibliographical note

Funding Information:
CONVERGENCE OF CUTANEOUS AND PELVIC VISCERAL NOCICEPTIVE INPUTS ONTO PRIMATE SPINOTHALAMIC NEURONS. R.J. Milne .I , R.D. Foreman*, G.J. Giesler, Jr. I . and W.D. ~ 3 , iMarine Biomed. Inst., Depts. of ~Anatomy and of 3physiology & Biophysics, Univ. of Texas Med. Branch, Galveston, TX 77550, USA A_im of Investisation: Referral of pain is a consistent feature of visceral pathology, and the primate spinothalamic tract has been implicated in cutaneous and visceral nocieeption. We have recorded the responses of individual spinothalamie neurons to cutaneous and visceral noxious stimuli, to determine whether viseerosomatie convergence, a possible mechanism for pain referral, occurs in spinothalamic neurons. Methods: Extracellular recordings were made from 66 spinothalamic neurons in segments caudal to TII in anesthetized monkeys (Mac aca fasci-cularis). Cells were classified as wide dynamic range (W-DR), high threshold (HT), low threshold (LT) or 'deep', according to their responses to somatic stimuli. The responses to graded distension of the urinary bladder and/or compression of the ipsilateral testicle were studied. Results: Of 53 units located at the thoraco-lumbar junction or in sacral segments, 84% of 38 HT and W-DR cells, and 4 out of 13 'deep' cells responded to bladder distension with transient and/or maintained excitation. Two LT cells were not excited. Seventeen out of 20 W\])Ra nd HT neurons located in segments TI2 to L2 were excited by compression of the testicle. Thirteen lumbosacral units were inhibited by bladder distension. Conclusion: Spinothalamic neurons that convey nociceptive input from the skin may also respond to noxious visceral stimuli. Such viscerosomatic convergence may provide a neural substrate for the phenomenon of referred pelvic visceral pain. This work was supported, in part, by NIH grants NS09743, NSI1255 and by The Moody Foundation.

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