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Inhibition of the responses of cat dorsal horn neurons to noxious skin heating by stimulation in medial or lateral medullary reticular formation

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Summary

Responses of single lumbar dorsal horn units to noxious radiant heating (50° C, 10 s) of glabrous footpad skin were recorded in cats anesthetized with sodium pentobarbital and 70% nitrous oxide. The heat-evoked responses of 37/40 units were reduced during electrical stimulation (100 ms trains, 100 Hz, 3/s, 25–600 μA) in the medullary nucleus raphe magnus (NRM) and/or in laterally adjacent regions of the medullary reticular formation (MRF). Inhibition was elicited by stimulation in widespread areas of the medulla, but with greatest efficacy at ventrolateral sites. The magnitude of inhibition increased with graded increases in medullary stimulation intensity. Mean current intensities at threshold for inhibition or to produce 50% inhibition were higher for NRM than for MRF sites. Units’ responses to graded noxious heat stimuli increased linearly from threshold (42–43° C) to 52° C. During NRM (5 units) or ipsilateral MRF stimulation (7 units), responses were inhibited such that the mean temperature-response functions were shifted toward higher temperatures with increased thresholds (1.5° and 1° C, respectively) and reduced slopes (to 60% of control). Contralateral MRF stimulation had a similar effect in 4 units. Inhibitory effects of NRM and MRF stimulation were reduced (by >25%) or abolished in 4/6 and 5/12 units, respectively, following systemic administration of the serotonin antagonist methysergide. Inhibitory effects from NRM, ipsi- and contralateral MRF were reduced or abolished in 2/9, 4/8 and 6/9 cases, respectively, following systemic administration of the noradrenergic antagonist phentolamine. These results confirm and extend previous studies of medullospinal inhibition and the role of monoamines, and are discussed in terms of analgesic mechanisms.

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References

  • Azami J, Llewlyn MB, Roberts MHT (1982) The contribution of nucleus reticularis paragigantocellularis and nucleus raphe magnus to the analgesia produced by systemically administered morphine, investigated with the microinjection technique. Pain 12: 229–246

    Article  CAS  PubMed  Google Scholar 

  • Barbaro NM, Hammond DL, Fields HL (1985) Effects of intrathecally administered methysergide and yohimbine on microstimulation-produced antinociception in the rat. Brain Res 343: 223–229

    Article  CAS  PubMed  Google Scholar 

  • Basbaum AI, Clanton CH, Fields HL (1978) Three bulbospinal pathways from the rostral medulla of the cat: an autoradiographic study of pain modulating systems. J Comp Neurol 178: 209–224

    Article  CAS  PubMed  Google Scholar 

  • Basbaum AI, Fields HL (1984) Endogenous pain control systems: brainstem-spinal pathways and endorphin circuitry. Ann Rev Neurosci 7: 309–338

    Article  CAS  PubMed  Google Scholar 

  • Basbaum AI, Fields HL (1979) The origin of descending pathways in the dorsolateral funiculus of the spinal cord of the cat and rat: further studies on the anatomy of pain modulation. J Comp Neurol 187: 513–532

    Article  CAS  PubMed  Google Scholar 

  • Basbaum AI, Moss MS, Glazer EJ (1983) Opiate and stimulation produced analgesia: the contribution of the monoamines. Adv Pain Res Therap 5: 323–329

    CAS  Google Scholar 

  • Beck PW, Handwerker HO, Zimmermann M (1974) Nervous outflow from the cat’s foot during noxious radiant heat stimulation. Brain Res 67: 373–386

    Article  CAS  PubMed  Google Scholar 

  • Belcher G, Ryall RW, Schaffner R (1978) The differential effects of 5-hydroxytryptamine, noradrenaline and raphe stimulation on nociceptive and nonnociceptive dorsal horn interneurones in the cat. Brain Res 151: 307–321

    Article  CAS  PubMed  Google Scholar 

  • Berman AL (1968) The brainstem of the cat. University of Wisconsin Press, Madison

    Google Scholar 

  • Besson JM, Chaouch A (1987) Peripheral and spinal mechanisms of nociception. Physiol Rev 67: 67–186

    CAS  PubMed  Google Scholar 

  • Bowker RM, Steinbusch HWM, Coulter JD (1981a) Serotonergic and peptidergic projections to the spinal cord demonstrated by a combined retrograde HRP histochemical and immunocytochemical staining method. Brain Res 211: 412–417

    Article  CAS  PubMed  Google Scholar 

  • Bowker RM, Westlund KN, Coulter JD (1981b) Origins of serotonergic projections to the spinal cord in rat: an immunocytochemical-retrograde transport study. Brain Res 226: 187–199

    Article  CAS  PubMed  Google Scholar 

  • Bowker RM, Westlund KN, Coulter JD (1982) Origins of serotonergic projections to the lumbar spinal cord in the monkey using a combined retrograde transport and immunocytochemical technique. Brain Res Bull 9: 271–278

    Article  CAS  PubMed  Google Scholar 

  • Brown AG, Rethelyi M (1981) Spinal cord sensation. Scottish Acad Press Edinburgh, pp 331–333

    Google Scholar 

  • Carstens E, Fraunhoffer M, Zimmermann M (1981) Serotonergic mediation of descending inhibition from midbrain periaqueductal gray, but not reticular formation, of spinal nociceptive transmission in the cat. Pain 10: 149–167

    Article  CAS  PubMed  Google Scholar 

  • Carstens E, Klumpp D, Zimmermann M (1980) Differential inhibitory effects of medial and lateral midbrain stimulation on spinal neuronal discharges to noxious skin heating in the cat. J Neurophysiol 43: 332–342

    CAS  PubMed  Google Scholar 

  • Dickenson AH, Hellon RF, Woolf CJ (1981) Tooth pulp input to the spinal trigeminal nucleus: a comparison of inhibitions following segmental and raphe magnus stimulation. Brain Res 214: 73–87

    Article  CAS  PubMed  Google Scholar 

  • Dubner R, Bennett GJ (1983) Spinal and trigeminal mechanisms of nociception. Ann Rev Neurosci 6: 381–418

    Article  CAS  PubMed  Google Scholar 

  • Duggan AW, Griersmith BT (1979) Inhibition of the spinal transmission of nociceptive information by supraspinal stimulation in the cat. Pain 6: 149–161

    Article  CAS  PubMed  Google Scholar 

  • Edeson RO, Ryall RW (1983) Systematic mapping of descending inhibitory control by the medulla of nociceptive spinal neurons in cats. Brain Res 271: 251–262

    Article  CAS  PubMed  Google Scholar 

  • Engberg I, Lundberg A, Ryall RW (1968) Reticulospinal inhibition of transmission in reflex pathways. J Physiol 194: 201–223

    CAS  PubMed  Google Scholar 

  • Fields HL, Basbaum AI, Clanton CH, Anderson SD (1977) Nucleus raphe magnus inhibition of spinal cord dorsal horn neurons. Brain Res 126: 441–453

    Article  CAS  PubMed  Google Scholar 

  • Fleischer E, Handwerker HO, Joukhadar S (1983) Unmyelinated nociceptive units in two skin areas of the rat. Brain Res 267: 81–92

    Article  CAS  PubMed  Google Scholar 

  • Gebhart GF, Ossipov MH (1986) Characterization of inhibition of the spinal nociceptive tail-flick reflex in the rat from the medullary lateral reticular nucleus. J Neurosci 6: 701–713

    CAS  PubMed  Google Scholar 

  • Gebhart GF, Sandkuhler J, Thalhammer JG, Zimmermann M (1983a) Quantitative comparison of inhibition in spinal cord of nociceptive information by stimulation in periaqueductal gray or nucleus raphe magnus of the cat. J Neurophysiol 50: 1433–1445

    CAS  PubMed  Google Scholar 

  • Gebhart GF, Sandkuhler J, Thalhammer JG, Zimmermann M (1983b) Inhibition of spinal nociceptive information by stimulation in midbrain of the cat is blocked by lidocaine microinjected in nucleus raphe magnus and medullary reticular formation. J Neurophysiol 50: 1446–1459

    CAS  PubMed  Google Scholar 

  • Gerhart KD, Wilcox TK, Chung JM, Willis WD (1981) Inhibition of nociceptive and nonnociceptive responses of primate spinothalamic tract neurons by stimulation in medial brain stem. J Neurophysiol 45: 121–136

    CAS  PubMed  Google Scholar 

  • Giesler GJ, Gerhart KD, Yezierski RP, Wilcox TK, Willis WD (1981) Postsynaptic inhibition of primate spinothalamic neurons by stimulation in nucleus raphe magnus. Brain Res 204: 184–188

    Article  PubMed  Google Scholar 

  • Gray BG, Dostrovsky JO (1983) Descending inhibitory influences from periaqueductal gray, nucleus raphe magnus, and adjacent reticular formation. I. Effects on lumbar spinal cord nociceptive and nonnociceptive neurons. J Neurophysiol 49: 932–947

    CAS  PubMed  Google Scholar 

  • Gray BG, Dostrovsky JO (1985) Inhibition of feline spinal cord dorsal horn neurons following electrical stimulation of nucleus paragigantocellularis lateralis. A comparison with nucleus raphe magnus. Brain Res 348: 261–273

    Article  CAS  PubMed  Google Scholar 

  • Gregor M, Zimmermann M (1972) Characteristics of spinal neurones responding to cutaneous myelinated and unmyelinated fibres. J Physiol 221: 555–576

    CAS  PubMed  Google Scholar 

  • Griersmith BT, Duggan AW (1980) Prolonged depression of spinal transmission of nociceptive information by 5-HT administered in the substantia gelatinosa: antagonism by methysergide. Brain Res 187: 231–236

    Article  CAS  PubMed  Google Scholar 

  • Griersmith BT, Duggan AW, North RA (1981) Methysergide and supraspinal inhibition of the spinal transmission of nociceptive information in the anesthetized cat. Brain Res 204: 147–158

    Article  CAS  PubMed  Google Scholar 

  • Griffith JL, Gatipon GB (1981) A comparative study of selective stimulation of raphe nuclei in the cat in inhibiting dorsal horn neuron responses to noxious stimulation. Brain Res 229: 520–524

    Article  CAS  PubMed  Google Scholar 

  • Guilbaud G, Besson JM, Oliveras JL, Liebeskind JC (1973) Suppression by LSD of the inhibitory effect exerted by dorsal raphe stimulation on certain spinal cord interneurons in the cat. Brain Res 61: 417–422

    Article  CAS  PubMed  Google Scholar 

  • Guilbaud G, Oliveras JL, Giesler G, Besson JM (1977) Effects induced by stimulation of the centralis inferior nucleus of the raphe on dorsal horn interneurons in cat’s spinal cord. Brain Res 126: 355–360

    Article  CAS  PubMed  Google Scholar 

  • Hammond DL, Yaksh TL (1984) Antagonism of stimulation produced antinociception by intrathecal administration of methysergide or phentolamine. Brain Res 298: 329–337

    Article  CAS  PubMed  Google Scholar 

  • Haber LH, Martin RF, Chung JM, Willis WD (1980) Inhibition and excitation of primate spinothalamic tract neurons by stimulation in the region of nucleus reticularis gigantocellularis. J Neurophysiol 43: 1578–1593

    CAS  PubMed  Google Scholar 

  • Hodge CJ, Apkarian AV, Stevens RT, Vogelsang GD, Brown O, Franck JI (1983) Dorsolateral pontine inhibition of dorsal horn cell responses to cutaneous stimulation: lack of dependence on catecholaminergic systems in cat. J Neurophysiol 50: 1220–1235

    PubMed  Google Scholar 

  • Johnston SE, Davies J (1981) Descending inhibitions from the nucleus raphe magnus and adjacent reticular formation to the dorsal horn of the rat are not antagonized by bicuculline or strychnine. Neurosci Lett 26: 43–47

    Article  CAS  PubMed  Google Scholar 

  • Jones SL, Gebhart GF (1986) Characterization of coeruleospinal inhibition of the nociceptive tail-flick reflex in the rat: mediation by spinal alpha-2-receptors. Brain Res 364: 315–330

    Article  CAS  PubMed  Google Scholar 

  • Kuypers HGJM, Maisky VA (1977) Funicular trajectories of descending brain stem pathways in cat. Brain Res 136: 159–165

    Article  CAS  PubMed  Google Scholar 

  • Lovick TA, Wolstencroft JH (1979) Inhibitory effects of nucleus raphe magnus on neuronal responses in the spinal trigeminal nucleus to nociceptive compared with nonnociceptive inputs. Pain 7: 135–145

    Article  CAS  PubMed  Google Scholar 

  • Maceiwicz R, Sandrew BB, Phipps BS, Poletti CE, Foote WE (1984) Pontomedullary raphe neurons: intracellular responses to central and peripheral electrical stimulation. Brain Res 293: 17–33

    Article  Google Scholar 

  • Magoun HW, Rhines R (1946) An inhibitory mechanism in the bulbar reticular formation. J Neurophysiol 9: 165–171

    Google Scholar 

  • McCreery DB, Bloedel JR (1975) Reduction in the response of cat spinothalamic neurons to graded mechanical stimuli by electrical stimulation of the lower brain stem. Brain Res 97: 151–156

    Article  CAS  PubMed  Google Scholar 

  • McCreery DB, Bloedel JR, Hames EG (1979) Effects of stimulating in the raphe nuclei and in reticular formation on response of spinothalamic neurons to mechanical stimuli. J Neurophysiol 42: 166–182

    CAS  PubMed  Google Scholar 

  • Mokha SS, McMillan JA, Iggo A (1985) Descending control of spinal nociceptive transmission. Actions produced on spinal multireceptive neurones from the nuclei locus coeruleus (LC) and raphe magnus (NRM). Exp Brain Res 58: 213–226

    Article  CAS  PubMed  Google Scholar 

  • Morton CR, Duggan AW, Zhao ZQ (1984) The effects of lesions of medullary midline and lateral reticular areas on inhibition in the dorsal horn produced by periaqueductal gray stimulation in the cat. Brain Res 301: 121–130

    Article  CAS  PubMed  Google Scholar 

  • Morton CR, Johnson SM, Duggan AW (1983) Lateral reticular regions and the descending control of dorsal horn neurons of the cat: selective inhibition by electrical stimulation. Brain Res 275: 13–21

    Article  CAS  PubMed  Google Scholar 

  • Oliveras JL, Redjemi F, Guilbaud G, Besson JM (1975) Analgesia induced by electrical stimulation of the inferior centralis nucleus of the raphe in the cat. Pain 1: 139–145

    Article  CAS  PubMed  Google Scholar 

  • Pretel S, Guinan MJ, Carstens E (1984) Medullo-spinal inhibition of cat dorsal horn neurons. Soc Neurosci Abstr 10: 100

    Google Scholar 

  • Pretel S, Ruda MA (1985) Immunocytochemical investigation of monoaminergic interaction in brain stem raphe nuclei of the cat. Soc Neurosci Abstr 11: 579

    Google Scholar 

  • Rexed B (1952) The cytoarchitectonic organization of the spinal cord in the cat. J Comp Neurol 96: 415–495

    Article  Google Scholar 

  • Rivot JP, Chaouch A, Besson JM (1980) Nucleus raphe magnus modulation of response of rat dorsal horn neurons to unmyelinated fiber inputs: partial involvement of serotonergic pathways. J Neurophysiol 44: 1039–1057

    CAS  PubMed  Google Scholar 

  • Ross CA, Armstrong DM, Ruggiero DA, Pickel VM, Joh TH, Reis DJ (1981) Adrenaline neurons in the rostral ventrolateral medulla innervate thoracic spinal cord: combined immunocytochemical and retrograde transport demonstration. Neurosci Lett 25: 257–262

    Article  CAS  PubMed  Google Scholar 

  • Satoh M, Akaike A, Nakazawa T, Takagi H (1980) Evidence for involvement of separate mechanisms in the production of analgesia by electrical stimulation of the nucleus reticularis paragigantocellularis and nucleus raphe magnus in the rat. Brain Res 194: 525–529

    Article  CAS  PubMed  Google Scholar 

  • Shah Y, Dostrovsky JO (1982) Postsynaptic inhibition of cat medullary dorsal horn neurons by stimulation of nucleus raphe magnus and other brain stem sites. Exp Neurol 77: 419–435

    Article  CAS  PubMed  Google Scholar 

  • Skagerberg GS, Björklund A (1985) Topographic principles in the spinal projections of serotonergic and non-serotonergic brainstem neurons in the rat. Neuroscience 15: 445–480

    Article  CAS  PubMed  Google Scholar 

  • Tohyama M, Sakai K, Salvert D, Touret H, Jouvet M (1979) Spinal projection from the lower brainstem in the cat as demonstrated by the horseradish peroxidase technique. I. Origins of the reticulo-spinal tracts and their funicular trajectories. Brain Res 173: 383–403

    Article  CAS  PubMed  Google Scholar 

  • Westlund KN, Bowker RM, Ziegler MG, Coulter JD (1983) Noradrenergic projections to the spinal cord of the rat. Brain Res 263: 15–31

    Article  CAS  PubMed  Google Scholar 

  • Westlund KN, Bowker RM, Ziegler MG, Coulter JD (1984) Origins and terminations of descending noradrenergic projections to the spinal cord of monkey. Brain Res 292: 1–16

    Article  CAS  PubMed  Google Scholar 

  • Wicklund L, Leger L, Persson M (1982) Monoamine distribution in the cat brainstem: a fluorescence histochemical study with quantification of indolaminergic and locus coeruleus cell groups. J Comp Neurol 203: 613–647

    Article  Google Scholar 

  • Willis WD (1982) Control of nociceptive transmission in the spinal cord. In: Ottoson D (ed) Progress in sensory physiology, Vol 3. Springer, Heidelberg, pp 159

    Google Scholar 

  • Willis WD, Haber LH, Martin RF (1977) Inhibition of spinothalamic tract cells and interneurons by brain stem stimulation in the monkey. J Neurophysiol 40: 968–981

    CAS  PubMed  Google Scholar 

  • Yezierski RP, Wilcox TK, Willis WD (1982) The effects of serotonin antagonists on the inhibition of primate spinothalamic tract cells produced by stimulation in nucleus raphe magnus or periaqueductal gray. J Pharmacol Exp Therap 220: 266–277

    CAS  Google Scholar 

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  1. S. Pretel

    Present address: Neurobiology and Anesthesiology Branch, NIDR-NIH, Building 30, Room B20, 20205, Bethesda, MD, USA

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  1. Department of Animal Physiology, University of California, 95616, Davis, CA, USA

    S. Pretel, M. J. Guinan & E. Carstens

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  2. M. J. Guinan
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Pretel, S., Guinan, M.J. & Carstens, E. Inhibition of the responses of cat dorsal horn neurons to noxious skin heating by stimulation in medial or lateral medullary reticular formation. Exp Brain Res 72, 51–62 (1988). https://doi.org/10.1007/BF00248500

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