Abstract
In cats, we studied the influences of stimulation of the periaqueductal gray (PAG) and locus coeruleus (LC) on postsynaptic processes evoked in neurons of the somatosensory cortex by stimulation of nociceptive (intensive stimulation of the tooth pulp) and non-nociceptive (moderate stimulations of the infraorbital nerve and ventroposteromedial nucleus of the thalamus) afferent inputs. Twelve cells activated exclusively by nociceptors and 16 cells activated by both nociceptive and non-nociceptive influences (hereafter, nociceptive and convergent neurons, respectively) were recorded intracellularly. In neurons of both groups, responses to nociceptive stimulation (of sufficient intensity) looked like an EPSP-spike-IPSP (the latter, of significant duration, up to 200 msec) complex. Electrical stimulation of the PAG (which could itself evoke activation of the cortical neurons under study) resulted in long-term suppression of synaptic responses evoked by excitation of nociceptors (inhibition reached its maximum at a test interval of 600 to 800 msec). We observed a certain parallelism between conditioning influences of PAG activation and effects of systemic injections of morphine. Isolated stimulation of LC by a short high-frequency train of stimuli evoked primary excitatory responses (complex EPSPs) in a part of the examined cortical neurons, while in other cells high-amplitude and long-lasting IPSP (up to 120 msec) were observed. Independently of the type of the primary response to PAG stimulation, the latter resulted in long-term (several seconds) suppression of the responses evoked in cortical cells by stimulation of the nociceptive inputs. The mechanisms of modulatory influences coming from opioidergic and noradrenergic brain systems to somatosensory cortex neurons activated due to excitation of high-threshold (nociceptive) afferent inputs are discussed.
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REFERENCES
R. Maldonado, “Participation of noradrenergic pathways in the expression of opiate withdrawal: biochemical and pharmacological evidence,” Neurosci. Biobehav. Rev., 21, 91–104 (1997).
R. Sumino, Y. Tsuboi, J. Yagi, et al., “Morphology of primary somatosensory cortical neurons responsive to noxious stimulation of the trigeminal regions,” in: Proceedings of the 7th World Congress on Pain. Progress in Pain Research and Management, Vol. 2, G. F. Gebhart, D. L. Hammond, and T. S. Jensen (eds.), IASP Press, Seattle (1994), pp. 813–816.
D. R. Kenshalo, K. Iwata, M. Sholas, and D. A. Thomas, “Response properties and organization of nociceptive neurons in area 1 of monkey primary somatosensory cortex,” J. Neurophysiol., 84, No.2, 719–729 (2000).
R. Dubner and G. J. Bennett, “Spinal and trigeminal mechanisms of nociception,” Annu. Rev. Neurosci., 6, 381–418 (1983).
E. V. Gura, “Suppression of postsynaptic responses of motoneurons of the nucleus of the trigeminal nerve induced by stimulation of the midbrain periaqueductal gray,” Neirofiziologiya, 22, No.4, 543–549 (1990).
E. V. Gura and V. V. Garkavenko, “Effect of stimulation of the midbrain periaqueductal gray on responses of neurons of the ventroposteromedial nucleus of the thalamus in the cat,” Neirofiziologiya, 20, No.5, 688–694 (1988).
J. Hosobuchi, J. Rossier, F. E. Bloom, and R. Guillemin, Periaqueductal Gray Stimulation for Pain Suppression in Humans, Vol. 3, Raven Press (1979), pp. 515–523
E. O. Bragin, Neurochemical Mechanisms of the Control of Pain Sensitivity [in Russian], Nauka, Moscow (1991).
F. E. Bloom, “What is the role of general activating systems in cortical function?” in: Neurobiology of Neocortex, P. Rakic and W. Singer (eds.), John Willey and Sons, Berlin (1988), pp. 407–421.
D. A. McCormic, “Cholinergic and noradrenergic modulation of thalamocortical processing,” Trends Neurosci., 12, No.6, 215–226 (1989).
N. Reader, F. Ferron, L. Descerries, and H. H. Jasper, “Modulator role for biogenic amines in the cerebral cortex; microiontophoretic studies,” Trends Neurosci., 160, No.2, 217–229 (1979).
B. D. Waterhouse and D. J. Woodward, “Noradrenergic modulation of somatosensory cortical neuronal responses to iontophoretically applied putative neurotransmitter,” Exp. Neurol., 69, No.1, 30–49 (1980).
S. L. Foote and J. H. Morrison, “Extrathalamic modulation of cortical function,” Ann. Rev. Neurosci., 10, 67–95 (1987).
F. Reinoso-Suarez, Topographischer Hirnatlas der Katze, E. Merck, Darmstadt (1961).
O. G. Baklavadzhyan, A. G. Darbinyan, and I. Kh. Taturyan, “Responses of neurons of different hypothalamic structures to stimulation of the tooth pulp and Aβ fibers of the sciatic nerve in the cat,” Neirofiziologiya, 18, No.2, 171–180 (1986).
A. I. Semenyutin, “Effect of electrical stimulation of the locus coeruleus on the activity of neurons of the parietal associative cortex,” Neirofiziologiya, 22, No.4, 486–494 (1990).
E. C. Cropper, J. S. Eisenman, and E. S. Armitia, “5 HT immunoreactive fibers in the trigeminal nuclear complex of the cat,” Exp. Brain Res., 55, No.2, 515–522 (1984).
R. A. Nicoll, G. R. Siggins, N. Ling, and F. E. Bloom, “Neuronal actions of endorphins and enkephalins among brain regions: A comparative microiontophoretic study,” Proc. Natl. Acad. Sci. USA, 74, 2584–2588 (1977).
H. Khachaturian, M. E. Levis, M. K. H. Schafer, and S. J. Watson, “Anatomy of the CNS opioid systems,” Trends Neurosci., 8, 111–119 (1985).
F. M. Sessler, R. D. Mouradian, J. T. Chang, et al., “Noradrenergic potentiation of cerebellar Purkinje cell responses t o GABA: Evidence for mediation through the b-adrenoceptor-coupled cyclic AMP system,” Brain Res., 499, No.1, 27–38 (1989).
T. Kasanatsu and P. Heggelund, “Single cell responses in cat visual cortex to visual stimulation during iontophoresis of noradrenaline,” Exp. Brain Res., 45, No.2, 317–327 (1982).
A. P. Kniga and B. I. Bousel’, “Modulatory effect of noradrenaline on the impulse activity of neurons of the cat motor cortex upon electrical stimulation and influence of the additional stimulus,” Neirofiziologiya/Neurophysiology, 1, No.2, 119–125 (1993).
O. Kh. Koshtoyants and T. Yu. Antipina, Neurochemical Basis of Learning and Memory [in Russian] Nauka, Moscow (1989).
R. C. Foehring, P. C. Schwindt, and W. F. Crill, “Norepinephrine selectively reduces slow Ca2+ and Na+-mediated K+ currents in cat neocortical neurons,” J. Neurophysiol., 61, No.2, 245–256 (1989).
J. M. Crowder and H. F. Bradford, “Noradrenaline and dopamine effects on calcium influx and neurotransmitter glutamate release in mammalian brain slices,” Eur. J. Pharmacol., 143, No.3, 343–352 (1987).
M. Nishiori, R. Oishi, Y. Itoh, and K. Saeki, “Galanin inhibits noradrenaline-induced accumulation of cyclic AMP in the rat cerebral cortex,” J. Neurochem., 51, No.6, 1953–1955 (1988).
H. Tatsumi, M. Costa, M. Schimeric, and R. A. North, “Potassium conductance increased by noradrenaline, opioids, somatostatin and G-protein,” J. Neurosci., 10, No.5, 1675–1682 (1990).
D. V. Madison and R. A. Nicoll, “Noradrenaline blocks accommodation of pyramidal cell discharge in the hippocampus,” Nature, 299, No.5884, 636–638 (1982).
W. Singewald, S. T. Kachler, and A. Philippu, “Stress-evoked noradrenaline release in somatodendritic (locus coeruleus) and terminal (amygdala) regions of noradrenergic neurons: a dual-probe push-pull perfusion study,” Schmiedeberg’s Arch. Pharmacol., 357,Suppl. 27 (1998).
J. A. Stampord, “Descending control of pain,” J. Anesth., 75, 217–227 (1995).
L. Descarries, K. C. Watkins, and Y. Lapierre, “Noradrenergic axon terminals in the cerebral cortex of rat,” Brain Res., 133, No.1, 117–122 (1977).
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Neirofiziologiya/Neurophysiology, Vol. 37, No. 1, pp. 61–73, January–February, 2005.
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Labakhua, T.S., Butkhousi, S.M., Bekaya, G.L. et al. Effects of Stimulation of the Periaqueductal Gray and Locus Coeruleus on Postsynaptic Reactions of Cat Somatosensory Cortex Neurons Activated by Nociceptors. Neurophysiology 37, 56–66 (2005). https://doi.org/10.1007/s11062-005-0045-z
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DOI: https://doi.org/10.1007/s11062-005-0045-z