GABAergic transmission in rat pontine reticular formation regulates the induction phase of anesthesia and modulates hyperalgesia caused by sleep deprivation

European Journal of Neuroscience

Volumn 40, Issue 1, 2014, Pages 2264-2273

  Vanini, Giancarlo ^a   Nemanis, Kriste ^a   Baghdoyan, Helen A ^a   Lydic, Ralph ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Consciousness; Emergence; Microdialysis; Microinjection; Pain

Indexed keywords

3 MERCAPTOPROPIONIC ACID; 4 AMINOBUTYRIC ACID; ISOFLURANE; NIPECOTIC ACID; PROPOFOL; 4 AMINOBUTYRIC ACID UPTAKE INHIBITOR; ANESTHETIC AGENT; GABAERGIC RECEPTOR AFFECTING AGENT; NIPECOTIC ACID DERIVATIVE;

ADULT; ANESTHESIA INDUCTION; ANESTHETIC RECOVERY; ANIMAL EXPERIMENT; ARTICLE; CONSCIOUSNESS; CONTROLLED STUDY; EXTRACELLULAR SPACE; GABAERGIC TRANSMISSION; HYPERALGESIA; MALE; NOCICEPTION; NONHUMAN; PONS RETICULAR FORMATION; PRIORITY JOURNAL; RAT; RIGHTING REFLEX; SLEEP DEPRIVATION; WAKEFULNESS; ANIMAL; DRUG EFFECTS; HEAT; METABOLISM; PAIN THRESHOLD; PATHOPHYSIOLOGY; PHYSIOLOGY; PONTINE TEGMENTUM; SPRAGUE DAWLEY RAT; TIME;

3-MERCAPTOPROPIONIC ACID; ANESTHETICS, GENERAL; ANIMALS; CONSCIOUSNESS; GABA AGENTS; GABA UPTAKE INHIBITORS; GAMMA-AMINOBUTYRIC ACID; HOT TEMPERATURE; HYPERALGESIA; ISOFLURANE; MALE; NIPECOTIC ACIDS; NOCICEPTION; PAIN THRESHOLD; PONTINE TEGMENTUM; PROPOFOL; RATS, SPRAGUE-DAWLEY; REFLEX, RIGHTING; SLEEP DEPRIVATION; TIME FACTORS;

EID: 84903906309     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12571     Document Type: Article

References (83)

1. Alkire, M.T., McReynolds, J.R., Hahn, E.L. & Trivedi, A.N. (2007) Thalamic microinjection of nicotine reverses sevoflurane-induced loss of righting reflex in the rat. Anesthesiology, 107, 264-272.
2. Alsip, N.L. & DiMicco, J.A. (1992) Time course of effects of 3-mercaptopropionic acid on GABA levels in different brain regions in guinea pigs: possible relationship with associated cardiovascular changes. Neurochem. Res., 17, 443-448.
3. Alsip, N.L., Simon, J.R., Fohl, L.D. & DiMicco, J.A. (1984) Cardiovascular effects of 3-mercaptopropionic acid and levels of GABA in regions of the brain of guinea-pigs. Neuropharmacology, 23, 349-357.
4. Angulo, M.C., Le Meur, K., Kozlov, A.S., Charpak, S. & Audinat, E. (2008) GABA, a forgotten gliotransmitter. Prog. Neurobiol., 86, 297-303.
5. Arima, T., Svensson, P., Rasmussen, C., Nielsen, K.D., Drewes, A.M. & Arendt-Nielsen, L. (2001) The relationship between selective sleep deprivation, nocturnal jaw-muscle activity and pain in healthy men. J. Oral Rehabil., 28, 140-148.
6. Baghdoyan, H.A. & Lydic, R. (2012) The neurochemistry of sleep and wakefulness. In Brady, S.T., Albers, R.W., Price, D.L. & Siegel, G.J. (Eds), Basic Neurochemistry. Elsevier, New York, pp. 982-999.
7. A receptor. Mol. Pharmacol., 65, 68-76.
8. Baracchi, F. & Opp, M.R. (2008) Sleep-wake behavior and responses to sleep deprivation of mice lacking both interleukin-1 beta receptor 1 and tumor necrosis factor-alpha receptor 1. Brain Behav. Immun., 22, 982-993.
9. Boissard, R., Fort, P., Gervasoni, D., Barbagli, B. & Luppi, P.H. (2003) Localization of the GABAergic and non-GABAergic neurons projecting to the sublaterodorsal nucleus and potentially gating paradoxical sleep onset. Eur. J. Neurosci., 18, 1627-1639.
10. Brevig, H.N., Watson, C.J., Lydic, R. & Baghdoyan, H.A. (2010) Hypocretin and GABA interact in the pontine reticular formation to increase wakefulness. Sleep, 33, 1285-1293.
11. Brown, E.N., Lydic, R. & Schiff, N.D. (2010) General anesthesia, sleep, and coma. New Engl. J. Med., 363, 2638-2650.
12. Brown, R.E., Basheer, R., McKenna, J.T., Strecker, R.E. & McCarley, R.W. (2012) Control of sleep and wakefulness. Physiol. Rev., 92, 1087-1187.
13. Callahan, B.L., Gil, A.S., Levesque, A. & Mogil, J.S. (2008) Modulation of mechanical and thermal nociceptive sensitivity in the laboratory mouse by behavioral state. J. Pain, 9, 174-184.
14. Camacho-Arroyo, I., Alvarado, R., Manjarrez, J. & Tapia, R. (1991) Microinjections of muscimol and bicuculline into the pontine reticular formation modify the sleep-waking cycle in the rat. Neurosci. Lett., 129, 95-97.
15. Devor, M. & Zalkind, V. (2001) Reversible analgesia, atonia, and loss of consciousness on bilateral intracerebral microinjection of pentobarbital. Pain, 94, 101-112.
16. DiMicco, J.A. & Abshire, V.M. (1987) Evidence for GABAergic inhibition of a hypothalamic sympathoexcitatory mechanism in anesthetized rats. Brain Res., 402, 1-10.
17. Dutta, S., Matsumoto, Y., Gothgen, N.U. & Ebling, W.F. (1997) Concentration-EEG effect relationship of propofol in rats. J. Pharm. Sci., 86, 37-43.
18. Edwards, R.R., Almeida, D.M., Klick, B., Haythornthwaite, J.A. & Smith, M.T. (2008) Duration of sleep contributes to next-day pain report in the general population. Pain, 137, 202-207.
19. Engel, D., Pahner, I., Schulze, K., Frahm, C., Jarry, H., Ahnert-Hilger, G. & Draguhn, A. (2001) Plasticity of rat central inhibitory synapses through GABA metabolism. J. Physiol., 535, 473-482.
20. Enna, S.J. & McCarson, K.E. (2006) The role of GABA in the mediation and perception of pain. Adv. Pharmacol., 54, 1-27.
21. A receptors in the pontine reticular formation of C57BL/6J mouse modulate neurochemical, electrographic, and behavioral phenotypes of wakefulness. J. Neurosci., 30, 12301-12309.
22. Franks, N.P. (2008) General anaesthesia: from molecular targets to neuronal pathways of sleep and arousal. Nat. Rev. Neurosci., 9, 370-386.
23. Friedman, E.B., Sun, Y., Moore, J.T., Hung, H.T., Meng, Q.C., Perera, P., Joiner, W.J., Thomas, S.A., Eckenhoff, R.G., Sehgal, A. & Kelz, M.B. (2010) A conserved behavioral state barrier impedes transitions between anesthetic-induced unconsciousness and wakefulness: evidence for neural inertia. PLoS ONE, 5, e11903.
24. Gauthier, E.A., Guzick, S.E., Brummett, C.M., Baghdoyan, H.A. & Lydic, R. (2011) Buprenorphine disrupts sleep and decreases adenosine concentrations in sleep-regulating brain regions of Sprague Dawley rat. Anesthesiology, 115, 743-753.
25. Ghazni, N.F., Cahill, C.M. & Stroman, P.W. (2010) Tactile sensory and pain networks in the human spinal cord and brain stem mapped by means of functional MR imaging. Am. J. Neuroradiol., 31, 661-667.
26. Halassa, M.M., Fellin, T. & Haydon, P.G. (2009) Tripartite synapses: roles for astrocytic purines in the control of synaptic physiology and behavior. Neuropharmacology, 57, 343-346.
27. Hamann, M., Rossi, D.J. & Attwell, D. (2002) Tonic and spillover inhibition of granule cells control information flow through cerebellar cortex. Neuron, 33, 625-633.
28. Hambrecht-Wiedbusch, V.S., Gauthier, E.A., Baghdoyan, H.A. & Lydic, R. (2010) Benzodiazepine receptor agonists cause drug-specific and state-specific alterations in EEG power and acetylcholine release in rat pontine reticular formation. Sleep, 33, 909-918.
29. Hargreaves, K., Dubner, R., Brown, F., Flores, C. & Joris, J. (1988) A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain, 32, 77-88.
30. Hayes, R.L., Katayama, Y., Watkins, L.R. & Becker, D.P. (1984) Bilateral lesions of the dorsolateral funiculus of the cat spinal cord: effects on basal nociceptive reflexes and nociceptive suppression produced by cholinergic activation of the pontine parabrachial region. Brain Res., 311, 267-280.
31. Herbison, A.E., Heavens, R.P. & Dyer, R.G. (1990) Endogenous release of gamma-aminobutyric acid from the medial preoptic area measured by microdialysis in the anaesthetised rat. J. Neurochem., 55, 1617-1623.
32. A receptors important targets for sedative/hypnotic drugs? J. Neurosci., 32, 3887-3897.
33. Hudetz, A.G., Vizuete, J.A. & Pillay, S. (2011) Differential effects of isoflurane on high-frequency and low-frequency gamma oscillations in the cerebral cortex and hippocampus in freely moving rats. Anesthesiology, 114, 588-595.
34. Kehr, J. & Ungerstedt, U. (1988) Fast HPLC estimation of gamma-aminobutyric acid in microdialysis perfusates: effect of nipecotic and 3-mercaptopropionic acids. J. Neurochem., 51, 1308-1310.
35. Kelz, M.B., Sun, Y., Chen, J., Cheng Meng, Q., Moore, J.T., Veasey, S.C., Dixon, S., Thornton, M., Funato, H. & Yanagisawa, M. (2008) An essential role for orexins in emergence from general anesthesia. Proc. Natl. Acad. Sci. USA, 105, 1309-1314.
36. Kennedy, D. & Norman, C. (2005) What don't we know? Science, 309, 75.
37. Knight, Y.E., Classey, J.D., Lasalandra, M.P., Akerman, S., Kowacs, F., Hoskin, K.L. & Goadsby, P.J. (2005) Patterns of fos expression in the rostral medulla and caudal pons evoked by noxious craniovascular stimulation and periaqueductal gray stimulation in the cat. Brain Res., 1045, 1-11.
38. Krogsgaard-Larsen, P. & Johnston, G.A. (1975) Inhibition of GABA uptake in rat brain slices by nipecotic acid, various isoxazoles and related compounds. J. Neurochem., 25, 797-802.
39. Kshatri, A.M., Baghdoyan, H.A. & Lydic, R. (1998) Cholinomimetics, but not morphine, increase antinociceptive behavior from pontine reticular regions regulating rapid-eye-movement sleep. Sleep, 21, 677-685.
40. Liang, C.L. & Marks, G.A. (2009) A novel GABAergic afferent input to the pontine reticular formation: the mesopontine GABAergic column. Brain Res., 1297, 32-40.
41. Maneuf, Y.P., Gonzalez, M.I., Sutton, K.S., Chung, F.Z., Pinnock, R.D. & Lee, K. (2003) Cellular and molecular action of the putative GABA-mimetic, gabapentin. Cell. Mol. Life Sci., 60, 742-750.
42. Marks, G.A., Sachs, O.W. & Birabil, C.G. (2008) Blockade of GABA, type A, receptors in the rat pontine reticular formation induces rapid eye movement sleep that is dependent upon the cholinergic system. Neuroscience, 156, 1-10.
43. Miller, G. (2005) What is the biological basis of consciousness? Science, 309, 79.
44. Mitchell, S.J. & Silver, R.A. (2000) GABA spillover from single inhibitory axons suppresses low-frequency excitatory transmission at the cerebellar glomerulus. J. Neurosci., 20, 8651-8658.
45. Monnerie, H. & Le Roux, P.D. (2007) Reduced dendrite growth and altered glutamic acid decarboxylase (GAD) 65- and 67-kDa isoform protein expression from mouse cortical GABAergic neurons following excitotoxic injury in vitro. Exp. Neurol., 205, 367-382.
46. Namjoshi, D.R., McErlane, S.A., Taepavarapruk, N. & Soja, P.J. (2009) Network actions of pentobarbital in the rat mesopontine tegmentum on sensory inflow through the spinothalamic tract. J. Neurophysiol., 102, 700-713.
47. Nemanis, K., Vanini, G., Baghdoyan, H.A. & Lydic, R. (2011) GABAergic transmission in Sprague-Dawley rat pontine reticular formation (PRF) modulates time required for the general anesthetic propofol to cause loss of wakefulness. SLEEP 34 (Abstr Suppl):0010, 2011. SLEEP Meeting, 2011. Minneapolis.
48. Paxinos, G. & Watson, C. (2007) The Rat Brain in Stereotaxic Coordinates, 6th Edn. Academic Press, Burlington, MA.
49. Peterfi, Z., McGinty, D., Sarai, E. & Szymusiak, R. (2010) Growth hormone-releasing hormone activates sleep regulatory neurons of the rat preoptic hypothalamus. Am. J. Physiol.-Reg. I., 298, R147-R156.
50. Porro, C.A., Cavazzuti, M., Galetti, A. & Sassatelli, L. (1991) Functional activity mapping of the rat brainstem during formalin-induced noxious stimulation. Neuroscience, 41, 667-680.
51. Price, D.D. (2000) Psychological and neural mechanisms of the affective dimension of pain. Science, 288, 1769-1772.
52. Richey, S.M. & Krystal, A.D. (2011) Pharmacological advances in the treatment of insomnia. Curr. Pharm. Design, 17, 1471-1475.
53. Robinson, T.E., Gorny, G., Mitton, E. & Kolb, B. (2001) Cocaine self-administration alters the morphology of dendrites and dendritic spines in the nucleus accumbens and neocortex. Synapse, 39, 257-266.
54. Rodrigo-Angulo, M.L., Heredero, S., Rodriguez-Veiga, E. & Reinoso-Suarez, F. (2008) GABAergic and non-GABAergic thalamic, hypothalamic and basal forebrain projections to the ventral oral pontine reticular nucleus: their implication in REM sleep modulation. Brain Res., 1210, 116-125.
55. Roehrs, T., Hyde, M., Blaisdell, B., Greenwald, M. & Roth, T. (2006) Sleep loss and REM sleep loss are hyperalgesic. Sleep, 29, 145-151.
56. Roehrs, T.A., Harris, E., Randall, S. & Roth, T. (2012) Pain sensitivity and recovery from mild chronic sleep loss. Sleep, 35, 1667-1672.
57. Sanford, L.D., Tang, X., Xiao, J., Ross, R.J. & Morrison, A.R. (2003) GABAergic regulation of REM sleep in reticularis pontis oralis and caudalis in rats. J. Neurophysiol., 90, 938-945.
58. Sapin, E., Lapray, D., Berod, A., Goutagny, R., Leger, L., Ravassard, P., Clement, O., Hanriot, L., Fort, P. & Luppi, P.H. (2009) Localization of the brainstem GABAergic neurons controlling paradoxical (REM) sleep. PLoS ONE, 4, e4272.
59. Steriade, M. & McCarley, R.W. (2005) Brain Control of Wakefulness and Sleep. Kluwer Academic/Plenum Press, New York.
60. Tanase, D., Baghdoyan, H.A. & Lydic, R. (2002) Microinjection of an adenosine A1 agonist into the medial pontine reticular formation increases tail flick latency to thermal stimulation. Anesthesiology, 97, 1597-1601.
61. Tassone, D.M., Boyce, E., Guyer, J. & Nuzum, D. (2007) Pregabalin: a novel gamma-aminobutyric acid analogue in the treatment of neuropathic pain, partial-onset seizures, and anxiety disorders. Clin. Ther., 29, 26-48.
62. Timmerman, W. & Westerink, B.H. (1997) Brain microdialysis of GABA and glutamate: what does it signify? Synapse, 27, 242-261.
63. Timmerman, W., Zwaveling, J. & Westerink, B.H. (1992) Characterization of extracellular GABA in the substantia nigra reticulata by means of brain microdialysis. N.-S. Arch. Pharmacol., 345, 661-665.
64. Tobler, I. & Jaggi, K. (1987) Sleep and EEG spectra in the Syrian hamster (Mesocricetus auratus) under baseline conditions and following sleep deprivation. J. Comp. Physiol. A., 161, 449-459.
65. Toth, E. & Lajtha, A. (1988) 3-Mercaptopropionic acid administration into the caudate-putamen of the rat provokes dyskinesia. Pharmacol. Biochem. Be., 29, 525-528.
66. Tung, A., Herrera, S., Szafran, M.J., Kasza, K. & Mendelson, W.B. (2005) Effect of sleep deprivation on righting reflex in the rat is partially reversed by administration of adenosine A1 and A2 receptor antagonists. Anesthesiology, 102, 1158-1164.
67. Van der Heyden, J.A., Venema, K. & Korf, J. (1979) In vivo release of endogenous GABA from rat substantia nigra measured by a novel method. J. Neurochem., 32, 469-476.
68. A receptors in rat pontine reticular formation increase wakefulness. Sleep, 36, 337-343.
69. Vanini, G. & Nemanis, K. (2013) Nociception caused by sleep deprivation is reduced by decreasing GABA levels in rat pontine reticular formation. Sleep 36 (Abstr Suppl):0281, 2013. SLEEP Meeting, 2013. Baltimore.
70. Vanini, G., Torterolo, P., McGregor, R., Chase, M.H. & Morales, F.R. (2007) GABAergic processes in the mesencephalic tegmentum modulate the occurrence of active (rapid eye movement) sleep in guinea pigs. Neuroscience, 145, 1157-1167.
71. Vanini, G., Watson, C.J., Lydic, R. & Baghdoyan, H.A. (2008) Gamma-aminobutyric acid-mediated neurotransmission in the pontine reticular formation modulates hypnosis, immobility, and breathing during isoflurane anesthesia. Anesthesiology, 109, 978-988.
72. Vanini, G., Teran, M.A., Zhou, M., Baghdoyan, H.A. & Lydic, R. (2009) GABAergic transmission in rat pontine reticular formation (PRF) does not modulate recovery time from isoflurane anesthesia. Society for Neuroscience Abstract Viewer/Itinerary Planner, Online: Program No. 375.13, 2009. 39th Annual Meeting, Chicago.
73. Vanini, G., Wathen, B.L., Lydic, R. & Baghdoyan, H.A. (2011) Endogenous GABA levels in the pontine reticular formation are greater during wakefulness than during rapid eye movement sleep. J. Neurosci., 31, 2649-2656.
74. Vanini, G., Lydic, R. & Baghdoyan, H.A. (2012) GABA-to-ACh ratio in basal forebrain and cerebral cortex varies significantly during sleep. Sleep, 35, 1325-1334.
75. B receptors in the brainstem of the rat. Eur. J. Pharmacol., 214, 223-232.
76. Wang, W., Baghdoyan, H.A. & Lydic, R. (2009) Leptin replacement restores supraspinal cholinergic antinociception in leptin-deficient obese mice. J. Pain, 10, 836-843.
77. Watson, C.J., Venton, B.J. & Kennedy, R.T. (2006) In vivo measurements of neurotransmitters by microdialysis sampling. Anal. Chem., 78, 1391-1399.
78. Watson, C.J., Lydic, R. & Baghdoyan, H.A. (2007) Sleep and GABA levels in the oral part of rat pontine reticular formation are decreased by local and systemic administration of morphine. Neuroscience, 144, 375-386.
79. Watson, C.J., Soto-Calderon, H., Lydic, R. & Baghdoyan, H.A. (2008) Pontine reticular formation (PnO) administration of hypocretin-1 increases PnO GABA levels and wakefulness. Sleep, 31, 453-464.
80. Watson, S.L., Watson, C.J., Baghdoyan, H.A. & Lydic, R. (2010) Thermal nociception is decreased by hypocretin-1 and an adenosine A1 receptor agonist microinjected into the pontine reticular formation of Sprague Dawley rat. J. Pain, 11, 535-544.
81. Watson, C.J., Lydic, R. & Baghdoyan, H.A. (2011) Sleep duration varies as a function of glutamate and GABA in rat pontine reticular formation. J. Neurochem., 118, 571-580.
82. Westphalen, R.I. & Hemmings, H.C. Jr. (2003) Selective depression by general anesthetics of glutamate versus GABA release from isolated cortical nerve terminals. J. Pharmacol. Exp. Ther., 304, 1188-1196.
83. Xi, M.C., Morales, F.R. & Chase, M.H. (1999) Evidence that wakefulness and REM sleep are controlled by a GABAergic pontine mechanism. J. Neurophysiol., 82, 2015-2019.