Nucleus accumbens local field potential power spectrums, phase - amplitude couplings and coherences following morphine treatment

• Autorzy: Reakkamnuan C. , Cheaha D. , Kumarnsit E.
• Języki publikacji: EN

Abstrakty

EN

In the past decade, neural processing has been extensively studied in cognitive neuroscience. However, neural signaling in the nucleus accumbens (NAc) that might clarify reward process remained to be investigated. Male Swiss albino ICR mice implanted with intracranial electrodes into the NAc and the ventral tegmental area (VTA) were used for morphine administration and local field potential (LFP) recording. One‑way ANOVA revealed significant increases in low (30.3–44.9 Hz) and high (60.5–95.7 Hz) gamma powers in the NAc following morphine administration (5 and 15 mg/kg, i.p.). These gamma activities oscillated independently with different time‑course responses. Locomotor activity was also significantly increased by morphine administration. Regression analyses revealed that high gamma activity induced by morphine was positively correlated with distance travelled by animals. Low and high gamma powers were completely abolished by injection of naloxone, a non‑specific opiate antagonist. Analysis of phase‑amplitude coupling confirmed that slow oscillations at 1–4 Hz (delta) and 4–8 Hz (theta) for phase were found to significantly increase modulation index of broad (30.27–80.77 Hz) and narrow (59.48–70.34 Hz) frequency ranges for amplitude, respectively. Moreover, significant increases in coherence values between the NAc and the VTA during 30–40 min following morphine administration were seen for 22.46–44.90 Hz frequency range. Altogether, this study demonstrated changes of LFP oscillations in the NAc with low and high gamma activities, delta‑ and theta‑gamma couplings and interplay with VTA in response to morphine administration. These findings represent neural signaling in the mesolimbic dopamine pathway that might process reward function.

• Wydawca: -
• Czasopismo: Acta Neurobiologiae Experimentalis
• Rocznik: 2017
• Tom: 77
• Numer: 3
• Opis fizyczny: p.214-224,fig.,ref.

Twórcy

autor

Reakkamnuan C.

• Department of Physiology, Faculty of Science, Prince of Songkla University (PSU), Hat Yai, Songkhla, Thailand

autor

Cheaha D.

• Department of Biology, Faculty of Science, Prince of Songkla University (PSU), Hat Yai, Songkhla, Thailand
• Research Unit for EEG Biomarkers of Neuronal diseases, Faculty of Science, Prince of Songkla University (PSU), Hat Yai, Songkhla, Thailand

autor

Kumarnsit E.

• Department of Physiology, Faculty of Science, Prince of Songkla University (PSU), Hat Yai, Songkhla, Thailand
• 1Research Unit for EEG Biomarkers of Neuronal diseases, Faculty of Science, Prince of Songkla University (PSU), Hat Yai, Songkhla, Thailand

Bibliografia

• Abbott FV, Melzack R, Samuel C (1982) Morphine analgesia in the tail‑flick and formalin pain tests is mediated by different neural systems. Exp Neurol 75: 644–651.
• Albin RL, Young AB, Penney JB (1989) The functional anatomy of basal ganglia disorders. Trends Neurosci 12: 366–375.
• Becker A, Grecksch G, Brodemann R, Kraus J, Peters B, Schroeder H, Thiemann  W, Loh HH, Hollt  V (2000) Morphine self‑administration in mu‑opioid receptor‑deficient mice. Naunyn‑Schmiedeberg’s Arch of Pharmacol 361: 584–589.
• Bergamini G, Sigrist H, Ferger B, Singewald N, Seifritz E, Pryce CR (2016) Depletion of nucleus accumbens dopamine leads to impaired reward and aversion processing in mice: relevance to motivatio pathologies. Neuropharmacology 109: 306–319.
• Berke JD (2009) Fast oscillations in cortical‑striatal networks switch frequency following rewarding events and stimulant drugs. Eur J Neurosci 30: 848–859.
• Bott JB, Muller MA, Jackson J, Aubert J, Cassel JC, Mathis C, Goutagny  R (2015) Spatial reference memory is associated with modulation of theta‑gamma coupling in the dentate gyrus. Cereb Cortex 26: 1–10.
• Bozarth MA, Wise RA (1981) Intracranial self‑administration of morphine into the ventral tegmental area in rats. Life Sci 28: 551–555.
• Cheaha D, Bumrungsri S, Chatpun S, Kumarnsit E (2015) Characterization of in utero valproic acid mouse model of autism by local field potential in the hippocampus and the olfactory bulb. Neurosci Res 98: 28–34.
• De Solages C, Hill BC, Koop MM, Henderson JM, Bronte‑Stewart H (2010) Bilateral symmetry and coherence of subthalamic nuclei beta band activity in Parkinson’s disease. Exp Neurol 221: 260–266.
• DeCoteau WE, Thorn C, Gibson DJ, Courtemanche R, Mitra P, Kubota Y, Graybiel AM (2007) Oscillations of local field potentials in the rat dorsal striatum during spontaneous and instructed behaviors. J Neurophysiol 97: 3800–3805.
• Di Chiara G, Imperato A (1988) Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc Natl Acad Sci USA 85: 5274–5278.
• Ettenberg A, Pettit HO, Bloom FE, Koob GF (1982) Heroin and cocaine intravenous self‑administration in rats: mediation by separate neural systems. Psychopharmacology (Berl) 78: 204–209.
• Fibiger H, LePiane A, Jakubovic A, Phillips A (1987) The role of dopamine in intracranial self‑stimulatio of the ventral tegmental area. J Neurosci 7: 3888–3896.
• Gail A, Brinksmeyer HJ, Eckhorn R (2004) Perception‑related modulations of local field potential power and coherence in primary visual cortex of awake monkey during binocular rivalry. Cereb Cortex 14: 300–313.
• Ghosh S, Patel AH, Cousins M, Grasing K (1998) Different effects of opiate withdrawal on dopamine turnover, uptake, and release in the striatum and nucleus accumbens. Neurochem Res 23: 875–885.
• Goutagny R, Gu N, Cavanagh C, Jackson J, Chabot JG, Quirion R, Krantic S, Williams S (2013) Alterations in hippocampal network oscillations and theta‑gamma coupling arise before A β overproduction in a  mouse model of Alzheimer’s disease. Eur J of Neurosci 37: 1896–1902.
• Gysling K, Wang RY (1983) Morphine‑induced activation of A10 dopamine neurons in the rat. Brain Res 277: 119–127.
• Hnasko TS, Sotak BN, Palmiter RD (2005) Morphine reward in dopamine‑deficient mice. Nature 438: 854–857.
• Huo X, Xiang J, Wang Y, Kirtman EG, Kotecha R, Fujiwara H, Hemasilpin N, Rose DF, Degrauw T (2010) Gamma oscillations in the primary motor cortex studied with MEG. Brain and Development 32: 619–624.
• Johnson SW, North RA (1992) Opioids excite dopamine neurons by hyperpolarization of local interneurons. J Neurosci 12: 483–488.
• Kalenscher T, Lansink CS, Lankelma JV, Pennartz CM (2010) Reward‑associated gamma oscillations in ventral striatum are regionally differentiated and modulate local firing activity. J Neurophysiol 103: 1658–1672.
• Kalivas PW, Duffy P (1987) Sensitization to repeated morphine injection in the rat: possible involvement of A10 dopamine neurons. J  Pharmacol Exp Ther 241: 204–212.
• Komek K, Bard Ermentrout G, Walker C, Cho R (2012) Dopamine and gamma band synchrony in schizophrenia‑insights from computational and empirical studies. Eur J Neurosci 36: 2146–2155.
• Koob GF (1992a) Dopamine, addiction and reward. Seminars in Neuroscience 4: 139–148. Koob GF (1992b) Drugs of abuse: anatomy, pharmacology and function of reward pathways. Trends Pharmacol Sci 13: 177–184.
• Kornet  M, Goosen C, Van Ree JM (1991) Effect of naltrexone on alcohol consumption during chronic alcohol drinking and after a  period of imposed abstinence in free‑choice drinking rhesus monkeys. Psychopharmacology (Berl) 104: 367–376.
• Kumarnsit E, Harnyuttanakorn P, Meksuriyen D, Govitrapong P, Baldwin BA, Kotchabhakdi N, Casalotti SO (1999) Pseudoephedrine, a  sympathomimetic agent, induces Fos‑like immunoreactivity in rat nucleus accumbens and striatum. Neuropharmacology 38: 1381–1387.
• Lemaire N, Hernandez LF, Hu D, Kubota Y, Howe MW, Graybiel AM (2012) Effects of dopamine depletion on LFP oscillations in striatum are task‑and learning‑dependent and selectively reversed by L‑DOPA. Proc Natl Acad Sci USA 109: 18126–18131.
• Lotharius J, Brundin P (2002) Pathogenesis of Parkinson’s disease: dopamine, vesicles and alpha‑synuclein. Nat Rev Neurosci 3: 932–942.
• Lubetzki C, Chesselet MF, Glowinski J (1982) Modulation of dopamine release in rat striatal slices by delta opiate agonists. J  Pharmacol Exp Ther 222: 435–440.
• Maldonado R, Stinus  L, Gold LH, Koob GF (1992) Role of different brain structures in the expression of the physical morphine withdrawal syndrome. J Pharmacol Exp Ther 261: 669–677.
• Marsden CD (1982) Basal ganglia disease. Lancet 2: 1141–1147.
• McIntyre CK, Ragozzino ME, Gold PE (1998) Intra‑amygdala infusions of scopolamine impair performance on a  conditioned place preference task but not a spatial radial maze task. Behav Brain Res 95: 219–226.
• Muñoz‑Villegas P, Rodriques VM, Giordano M, Juarez J (2017) Risk‑taking, locomotor activity and dopamine levels in the nucleus accumbens and medial prefrontal cortex in male rats treated prenatally with alcohol. Pharmacol Biochem Behav 153: 88–96.
• Murphy NP, Lam HA, Maidment NT (2001) A comparison of morphine‑induced locomotor activity and mesolimbic dopamine release in C57BL6, 129Sv and DBA2 mice. J Neurochem 79: 626–635.
• Negus SS, Henriksen SJ, Mattox A, Pasternak GW, Portoghese PS, Takemori AE, Weinger MB, Koob GF (1993) Effect of antagonists selective for mu, delta and kappa opioid receptors on the reinforcing effects of heroin in rats. J Pharmacol Exp Ther 265: 1245–1252.
• Nishida H, Takahashi M, Lauwereyns J (2014) Within‑session dynamics of theta‑gamma coupling and high‑frequency oscillations during spatial alternation in rat hippocampal area CA1. Cogn Neurodyn 8: 363–372.
• Park JY, Lee YR, Lee J (2011) The relationship between theta‑gamma coupling and spatial memory ability in older adults. Neurosci Lett 498: 37–41.
• Park JY, Jhung K, Lee J, An SK (2013) Theta‑gamma coupling during a working memory task as compare to a simple vigilance task. Neurosci Lett 532: 39–43.
• Pothos E, Rada P, Mark GP, Hoebel BG (1991) Dopamine microdialysis in the nucleus accumbens during acute and chronic morphine, naloxone‑precipitated withdrawal and clonidine treatment. Brain Res 566: 348–350.
• Reakkamnuan C, Hiranyachattada S, Kumarnsit E (2015) Low gamma wave oscillations in the striatum of mice following morphine administration. J Physiol Sci 65(suppl2): 11–16.
• Samson HH, Doyle TF (1985) Oral ethanol self‑administration in the rat: effect of naloxone. Pharmacol Biochem Behav 22: 91–99.
• Sato W, Kochiyama T, Uono S, Matsuda K, Usui K, Inoue Y, Toichi M (2014) Rapid, high‑frequency, and theta‑coupled gamma oscillations in the inferior occipital gyrus during face processing. Cortex 60: 52–68.
• Sellings LH, Clarke PB (2003) Segregation of amphetamine reward and locomotor stimulation between nucleus accumbens medial shell and core. J Neurosci 23: 6295–6303.
• Singer  W, Gray CM (1995) Visual feature integration and the temporal correlation hypothesis. Annu Rev Neurosci 18: 555–586.
• Skelin I, Needham MA, Molina LM, Metz GA, Gruber AJ (2015) Multigenerational prenatal stress increases the coherence of brain signaling among cortico‑striatal‑limbic circuits in adult rats. Neuroscience 289: 270–278.
• Sklair‑Tavron  L, Shi WX, Lane SB, Harris HW, Bunney BS, Nestler EJ (1996) Chronic morphine induces visible changes in the morphology of mesolimbic dopamine neurons. Proc Natl Acad Sci USA 93: 11202–11207.
• Spanagel R, Weiss F (1999) The dopamine hypothesis of reward: past and current status. Trends Neurosci 22: 521–527.
• Sweeney‑Reed CM, Zaehle T, Voges J, Schmitt FC, Buentjen L, Kopitzki K, Hinrichs H, Heinze HJ, Rugg MD, Knight RT (2015) Thalamic theta phase alignment predicts human memory formation and anterior thalamic cross‑frequency coupling. Elife 4: 1–9.
• Tadel F, Baillet S, Mosher JC, Pantazis D, Leahy RM (2011) Brainstorm: A  user‑friendly application for MEG/EEG analysis. Comput Intell Neurosci 2011:1–13.
• Tallon‑Baudry C, Kreiter A, Bertrand O (1999) Sustained and transient oscillatory responses in the gamma and beta bands in a  visual short‑term memory task in humans. Vis Neurosci 16: 449–459.
• Tran AH, Tamura R, Uwano T, Kobayashi T, Katsuki M, Matsumoto G, Ono T (2002) Altered accumbens neural response to prediction of reward associated with place in dopamine D2 receptor knockout mice. Proc Natl Acad Sci USA 99: 8986–8991.
• Tran AH, Tamura R, Uwano T, Kobayashi T, Katsuki  M, Ono T (2005) Dopamine D1 receptors involved in locomotor activity and accumbens neural responses to prediction of reward associated with place. Proc Natl Acad Sci USA 102: 2117–2122.
• Uchimura N, North RA (1990) Actions of cocaine on rat nucleus accumbens neurones in vitro. Br J Pharmacol 99: 736–740.
• Van Der Kooy D, Mucha RF, O’Shaughnessy  M, Bucenieks P (1982) Reinforcing effects of brain microinjections of morphine revealed by conditioned place preference. Brain Res 243: 107–117.
• Van Der Meer MA, Redish AD (2009) Low and high gamma oscillations in rat ventral striatum have distinct relationships to behavior, reward, and spiking activity on a  learned spatial decision task. Front Integr Neurosci 3: 3–19.
• Volkow ND, Wang GJ, Fowler JS, Tomasi D, Telang F (2011) Addiction: beyond dopamine reward circuitry. Proc Natl Acad Sci USA 108: 15037–15042.
• Wikler A (1948) Recent progress in research on the neurophysiologic basis of morphine addiction. Am J Psychiatry 105: 329–338.
• Xi ZX, Fuller SA, Stein EA (1998) Dopamine release in the nucleus accumbens during heroin self‑administration is modulated by kappa opioid receptors: an in vivo fast‑cyclic voltammetry study. J Pharmacol Exp Ther 284: 151–161.
• Yim HJ, Gonzales RA (2000) Ethanol‑induced increases in dopamine extracellular concentration in rat nucleus accumbens are accounted for by increased release and not uptake inhibition. Alcohol 22: 107–115.
• Yokel RA, Wise RA (1975) Increased lever pressing for amphetamine after pimozide in rats: implications for a dopamine theory of reward. Science 187: 547–549.
• Yoo JH, Yang EM, Lee SY, Loh HH, Ho K, Jang CG (2003) Differential effects of morphine and cocaine on locomotor activity and sensitization in mu‑opioid receptor knockout mice. Neurosci Lett 344: 37–40.
• Zarrindast MR, Zarghi A (1992) Morphine stimulates locomotor activity by an indirect dopaminergic mechanism: possible D‑1 and D‑2 receptor involvement. Gen Pharmacol 23: 1221–1225.