Prolonged morphine exposure during adolescence alters the responses of lateral paragigantocellularis neurons to naloxone in adult morphine dependent rats

The Journal of Physiological Sciences - Tập 71 - Trang 1-8 - 2021
Sara Sabuee1, S. Mohammad Ahmadi-Soleimani2, Hossein Azizi1
1Department of Physiology, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran
2Deparment of Physiology, School of Paramedical Sciences, Torbat Heydariyeh University of Medical Sciences, Torbat Heydariyeh, Iran

Tóm tắt

Adolescence is a critical period in brain development, and it is characterized by persistent maturational alterations in the function of central nervous system. In this respect, many studies show the non-medical use of opioid drugs by adolescents. Although this issue has rather widely been addressed during the last decade, cellular mechanisms through which adolescent opioid exposure may induce long-lasting effects are not duly understood. The present study examined the effect of adolescent morphine exposure on neuronal responses of lateral paragigantocellularis nucleus to naloxone in adult morphine-dependent rats. Adolescent male Wistar rats (31 days old) received increasing doses of morphine (from 2.5 to 25 mg/kg, twice daily, s.c.) for 10 days. Control subjects were injected saline with the same protocol. After a drug-free interval (20 days), animals were rendered dependent on morphine during 10 days (10 mg/kg, s.c., twice daily). Then, extracellular single-unit recording was performed to investigate neural response of LPGi to naloxone in adult morphine-dependent rats. Results indicated that adolescent morphine treatment increases the number of excitatory responses to naloxone, enhances the baseline activity and alters the pattern of firing in neurons with excitatory responses in adult morphine-dependent rats. Moreover, the intensity of excitatory responses is reduced following the early life drug intake. It seems that prolonged opioid exposure during adolescence induces long-lasting neurobiological changes in LPGi responsiveness to future opioid withdrawal challenges.

Tài liệu tham khảo

Bohn LM, Gainetdinov RR, Lin F-T, Lefkowitz RJ, Caron MG (2000) μ-Opioid receptor desensitization by β-arrestin-2 determines morphine tolerance but not dependence. Nature 408(6813):720–723 Chen Y, Sommer C (2009) The role of mitogen-activated protein kinase (MAPK) in morphine tolerance and dependence. Mol Neurobiol 40(2):101–107 Martini L, Whistler JL (2007) The role of mu opioid receptor desensitization and endocytosis in morphine tolerance and dependence. Curr Opin Neurobiol 17(5):556–564 Ueda H, Ueda M (2009) Mechanisms underlying morphine analgesic tolerance and dependence. Front Biosci 14:5260–5272 Williams JT, Christie MJ, Manzoni O (2001) Cellular and synaptic adaptations mediating opioid dependence. Physiol Rev 81(1):299–343 Christie M, Williams J, North R (1987) Cellular mechanisms of opioid tolerance: studies in single brain neurons. Mol Pharmacol 32(5):633–638 Romer D (2010) Adolescent risk taking, impulsivity, and brain development: implications for prevention. Dev Psychobiol: J Int Soc Dev Psychobiol 52(3):263–276 Spear LP (2000) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24(4):417–463 Cecil KM, Brubaker CJ, Adler CM, Dietrich KN, Altaye M, Egelhoff JC et al (2008) Decreased brain volume in adults with childhood lead exposure. PLoS Med 5(5):112 Salmanzadeh H, Ahmadi-Soleimani SM, Pachenari N, Azadi M, Halliwell RF, Rubino T et al (2020) Adolescent drug exposure: a review of evidence for the development of persistent changes in brain function. Brain Res Bull 156:105–117 Salmanzadeh H, Ahmadi-Soleimani M, Azadi M, Halliwell RF, Azizi H (2021) Adolescent substance abuse, transgenerational consequences and epigenetics. Curr Neuropharmacol. https://doi.org/10.2174/1570159x19666210303121519 Salmanzadeh H, Azizi H, Semnanian S (2017) Adolescent chronic escalating morphine administration induces long lasting changes in tolerance and dependence to morphine in rats. Physiol Behav 174:191–196 Salmanzadeh H, Azizi H, Soleimani SMA, Pachenari N, Semnanian S (2018) Chronic adolescent morphine exposure alters the responses of lateral paragigantocellular neurons to acute morphine administration in adulthood. Brain Res Bull 137:178–186 Torabi M, Azizi H, Ahmadi-Soleimani SM, Rezayof A (2019) Adolescent nicotine challenge promotes the future vulnerability to opioid addiction: Involvement of lateral paragigantocellularis neurons. Life Sci 234:116784 Ahmadi-Soleimani SM, Ghaemi-Jandabi M, Azizi H, Semnanian S (2014) Orexin type 1 receptor antagonism in Lateral Paragigantocellularis nucleus attenuates naloxone precipitated morphine withdrawal symptoms in rats. Neurosci Lett 558:62–66 Azadi M, Gompf HS, Azizi H (2020) Paternal exposure to morphine during adolescence potentiates morphine withdrawal in male offspring: Involvement of the lateral paragigantocellularis nucleus. J Psychopharmacol 34(11):1289–99. Liu N, Rockhold RW, Ho K (1999) Electrical stimulation of nucleus paragigantocellularis induces opioid withdrawal-like behaviors in the rat. Pharmacol Biochem Behav 62(2):263–271 Hajos M, Engberg G (1990) A role of excitatory amino acids in the activation of locus coeruleus neurons following cutaneous thermal stimuli. Brain Res 521(1–2):325–328 Kaeidi A, Azizi H, Javan M, Soleimani SMA, Fathollahi Y, Semnanian S (2015) Direct facilitatory role of paragigantocellularis neurons in opiate withdrawal-induced hyperactivity of rat locus coeruleus neurons: an in vitro study. PLoS ONE 10(7):0134873 Aston-Jones G, Ennis M, Pieribone VA, Nickell WT, Shipley MT (1986) The brain nucleus locus coeruleus: restricted afferent control of a broad efferent network. Science 234(4777):734–737 Ennis M, Aston-Jones G (1988) Activation of locus coeruleus from nucleus paragigantocellularis: a new excitatory amino acid pathway in brain. J Neurosci 8(10):3644–3657 Ennis M, Aston-Jones G, Shiekhattar R (1992) Activation of locus coeruleus neurons by nucleus paragigantocellularis or noxious sensory stimulation is mediated by intracoerulear excitatory amino acid neurotransmission. Brain Res 598(1–2):185–195 Aghajanian GK, Kogan J, Moghaddam B (1994) Opiate withdrawal increases glutamate and aspartate efflux in the locus coeruleus: an in vivo microdialysis study. Brain Res 636(1):126–130 Rasmussen K, Aghajanian GK (1989) Withdrawal-induced activation of locus coeruleus neurons in opiate-dependent rats: attenuation by lesions of the nucleus paragigantocellularis. Brain Res 505(2):346–350 Ahmadi-Soleimani SM, Azizi H, Gompf HS, Semnanian S (2017) Role of orexin type-1 receptors in paragiganto-coerulear modulation of opioid withdrawal and tolerance: a site specific focus. Neuropharmacology 126:25–37 Johnson A, Peoples J, Stornetta R, Van Bockstaele E (2002) Opioid circuits originating from the nucleus paragigantocellularis and their potential role in opiate withdrawal. Brain Res 955(1–2):72–84 Ghaemi-Jandabi M, Azizi H, Semnanian S (2014) Blockade of orexin type 1 receptors inhibits the development of morphine tolerance in lateral paragigantocellularis nucleus: an electrophysiological approach. Brain Res 1578:14–22 Paxinos G, Watson C (2006) The rat brain in stereotaxic coordinates: hard cover edition: Elsevier. Sirieix C, Gervasoni D, Luppi P-H, Leger L (2012) Role of the lateral paragigantocellular nucleus in the network of paradoxical (REM) sleep: an electrophysiological and anatomical study in the rat. PLoS ONE 7(1):28724 Rahmati-Dehkordi F, Ghaemi-Jandabi M, Garmabi B, Semnanian S, Azizi H (2021) Circadian rhythm influences naloxone induced morphine withdrawal and neuronal activity of lateral paragigantocellularis nucleus. Behav Brain Res 414:113450. Glazer E, Steinbusch H, Verhofstad A, Basbaum A (1981) Serotonin neurons in nucleus raphe dorsalis and paragigantocellularis of the cat contain enkephalin. J de Physiol 77(2–3):241–245 Zhu H, Zhou W (2010) Discharge activities of neurons in the nucleus paragigantocellularis during the development of morphine tolerance and dependence: a single unit study in chronically implanted rats. Eur J Pharmacol 636(1–3):65–72 Labonte B, McLaughlin RJ, Dominguez-Lopez S, Bambico FR, Lucchino I, Ochoa-Sanchez R et al (2012) Adolescent amphetamine exposure elicits dose-specific effects on monoaminergic neurotransmission and behaviour in adulthood. Int J Neuropsychopharmacol 15(9):1319–1330 McQuiston AR, Saggau P (2003) Mu-opioid receptors facilitate the propagation of excitatory activity in rat hippocampal area CA1 by disinhibition of all anatomical layers. J Neurophysiol 90(3):1936–1948 Pan Y-Z, Li D-P, Chen S-R, Pan H-L (2004) Activation of μ-opioid receptors excites a population of locus coeruleus-spinal neurons through presynaptic disinhibition. Brain Res 997(1):67–78 Navratilova E, Ji G, Phelps C, Qu C, Hein M, Yakhnitsa V et al (2019) Kappa opioid signaling in the central nucleus of the amygdala promotes disinhibition and aversiveness of chronic neuropathic pain. Pain 160(4):824 Bull FA, Baptista-Hon DT, Lambert JJ, Walwyn W, Hales TG (2017) Morphine activation of mu opioid receptors causes disinhibition of neurons in the ventral tegmental area mediated by β-arrestin2 and c-Src. Sci Rep 7(1):1–11 Lovick T (1988) GABA-mediated inhibition in nucleus paragigantocellularis lateralis in the cat. Neurosci Lett 92(2):182–186 Saiepour MH, Semnanian S, Fathollahi Y (2001) Occurrence of morphine tolerance and dependence in the nucleus paragigantocellularis neurons. Eur J Pharmacol 411(1–2):85–92