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Published in: Metabolic Brain Disease 1/2020

01-01-2020 | Morphine | Original Article

Impact of different intensities of forced exercise on deficits of spatial and aversive memory, anxiety-like behavior, and hippocampal BDNF during morphine abstinence period in male rats

Authors: Azadeh Shahroodi, Fatemeh Mohammadi, Abbas Ali Vafaei, Hossein Miladi-Gorji, Ahmad Reza Bandegi, Ali Rashidy-Pour

Published in: Metabolic Brain Disease | Issue 1/2020

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Abstract

Forced exercise can alleviate cognitive-behavioral deficits in an experimental model of addiction. However, the effects of different intensities of forced exercise in improving behavioral, cognitive and biochemical deficits during morphine abstinence period are not well investigated. Thus, the current work examined the effects of different loads of forced exercise on cognition functions, anxiety behavior and BDNF changes in the hippocampus, and prefrontal cortex (PFC), and also serum levels of BDNF and corticosterone during the abstinent period in male rats. Animals received morphine injections (10 mg/kg, twice a day) for 10 consecutive days. Then, the animals were exposed to a 4-week forced exercise training program under low, moderate or high intensities (30 min per session on 5 days a week), which accompanied by behavioral and biochemical tests. In Experiment 1, anxiety-like behaviors using elevated plus maze (EPM), and light/dark box (L/D box) were examined. In Experiment 2, cognitive functions using T-maze alteration and passive avoidance tasks were tested, which accompanied by BDNF measurements in the hippocampus and PFC. In Experiment 3, serum levels of BDNF and corticosterone following the termination of forced exercise regimen were measured. Morphine-abstinent animals exhibited anxiogenic -like behaviors in the EPM, but not L/D box. They also exhibited impaired T-maze alternation performance and passive avoidance memory, and a decline in hippocampal BDNF, but not PFC. Forced exercise at a moderate intensity alleviated anxiety, cognitive and BDNF defects in morphine-abstinent animals. The high load exercise enhanced serum levels of corticosterone in both saline and morphine groups. Thus, regular moderate forced exercise may be beneficial in preserving cognitive and mood functions in male addicts during the abstinent period and drug rehabilitation.
Literature
go back to reference Ahmadalipour A, Sadeghzadeh J, Vafaei AA, Bandegi AR, Mohammadkhani R, Rashidy-Pour A (2015) Effects of environmental enrichment on behavioral deficits and alterations in hippocampal BDNF induced by prenatal exposure to morphine in juvenile rats. Neuroscience 305:372–383PubMed Ahmadalipour A, Sadeghzadeh J, Vafaei AA, Bandegi AR, Mohammadkhani R, Rashidy-Pour A (2015) Effects of environmental enrichment on behavioral deficits and alterations in hippocampal BDNF induced by prenatal exposure to morphine in juvenile rats. Neuroscience 305:372–383PubMed
go back to reference Albeck DS, Sano K, Prewitt GE, Dalton L (2006) Mild forced treadmill exercise enhances spatial learning in the aged rat. Behav Brain Res 168:345–348PubMed Albeck DS, Sano K, Prewitt GE, Dalton L (2006) Mild forced treadmill exercise enhances spatial learning in the aged rat. Behav Brain Res 168:345–348PubMed
go back to reference Anderson BJ, Rapp DN, Baek DH, McCloskey DP, Coburn-Litvak PS, Robinson JK (2000) Exercise influences spatial learning in the radial arm maze. Physiol Behav 70:425–429PubMed Anderson BJ, Rapp DN, Baek DH, McCloskey DP, Coburn-Litvak PS, Robinson JK (2000) Exercise influences spatial learning in the radial arm maze. Physiol Behav 70:425–429PubMed
go back to reference Barha CK, Davis JC, Falck RS, Nagamatsu LS, Liu-Ambrose T (2017) Sex differences in exercise efficacy to improve cognition: a systematic review and meta-analysis of randomized controlled trials in older humans. Front Neuroendocrinol 46:71–85PubMed Barha CK, Davis JC, Falck RS, Nagamatsu LS, Liu-Ambrose T (2017) Sex differences in exercise efficacy to improve cognition: a systematic review and meta-analysis of randomized controlled trials in older humans. Front Neuroendocrinol 46:71–85PubMed
go back to reference Bilkei-Gorzo A, Gyertyan I, Levay G (1998) mCPP-induced anxiety in the light-dark box in rats–a new method for screening anxiolytic activity. Psychopharmacology 136:291–298PubMed Bilkei-Gorzo A, Gyertyan I, Levay G (1998) mCPP-induced anxiety in the light-dark box in rats–a new method for screening anxiolytic activity. Psychopharmacology 136:291–298PubMed
go back to reference Binder E, Droste SK, Ohl F, Reul JM (2004) Regular voluntary exercise reduces anxiety-related behaviour and impulsiveness in mice. Behav Brain Res 155:197–206PubMed Binder E, Droste SK, Ohl F, Reul JM (2004) Regular voluntary exercise reduces anxiety-related behaviour and impulsiveness in mice. Behav Brain Res 155:197–206PubMed
go back to reference Blizard DA, Takahashi A, Galsworthy MJ, Martin B, Koide T (2007) Test standardization in behavioural neuroscience: a response to Stanford. J Psychopharmacol 21:136–139PubMed Blizard DA, Takahashi A, Galsworthy MJ, Martin B, Koide T (2007) Test standardization in behavioural neuroscience: a response to Stanford. J Psychopharmacol 21:136–139PubMed
go back to reference Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefPubMed Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefPubMed
go back to reference Chan CB, Ye K (2017) Sex differences in brain-derived neurotrophic factor signaling and functions. J Neurosci Res 95:328–335PubMedPubMedCentral Chan CB, Ye K (2017) Sex differences in brain-derived neurotrophic factor signaling and functions. J Neurosci Res 95:328–335PubMedPubMedCentral
go back to reference Chen Z-Y et al (2006) Genetic variant BDNF (Val66Met) polymorphism alters anxiety-related behavior. Science 314:140–143PubMedPubMedCentral Chen Z-Y et al (2006) Genetic variant BDNF (Val66Met) polymorphism alters anxiety-related behavior. Science 314:140–143PubMedPubMedCentral
go back to reference Cotman CW, Berchtold NC, Christie L-A (2007) Exercise builds brain health: key roles of growth factor cascades and inflammation. Trends Neurosci 30:464–472PubMed Cotman CW, Berchtold NC, Christie L-A (2007) Exercise builds brain health: key roles of growth factor cascades and inflammation. Trends Neurosci 30:464–472PubMed
go back to reference Cryan JF, Holmes A (2005) Model organisms: the ascent of mouse: advances in modelling human depression and anxiety. Nat Rev Drug Discov 4:775PubMed Cryan JF, Holmes A (2005) Model organisms: the ascent of mouse: advances in modelling human depression and anxiety. Nat Rev Drug Discov 4:775PubMed
go back to reference Davis P, Liddiard H, McMillan T (2002) Neuropsychological deficits and opiate abuse. Drug Alcohol Depend 67:105–108PubMed Davis P, Liddiard H, McMillan T (2002) Neuropsychological deficits and opiate abuse. Drug Alcohol Depend 67:105–108PubMed
go back to reference De Graaf R, Bijl R, Spijker J, Beekman A, Vollebergh W (2003) Temporal sequencing of lifetime mood disorders in relation to comorbid anxiety and substance use disorders. Soc Psychiatry Psychiatr Epidemiol 38:1–11PubMed De Graaf R, Bijl R, Spijker J, Beekman A, Vollebergh W (2003) Temporal sequencing of lifetime mood disorders in relation to comorbid anxiety and substance use disorders. Soc Psychiatry Psychiatr Epidemiol 38:1–11PubMed
go back to reference Deacon RM, Rawlins JNP (2006) T-maze alternation in the rodent. Nat Protoc 1:7PubMed Deacon RM, Rawlins JNP (2006) T-maze alternation in the rodent. Nat Protoc 1:7PubMed
go back to reference D'Sa C, Fox HC, Hong AK, Dileone RJ, Sinha R (2011) Increased serum brain-derived neurotrophic factor is predictive of cocaine relapse outcomes: a prospective study. Biol Psychiatry 70:706–711PubMedPubMedCentral D'Sa C, Fox HC, Hong AK, Dileone RJ, Sinha R (2011) Increased serum brain-derived neurotrophic factor is predictive of cocaine relapse outcomes: a prospective study. Biol Psychiatry 70:706–711PubMedPubMedCentral
go back to reference Duman RS, Monteggia LM (2006) A neurotrophic model for stress-related mood disorders. Biol Psychiatry 59:1116–1127PubMed Duman RS, Monteggia LM (2006) A neurotrophic model for stress-related mood disorders. Biol Psychiatry 59:1116–1127PubMed
go back to reference El Hayek L et al (2019) Lactate mediates the effects of exercise on learning and memory through SIRT1-dependent activation of hippocampal brain-derived neurotrophic factor (BDNF). J Neurosci 39:2369–2382PubMedPubMedCentral El Hayek L et al (2019) Lactate mediates the effects of exercise on learning and memory through SIRT1-dependent activation of hippocampal brain-derived neurotrophic factor (BDNF). J Neurosci 39:2369–2382PubMedPubMedCentral
go back to reference Fattore L, Altea S, Fratta W (2008) Sex differences in drug addiction: a review of animal and human studies Fattore L, Altea S, Fratta W (2008) Sex differences in drug addiction: a review of animal and human studies
go back to reference Fuss J et al (2010) Voluntary exercise induces anxiety-like behavior in adult C57BL/6J mice correlating with hippocampal neurogenesis. Hippocampus 20:364–376PubMed Fuss J et al (2010) Voluntary exercise induces anxiety-like behavior in adult C57BL/6J mice correlating with hippocampal neurogenesis. Hippocampus 20:364–376PubMed
go back to reference Ghodrati-Jaldbakhan S, Ahmadalipour A, Rashidy-Pour A, Vafaei AA, Miladi-Gorji H, Alizadeh M (2017) Low-and high-intensity treadmill exercise attenuates chronic morphine-induced anxiogenesis and memory impairment but not reductions in hippocampal BDNF in female rats. Brain Res 1663:20–28PubMed Ghodrati-Jaldbakhan S, Ahmadalipour A, Rashidy-Pour A, Vafaei AA, Miladi-Gorji H, Alizadeh M (2017) Low-and high-intensity treadmill exercise attenuates chronic morphine-induced anxiogenesis and memory impairment but not reductions in hippocampal BDNF in female rats. Brain Res 1663:20–28PubMed
go back to reference Gu C et al (2007) Chronic morphine selectively impairs cued fear extinction in rats: implications for anxiety disorders associated with opiate use. Neuropsychopharmacology 33:666–673PubMed Gu C et al (2007) Chronic morphine selectively impairs cued fear extinction in rats: implications for anxiety disorders associated with opiate use. Neuropsychopharmacology 33:666–673PubMed
go back to reference Gu C et al (2008) Chronic morphine selectively impairs cued fear extinction in rats: implications for anxiety disorders associated with opiate use. Neuropsychopharmacology 33:666–673PubMed Gu C et al (2008) Chronic morphine selectively impairs cued fear extinction in rats: implications for anxiety disorders associated with opiate use. Neuropsychopharmacology 33:666–673PubMed
go back to reference Han J, Zhu H, Chen G, Chen P, Luo L, Liu X, Wang C (2008) [The expression of BDNF and PSD-95 in hippocampal CA1 region of morphine-withdrawn rat with different dependent times] Sichuan da xue xue bao Yi xue ban= Journal of Sichuan University Medical science edition 39:253-255 Han J, Zhu H, Chen G, Chen P, Luo L, Liu X, Wang C (2008) [The expression of BDNF and PSD-95 in hippocampal CA1 region of morphine-withdrawn rat with different dependent times] Sichuan da xue xue bao Yi xue ban= Journal of Sichuan University Medical science edition 39:253-255
go back to reference Heberlein A et al (2011) Serum levels of BDNF are associated with craving in opiate-dependent patients. J Psychopharmacol 25:1480–1484PubMed Heberlein A et al (2011) Serum levels of BDNF are associated with craving in opiate-dependent patients. J Psychopharmacol 25:1480–1484PubMed
go back to reference Kennard JA, Woodruff-Pak DS (2012) A comparison of low-and high-impact forced exercise: effects of training paradigm on learning and memory. Physiol Behav 106:423–427PubMedPubMedCentral Kennard JA, Woodruff-Pak DS (2012) A comparison of low-and high-impact forced exercise: effects of training paradigm on learning and memory. Physiol Behav 106:423–427PubMedPubMedCentral
go back to reference Kim Y et al (2003) Magnitude-and time-dependence of the effect of treadmill exercise on cell proliferation in the dentate gyrus of rats. Int J Sports Med 24:114–117PubMed Kim Y et al (2003) Magnitude-and time-dependence of the effect of treadmill exercise on cell proliferation in the dentate gyrus of rats. Int J Sports Med 24:114–117PubMed
go back to reference Klein AB et al (2011) Blood BDNF concentrations reflect brain-tissue BDNF levels across species. Int J Neuropsychopharmacol 14:347–353PubMed Klein AB et al (2011) Blood BDNF concentrations reflect brain-tissue BDNF levels across species. Int J Neuropsychopharmacol 14:347–353PubMed
go back to reference Lalonde R (2002) The neurobiological basis of spontaneous alternation. Neurosci Biobehav Rev 26:91–104PubMed Lalonde R (2002) The neurobiological basis of spontaneous alternation. Neurosci Biobehav Rev 26:91–104PubMed
go back to reference Lister RG (1987) The use of a plus-maze to measure anxiety in the mouse. Psychopharmacology 92:180–185PubMed Lister RG (1987) The use of a plus-maze to measure anxiety in the mouse. Psychopharmacology 92:180–185PubMed
go back to reference Lu G et al (2010) Chronic morphine treatment impaired hippocampal long-term potentiation and spatial memory via accumulation of extracellular adenosine acting on adenosine A1 receptors. J Neurosci 30:5058–5070PubMedPubMedCentral Lu G et al (2010) Chronic morphine treatment impaired hippocampal long-term potentiation and spatial memory via accumulation of extracellular adenosine acting on adenosine A1 receptors. J Neurosci 30:5058–5070PubMedPubMedCentral
go back to reference Miladi-Gorji H, Rashidy-Pour A, Fathollahi Y, Akhavan MM, Semnanian S, Safari M (2011) Voluntary exercise ameliorates cognitive deficits in morphine dependent rats: the role of hippocampal brain-derived neurotrophic factor. Neurobiol Learn Mem 96:479–491PubMed Miladi-Gorji H, Rashidy-Pour A, Fathollahi Y, Akhavan MM, Semnanian S, Safari M (2011) Voluntary exercise ameliorates cognitive deficits in morphine dependent rats: the role of hippocampal brain-derived neurotrophic factor. Neurobiol Learn Mem 96:479–491PubMed
go back to reference Miladi-Gorji H, Rashidy-Pour A, Fathollahi Y (2012) Anxiety profile in morphine-dependent and withdrawn rats: effect of voluntary exercise. Physiol Behav 105:195–202PubMed Miladi-Gorji H, Rashidy-Pour A, Fathollahi Y (2012) Anxiety profile in morphine-dependent and withdrawn rats: effect of voluntary exercise. Physiol Behav 105:195–202PubMed
go back to reference Mokhtari-Zaer A, Ghodrati-Jaldbakhan S, Vafaei AA, Miladi-Gorji H, Akhavan MM, Bandegi AR, Rashidy-Pour A (2014) Effects of voluntary and treadmill exercise on spontaneous withdrawal signs, cognitive deficits and alterations in apoptosis-associated proteins in morphine-dependent rats. Behav Brain Res 271:160–170PubMed Mokhtari-Zaer A, Ghodrati-Jaldbakhan S, Vafaei AA, Miladi-Gorji H, Akhavan MM, Bandegi AR, Rashidy-Pour A (2014) Effects of voluntary and treadmill exercise on spontaneous withdrawal signs, cognitive deficits and alterations in apoptosis-associated proteins in morphine-dependent rats. Behav Brain Res 271:160–170PubMed
go back to reference Nasiraei-Moghadam S, Sherafat MA, Safari M-S, Moradi F, Ahmadiani A, Dargahi L (2013) Reversal of prenatal morphine exposure-induced memory deficit in male but not female rats. J Mol Neurosci 50:58–69PubMed Nasiraei-Moghadam S, Sherafat MA, Safari M-S, Moradi F, Ahmadiani A, Dargahi L (2013) Reversal of prenatal morphine exposure-induced memory deficit in male but not female rats. J Mol Neurosci 50:58–69PubMed
go back to reference Neeper SA, Gómez-Pinilla F, Choi J, Cotman CW (1996) Physical activity increases mRNA for brain-derived neurotrophic factor and nerve growth factor in rat brain. Brain Res 726:49–56PubMed Neeper SA, Gómez-Pinilla F, Choi J, Cotman CW (1996) Physical activity increases mRNA for brain-derived neurotrophic factor and nerve growth factor in rat brain. Brain Res 726:49–56PubMed
go back to reference Pellow S, Chopin P, File SE, Briley M (1985) Validation of open: closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods 14:149–167PubMed Pellow S, Chopin P, File SE, Briley M (1985) Validation of open: closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods 14:149–167PubMed
go back to reference Peterson AB, Hivick DP, Lynch WJ (2014) Dose-dependent effectiveness of wheel running to attenuate cocaine-seeking: impact of sex and estrous cycle in rats. Psychopharmacology 231:2661–2670PubMed Peterson AB, Hivick DP, Lynch WJ (2014) Dose-dependent effectiveness of wheel running to attenuate cocaine-seeking: impact of sex and estrous cycle in rats. Psychopharmacology 231:2661–2670PubMed
go back to reference Ploughman M (2008) Exercise is brain food: the effects of physical activity on cognitive function. Dev Neurorehabil 11:236–240PubMed Ploughman M (2008) Exercise is brain food: the effects of physical activity on cognitive function. Dev Neurorehabil 11:236–240PubMed
go back to reference Pu L, Bao G-B, Xu N-J, Ma L, Pei G (2002) Hippocampal long-term potentiation is reduced by chronic opiate treatment and can be restored by re-exposure to opiates. J Neurosci 22:1914–1921PubMedPubMedCentral Pu L, Bao G-B, Xu N-J, Ma L, Pei G (2002) Hippocampal long-term potentiation is reduced by chronic opiate treatment and can be restored by re-exposure to opiates. J Neurosci 22:1914–1921PubMedPubMedCentral
go back to reference Sartorius A et al (2009) Correlations and discrepancies between serum and brain tissue levels of neurotrophins after electroconvulsive treatment in rats. Pharmacopsychiatry 42:270–276PubMed Sartorius A et al (2009) Correlations and discrepancies between serum and brain tissue levels of neurotrophins after electroconvulsive treatment in rats. Pharmacopsychiatry 42:270–276PubMed
go back to reference Schaaf MJ, de Jong J, de Kloet ER, Vreugdenhil E (1998) Downregulation of BDNF mRNA and protein in the rat hippocampus by corticosterone. Brain Res 813:112–120PubMed Schaaf MJ, de Jong J, de Kloet ER, Vreugdenhil E (1998) Downregulation of BDNF mRNA and protein in the rat hippocampus by corticosterone. Brain Res 813:112–120PubMed
go back to reference Schrott LM, La'Tonya MF, Serrano PA (2008) Prenatal opiate exposure impairs radial arm maze performance and reduces levels of BDNF precursor following training. Brain Res 1198:132–140PubMedPubMedCentral Schrott LM, La'Tonya MF, Serrano PA (2008) Prenatal opiate exposure impairs radial arm maze performance and reduces levels of BDNF precursor following training. Brain Res 1198:132–140PubMedPubMedCentral
go back to reference Serra-Millàs M (2016) Are the changes in the peripheral brain-derived neurotrophic factor levels due to platelet activation? World J Psychiatr 6:84PubMedPubMedCentral Serra-Millàs M (2016) Are the changes in the peripheral brain-derived neurotrophic factor levels due to platelet activation? World J Psychiatr 6:84PubMedPubMedCentral
go back to reference Soya H et al (2007) BDNF induction with mild exercise in the rat hippocampus. Biochem Biophys Res Commun 358:961–967PubMed Soya H et al (2007) BDNF induction with mild exercise in the rat hippocampus. Biochem Biophys Res Commun 358:961–967PubMed
go back to reference Spain JW, Newsom GC (1991) Chronic opioids impair acquisition of both radial maze and Y-maze choice escape. Psychopharmacology 105:101–106PubMed Spain JW, Newsom GC (1991) Chronic opioids impair acquisition of both radial maze and Y-maze choice escape. Psychopharmacology 105:101–106PubMed
go back to reference Trejo J, Llorens-Martin M, Torres-Aleman I (2008) The effects of exercise on spatial learning and anxiety-like behavior are mediated by an IGF-I-dependent mechanism related to hippocampal neurogenesis. Mol Cell Neurosci 37:402–411PubMed Trejo J, Llorens-Martin M, Torres-Aleman I (2008) The effects of exercise on spatial learning and anxiety-like behavior are mediated by an IGF-I-dependent mechanism related to hippocampal neurogenesis. Mol Cell Neurosci 37:402–411PubMed
go back to reference Van der Borght K, Havekes R, Bos T, Eggen BJ, Van der Zee EA (2007) Exercise improves memory acquisition and retrieval in the Y-maze task: relationship with hippocampal neurogenesis. Behav Neurosci 121:324PubMed Van der Borght K, Havekes R, Bos T, Eggen BJ, Van der Zee EA (2007) Exercise improves memory acquisition and retrieval in the Y-maze task: relationship with hippocampal neurogenesis. Behav Neurosci 121:324PubMed
go back to reference van Praag H, Christie BR, Sejnowski TJ, Gage FH (1999) Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci 96:13427–13431PubMedPubMedCentral van Praag H, Christie BR, Sejnowski TJ, Gage FH (1999) Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci 96:13427–13431PubMedPubMedCentral
go back to reference Van Praag H, Shubert T, Zhao C, Gage FH (2005) Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci 25:8680–8685PubMedPubMedCentral Van Praag H, Shubert T, Zhao C, Gage FH (2005) Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci 25:8680–8685PubMedPubMedCentral
go back to reference Vaynman S, Ying Z, Gomez-Pinilla F (2004) Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. Eur J Neurosci 20:2580–2590PubMed Vaynman S, Ying Z, Gomez-Pinilla F (2004) Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. Eur J Neurosci 20:2580–2590PubMed
go back to reference Venezia AC, Guth LM, Sapp RM, Spangenburg EE, Roth SM (2016) Sex-dependent and independent effects of long-term voluntary wheel running on BDNF mRNA and protein expression. Physiol Behav 156:8–15PubMedPubMedCentral Venezia AC, Guth LM, Sapp RM, Spangenburg EE, Roth SM (2016) Sex-dependent and independent effects of long-term voluntary wheel running on BDNF mRNA and protein expression. Physiol Behav 156:8–15PubMedPubMedCentral
go back to reference Wu CW et al (2007) Treadmill exercise counteracts the suppressive effects of peripheral lipopolysaccharide on hippocampal neurogenesis and learning and memory. J Neurochem 103:2471–2481PubMed Wu CW et al (2007) Treadmill exercise counteracts the suppressive effects of peripheral lipopolysaccharide on hippocampal neurogenesis and learning and memory. J Neurochem 103:2471–2481PubMed
go back to reference Young R, Johnson DN (1991) A fully automated light/dark apparatus useful for comparing anxiolytic agents. Pharmacol Biochem Behav 40:739–743PubMed Young R, Johnson DN (1991) A fully automated light/dark apparatus useful for comparing anxiolytic agents. Pharmacol Biochem Behav 40:739–743PubMed
go back to reference Zhang J et al (2014) Increased serum brain-derived neurotrophic factor levels during opiate withdrawal. Neurosci Lett 571:61–65PubMed Zhang J et al (2014) Increased serum brain-derived neurotrophic factor levels during opiate withdrawal. Neurosci Lett 571:61–65PubMed
go back to reference Zhou Y, Zhao M, Zhou C, Li R (2016) Sex differences in drug addiction and response to exercise intervention: from human to animal studies. Front Neuroendocrinol 40:24–41PubMed Zhou Y, Zhao M, Zhou C, Li R (2016) Sex differences in drug addiction and response to exercise intervention: from human to animal studies. Front Neuroendocrinol 40:24–41PubMed
Metadata
Title
Impact of different intensities of forced exercise on deficits of spatial and aversive memory, anxiety-like behavior, and hippocampal BDNF during morphine abstinence period in male rats
Authors
Azadeh Shahroodi
Fatemeh Mohammadi
Abbas Ali Vafaei
Hossein Miladi-Gorji
Ahmad Reza Bandegi
Ali Rashidy-Pour
Publication date
01-01-2020
Publisher
Springer US
Keywords
Morphine
Anxiety
Published in
Metabolic Brain Disease / Issue 1/2020
Print ISSN: 0885-7490
Electronic ISSN: 1573-7365
DOI
https://doi.org/10.1007/s11011-019-00518-w

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