[en] While animal research has consistently reported preventive effects of exercise against drug abuse vulnerability, little is known about the influence of the developmental stage during which exercise is displayed on addictive drugs responsiveness. This study aimed to determine whether prenatal exercise could attenuate acute cocaine reactivity and psychomotor sensitization in youth offspring. We used a split-plot factorial design where C57BL/6 J females were randomly assigned into sedentary or exercised (wheel-running) conditions before and during gestation, the wheels being removed on gestational day 18. Offspring were weaned, gendered and individually housed on 24–28 days old. At 38–42 days old, they were tested for their acute psychomotor responsiveness to 8 mg/kg cocaine and their initiation of sensitization over 8 additional once-daily administrations, the long-term expression of sensitization occurring 30 days later. Adolescent females born from exercised mothers were much less responsive to the acute psychomotor-stimulating effect of cocaine than those born from sedentary mothers (d=0.75, p=0.02), whereas there was no evidence for such a difference in males (d=0.34, p=0.17). However, we did not find sizeable attenuating effects of prenatal exercise on the initiation and the long-term expression of the psychomotor-activating effect of cocaine, in either sex (Cohen’s ds varying from −0.13 to 0.39). These results suggest that prenatal exercise may induce initial protection against cocaine responsiveness in youth females, a finding that warrants further research.
Research Center/Unit :
GIGA CRC (Cyclotron Research Center) In vivo Imaging-Aging & Memory - ULiège
Disciplines :
Neurosciences & behavior
Author, co-author :
Lespine, Louis-Ferdinand ; Université de Liège - ULiège > Département de Psychologie > Neuroscience comportementale et psychopharmacologie expér.
Plenevaux, Alain ; Université de Liège - ULiège > Département de chimie (sciences) > Département de chimie (sciences)
Tirelli, Ezio ; Université de Liège - ULiège > Département de Psychologie > Neuroscience comportementale et psychopharmacologie expér.
Language :
English
Title :
Wheel-running exercise before and during gestation against acute and sensitized cocaine psychomotor-activation in offspring.
Publication date :
28 January 2019
Journal title :
Behavioural Brain Research
ISSN :
0166-4328
eISSN :
1872-7549
Publisher :
Elsevier, Netherlands
Volume :
363
Pages :
53-60
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE]
Hassandra, M., Goudas, M., Theodorakis, Y., Exercise and smoking: a literature overview. Health 07:11 (2015), 1477–1491, 10.4236/health.2015.711162.
Lynch, W.J., Peterson, A.B., Sanchez, V., Abel, J., Smith, M.A., Exercise as a novel treatment for drug addiction: a neurobiological and stage-dependent hypothesis. Neurosci. Biobehav. Rev. 37:8 (2013), 1622–1644, 10.1016/j.neubiorev.2013.06.011.
Bardo, M.T., Compton, W.M., Does physical activity protect against drug abuse vulnerability?. Drug Alcohol Depend. 153 (2015), 3–13, 10.1016/j.drugalcdep.2015.05.037.
Renteria Diaz, L., Siontas, D., Mendoza, J., Arvanitogiannis, A., High levels of wheel running protect against behavioral sensitization to cocaine. Behav. Brain Res. 237 (2013), 82–85, 10.1016/j.bbr.2012.09.014.
Geuzaine, A., Tirelli, E., Wheel-running mitigates psychomotor sensitization initiation but not post-sensitization conditioned activity and conditioned place preference induced by cocaine in mice. Behav. Brain Res. 262 (2014), 57–67, 10.1016/j.bbr.2014.01.002.
Lespine, L.-F., Tirelli, E., The protective effects of free wheel-running against cocaine psychomotor sensitization persist after exercise cessation in C57BL/6J mice. Neuroscience 310 (2015), 650–664, 10.1016/j.neuroscience.2015.10.009.
Lespine, L.-F., Tirelli, E., Evidence for a long-term protection of wheel-running exercise against cocaine psychomotor sensitization in adolescent but not in adult mice. Behav. Brain Res. 349 (2018), 63–72, 10.1016/j.bbr.2018.04.054.
Leyton, M., Vezina, P., Striatal ups and downs: their roles in vulnerability to addictions in humans. Neurosci. Biobehav. Rev. 37:9 (2013), 1999–2014, 10.1016/j.neubiorev.2013.01.018.
Steketee, J.D., Kalivas, P.W., Drug wanting: behavioral sensitization and relapse to drug-seeking behavior. Pharmacol. Rev. 63:2 (2011), 348–365, 10.1124/pr.109.001933.
Doremus-Fitzwater, T.L., Varlinskaya, E.I., Spear, L.P., Motivational systems in adolescence: possible implications for age differences in substance abuse and other risk-taking behaviors. Brain Cogn., 72(1), 2010, 114, 10.1016/j.bandc.2009.08.008.
Wahlstrom, D., White, T., Luciana, M., Neurobehavioral Evidence for Changes in Dopamine System Activity During Adolescence. Neurosci. Biobehav. Rev. 34:5 (2010), 631–648, 10.1016/j.neubiorev.2009.12.007.
Committee Opinion No. 650: Physical Activity and Exercise During Pregnancy and the Postpartum Period. Obstet. Gynecol. 126:6 (2015), e135–e142, 10.1097/AOG.0000000000001214.
Barakat, R., Perales, M., Garatachea, N., Ruiz, J.R., Lucia, A., Exercise during pregnancy. A narrative review asking: what do we know?. Br. J. Sports Med., 49(21), 2015, 1377, 10.1136/bjsports-2015-094756.
Riemann, M.K., Hansen, I.-L.K., Effects on the foetus of exercise in pregnancy. Scand. J. Med. Sci. Sports 10:1 (2000), 12–19, 10.1034/j.1600-0838.2000.010001012.x.
Mudd, L.M., Owe, K.M., Mottola, M.F., Pivarnik, J.M., Health benefits of physical activity during pregnancy: an international perspective. Med. Sci. Sports Exerc. 45:2 (2013), 268–277, 10.1249/MSS.0b013e31826cebcb.
Moyer, C., Reoyo, O.R., May, L., The influence of prenatal exercise on offspring health: a review. Clin. Med. Insights Womens Health, 2016, 9, 10.4137/CMWH.S34670 CMWH.S34670.
Aksu, I., Baykara, B., Ozbal, S., Cetin, F., Sisman, A.R., Dayi, A., et al. Maternal treadmill exercise during pregnancy decreases anxiety and increases prefrontal cortex VEGF and BDNF levels of rat pups in early and late periods of life. Neurosci. Lett. 516:2 (2012), 221–225, 10.1016/j.neulet.2012.03.091.
Gomes da Silva, S., Unsain, N., Mascó D.H., Toscano-Silva, M., de Amorim, H.A., Silva Araújo, B.H., et al. Early exercise promotes positive hippocampal plasticity and improves spatial memory in the adult life of rats. Hippocampus 22:2 (2012), 347–358, 10.1002/hipo.20903.
Parnpiansil, P., Jutapakdeegul, N., Chentanez, T., Kotchabhakdi, N., Exercise during pregnancy increases hippocampal brain-derived neurotrophic factor mRNA expression and spatial learning in neonatal rat pup. Neurosci. Lett. 352:1 (2003), 45–48, 10.1016/j.neulet.2003.08.023.
Robinson, A.M., Bucci, D.J., Physical exercise during pregnancy improves object recognition memory in adult offspring. Neuroscience, 2014, 256, 10.1016/j.neuroscience.2013.10.012.
Kilkenny, C., Browne, W.J., Cuthill, I.C., Emerson, M., Altman, D.G., Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. J. Pharmacol. Pharmacother. 1:2 (2010), 94–99, 10.4103/0976-500X.72351.
Kirk, R.E., Experimental Design: Procedures for the Behavioral Sciences. 3rd ed., 1995, Brooks/Cole, Pacific Grove, Calif.
Laviola, G., Macrı̀ S., Morley-Fletcher, S., Adriani, W., Risk-taking behavior in adolescent mice: psychobiological determinants and early epigenetic influence. Neurosci. Biobehav. Rev. 27:1–2 (2003), 19–31, 10.1016/S0149-7634(03)00006-X.
Brabant, C., Quertemont, E., Tirelli, E., Evidence that the relations between novelty-induced activity, locomotor stimulation and place preference induced by cocaine qualitatively depend upon the dose: a multiple regression analysis in inbred C57BL/ 6J mice. Behav. Brain Res. 158 (2005), 201–210, 10.1016/j.bbr.2004.08.020.
Pruessner, J.C., Kirschbaum, C., Meinlschmid, G., Hellhammer, D.H., Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-dependent change. Psychoneuroendocrinology 28:7 (2003), 916–931, 10.1016/S0306-4530(02)00108-7.
Cohen, J., Statistical Power Analysis for the Behavioral Sciences. 1988, L. Erlbaum Associates, Hillsdale, N.J.
Rosenthal, R., Rosnow, R.L., Contrast Analysis: Focused Comparisons in the Analysis of Variance. 2009, Cambridge Univ. Pr., Cambridge.
Sawilowsky, S.S., New effect size rules of thumb. J. Mod. Appl. Stat. Methods 8:2 (2009), 597–599, 10.22237/jmasm/1257035100.
Karasawa, K., Suwa, J., Kimura, S., Voluntary exercise during pregnancy and lactation and its effect on lactational performance in mice. J. Nutr. Sci. Vitaminol. 27:4 (1981), 333–339.
Kelly, S.A., Hua, K., Wallace, J.N., Wells, S.E., Nehrenberg, D.L., Pomp, D., Maternal exercise before and during pregnancy does not impact offspring exercise or body composition in mice. J. Negat. Results Biomed., 14(1), 2015, 10.1186/s12952-015-0032-x.
Zhao, Z.-J., Król, E., Moille, S., Gamo, Y., Speakman, J.R., Limits to sustained energy intake. XV. Effects of wheel running on the energy budget during lactation. J. Exp. Biol., 216(12), 2013, 2316, 10.1242/jeb.078402.
Dayi, A., Agilkaya, S., Ozbal, S., Cetin, F., Aksu, I., Gencoglu, C., et al. Maternal aerobic exercise during pregnancy can increase spatial learning by affecting leptin expression on offspring's early and late period in life depending on gender. Sci. World J., 2012, 10.1100/2012/429803.
Kim, H., Lee, S.-H., Kim, S.-S., Yoo, J.-H., Kim, C.-J., The influence of maternal treadmill running during pregnancy on short-term memory and hippocampal cell survival in rat pups. Int. J. Dev. Neurosci. 25:4 (2007), 243–249, 10.1016/j.ijdevneu.2007.03.003.
Lee, H.-H., Kim, H., Lee, J.-W., Kim, Y.-S., Yang, H.-Y., Chang, H.-K., et al. Maternal swimming during pregnancy enhances short-term memory and neurogenesis in the hippocampus of rat pups. Brain Dev. 28:3 (2006), 147–154, 10.1016/j.braindev.2005.05.007.
Rice, D., Barone, S., Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ. Health Perspect. 108:Suppl. 3 (2000), 511–533.
Maccari, S., Krugers, H.J., Morley-Fletcher, S., Szyf, M., Brunton, P.J., The Consequences of early-life adversity: neurobiological, behavioural and epigenetic adaptations. J. Neuroendocrinol. 26:10 (2014), 707–723, 10.1111/jne.12175.
Hamilton, D.A., Akers, K.G., Rice, J.P., Johnson, T.E., Candelaria-Cook, F.T., Maes, L.I., et al. Prenatal exposure to moderate levels of ethanol alters social behavior in adult rats: relationship to structural plasticity and immediate early gene expression in frontal cortex. Behav. Brain Res., 207(2), 2010, 290, 10.1016/j.bbr.2009.10.012.
Fodor, A., Tímár, J., Zelena, D., Behavioral effects of perinatal opioid exposure. Life Sci. 104:1 (2014), 1–8, 10.1016/j.lfs.2014.04.006.
Sanchez Vega, M.C., Chong, S., Burne, T.H.J., Early gestational exposure to moderate concentrations of ethanol alters adult behaviour in C57BL/6J mice. Behav. Brain Res. 252 (2013), 326–333, 10.1016/j.bbr.2013.06.003.
Hausknecht, K., Haj-Dahmane, S., Shen, R.-Y., Prenatal stress exposure increases the excitation of dopamine neurons in the Ventral Tegmental Area and alters their responses to psychostimulants. Neuropsychopharmacology 38:2 (2013), 293–301, 10.1038/npp.2012.168.
Bustamante, C., Bilbao, P., Contreras, W., Martínez, M., Mendoza, A., Reyes, Á et al. Effects of prenatal stress and exercise on dentate granule cells maturation and spatial memory in adolescent mice. Int. J. Dev. Neurosci. 28:7 (2010), 605–609, 10.1016/j.ijdevneu.2010.07.229.
Bustamante, C., Henríquez, R., Medina, F., Reinoso, C., Vargas, R., Pascual, R., Maternal exercise during pregnancy ameliorates the postnatal neuronal impairments induced by prenatal restraint stress in mice. Int. J. Develop. Neurosci. 31:4 (2013), 267–273, 10.1016/j.ijdevneu.2013.02.007.
Greenwood, B.N., Foley, T.E., Le, T.V., Strong, P.V., Loughridge, A.B., Day, H.E.W., Fleshner, M., Long-term voluntary wheel running is rewarding and produces plasticity in the mesolimbic reward pathway. Behav. Brain Res. 217:2 (2011), 354–362, 10.1016/j.bbr.2010.11.005.
Champagne, F.A., Meaney, M.J., Stress during gestation alters postpartum maternal care and the development of the offspring in a rodent model. Biol. Psychiatry 59:12 (2006), 1227–1235, 10.1016/j.biopsych.2005.10.016.
Zhou, Y., Zhao, M., Zhou, C., Li, R., Sex differences in drug addiction and response to exercise intervention: from human to animal studies. Front. Neuroendocrinol. 40 (2016), 24–41, 10.1016/j.yfrne.2015.07.001.
Maruoka, T., Kodomari, I., Yamauchi, R., Wada, E., Wada, K., Maternal enrichment affects prenatal hippocampal proliferation and open-field behaviors in female offspring mice. Neurosci. Lett. 454:1 (2009), 28–32, 10.1016/j.neulet.2009.02.052.
Sciolino, N.R., Holmes, P.V., Exercise offers anxiolytic potential: A role for stress and brain noradrenergic-galaninergic mechanisms. Neurosci. Biobehav. Rev. 36:9 (2012), 1965–1984, 10.1016/j.neubiorev.2012.06.005.
Thomas, M.J., Kalivas, P.W., Shaham, Y., Neuroplasticity in the mesolimbic dopamine system and cocaine addiction: neuroplasticity and cocaine addiction. Br. J. Pharmacol. 154:2 (2009), 327–342, 10.1038/bjp.2008.77.
de Jong, I.E.M., Steenbergen, P.J., de Kloet, E.R., Behavioral sensitization to cocaine: cooperation between glucocorticoids and epinephrine. Psychopharmacology 204:4 (2009), 693–703, 10.1007/s00213-009-1498-3.
Tirelli, E., Laviola, G., Adriani, W., Ontogenesis of behavioral sensitization and conditioned place preference induced by psychostimulants in laboratory rodents. Neurosci. Biobehav. Rev. 27:1 (2003), 163–178, 10.1016/S0149-7634(03)00018-6.