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Erschienen in: Brain Structure and Function 1/2016

01.01.2016 | Original Article

Repeated administration of a synthetic cannabinoid receptor agonist differentially affects cortical and accumbal neuronal morphology in adolescent and adult rats

verfasst von: A. F. Carvalho, B. A. S. Reyes, F. Ramalhosa, N. Sousa, E. J. Van Bockstaele

Erschienen in: Brain Structure and Function | Ausgabe 1/2016

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Abstract

Recent studies demonstrate a differential trajectory for cannabinoid receptor expression in cortical and sub-cortical brain areas across postnatal development. In the present study, we sought to investigate whether chronic systemic exposure to a synthetic cannabinoid receptor agonist causes morphological changes in the structure of dendrites and dendritic spines in adolescent and adult pyramidal neurons in the medial prefrontal cortex (mPFC) and medium spiny neurons (MSN) in the nucleus accumbens (Acb). Following systemic administration of WIN 55,212-2 in adolescent (PN 37–40) and adult (P55–60) male rats, the neuronal architecture of pyramidal neurons and MSN was assessed using Golgi–Cox staining. While no structural changes were observed in WIN 55,212-2-treated adolescent subjects compared to control, exposure to WIN 55,212-2 significantly increased dendritic length, spine density and the number of dendritic branches in pyramidal neurons in the mPFC of adult subjects when compared to control and adolescent subjects. In the Acb, WIN 55,212-2 exposure significantly decreased dendritic length and number of branches in adult rat subjects while no changes were observed in the adolescent groups. In contrast, spine density was significantly decreased in both the adult and adolescent groups in the Acb. To determine whether regional developmental morphological changes translated into behavioral differences, WIN 55,212-2-induced aversion was evaluated in both groups using a conditioned place preference paradigm. In adult rats, WIN 55,212-2 administration readily induced conditioned place aversion as previously described. In contrast, adolescent rats did not exhibit aversion following WIN 55,212-2 exposure in the behavioral paradigm. The present results show that synthetic cannabinoid administration differentially impacts cortical and sub-cortical neuronal morphology in adult compared to adolescent subjects. Such differences may underlie the disparate development effects of cannabinoids on behavior.
Literatur
Zurück zum Zitat Anthony JC, Petronis KR (1991) Epidemiologic evidence on suspected associations between cocaine use and psychiatric disturbances. NIDA Res Monogr 110:189–210PubMed Anthony JC, Petronis KR (1991) Epidemiologic evidence on suspected associations between cocaine use and psychiatric disturbances. NIDA Res Monogr 110:189–210PubMed
Zurück zum Zitat Baird B, Smallwood J, Gorgolewski KJ, Margulies DS (2013) Medial and lateral networks in anterior prefrontal cortex support metacognitive ability for memory and perception. J Neurosci 33(42):16657–16665PubMedCrossRef Baird B, Smallwood J, Gorgolewski KJ, Margulies DS (2013) Medial and lateral networks in anterior prefrontal cortex support metacognitive ability for memory and perception. J Neurosci 33(42):16657–16665PubMedCrossRef
Zurück zum Zitat Bardo MT, Bevins RA (2000) Conditioned place preference: what does it add to our preclinical understanding of drug reward? Psychopharmacology 153(1):31–43PubMedCrossRef Bardo MT, Bevins RA (2000) Conditioned place preference: what does it add to our preclinical understanding of drug reward? Psychopharmacology 153(1):31–43PubMedCrossRef
Zurück zum Zitat Bardo MT, Cain ME, Bylica KE (2006) Effect of amphetamine on response inhibition in rats showing high or low response to novelty. Pharmacol Biochem Behav 85(1):98–104PubMedCrossRef Bardo MT, Cain ME, Bylica KE (2006) Effect of amphetamine on response inhibition in rats showing high or low response to novelty. Pharmacol Biochem Behav 85(1):98–104PubMedCrossRef
Zurück zum Zitat Belleau ML, Warren RA (2000) Postnatal development of electrophysiological properties of nucleus accumbens neurons. J Neurophysiol 84(5):2204–2216PubMed Belleau ML, Warren RA (2000) Postnatal development of electrophysiological properties of nucleus accumbens neurons. J Neurophysiol 84(5):2204–2216PubMed
Zurück zum Zitat Biscaia M, Fernandez B, Higuera-Matas A, Miguens M, Viveros MP, Garcia-Lecumberri C, Ambrosio E (2008) Sex-dependent effects of periadolescent exposure to the cannabinoid agonist CP-55,940 on morphine self-administration behaviour and the endogenous opioid system. Neuropharmacology 54(5):863–873PubMedCrossRef Biscaia M, Fernandez B, Higuera-Matas A, Miguens M, Viveros MP, Garcia-Lecumberri C, Ambrosio E (2008) Sex-dependent effects of periadolescent exposure to the cannabinoid agonist CP-55,940 on morphine self-administration behaviour and the endogenous opioid system. Neuropharmacology 54(5):863–873PubMedCrossRef
Zurück zum Zitat Bodor AL, Katona I, Nyiri G, Mackie K, Ledent C, Hajos N, Freund TF (2005) Endocannabinoid signaling in rat somatosensory cortex: laminar differences and involvement of specific interneuron types. J Neurosci 25(29):6845–6856PubMedCrossRef Bodor AL, Katona I, Nyiri G, Mackie K, Ledent C, Hajos N, Freund TF (2005) Endocannabinoid signaling in rat somatosensory cortex: laminar differences and involvement of specific interneuron types. J Neurosci 25(29):6845–6856PubMedCrossRef
Zurück zum Zitat Broadwater M, Varlinskaya EI, Spear LP (2013) Effects of voluntary access to sweetened ethanol during adolescence on intake in adulthood. Alcohol Clin Exp Res 37(6):1048–1055PubMedCentralPubMedCrossRef Broadwater M, Varlinskaya EI, Spear LP (2013) Effects of voluntary access to sweetened ethanol during adolescence on intake in adulthood. Alcohol Clin Exp Res 37(6):1048–1055PubMedCentralPubMedCrossRef
Zurück zum Zitat Bunge SA, Wright SB (2007) Neurodevelopmental changes in working memory and cognitive control. Cur Opinion Neurobiol 17(2):243–250CrossRef Bunge SA, Wright SB (2007) Neurodevelopmental changes in working memory and cognitive control. Cur Opinion Neurobiol 17(2):243–250CrossRef
Zurück zum Zitat Cagni P, Barros M (2013) Cannabinoid type 1 receptor ligands WIN 55,212–2 and AM 251 alter anxiety-like behaviors of marmoset monkeys in an open-field test. Behav Brain Res 240:91–94PubMedCrossRef Cagni P, Barros M (2013) Cannabinoid type 1 receptor ligands WIN 55,212–2 and AM 251 alter anxiety-like behaviors of marmoset monkeys in an open-field test. Behav Brain Res 240:91–94PubMedCrossRef
Zurück zum Zitat Cain ME, Dotson WF, Bardo MT (2006) Individual differences in the effect of novel environmental stimuli prior to amphetamine self-administration in rats (Rattus norvegicus). Exp Clin Psychopharmacol 14(3):389–401PubMedCrossRef Cain ME, Dotson WF, Bardo MT (2006) Individual differences in the effect of novel environmental stimuli prior to amphetamine self-administration in rats (Rattus norvegicus). Exp Clin Psychopharmacol 14(3):389–401PubMedCrossRef
Zurück zum Zitat Cajal S (1995) Histology of the nervous system of man and vertebrates. Oxford University Press, New York Cajal S (1995) Histology of the nervous system of man and vertebrates. Oxford University Press, New York
Zurück zum Zitat Carlezon WA Jr, Thomas MJ (2009) Biological substrates of reward and aversion: a nucleus accumbens activity hypothesis. Neuropharmacology 56(Suppl 1):122–132PubMedCentralPubMedCrossRef Carlezon WA Jr, Thomas MJ (2009) Biological substrates of reward and aversion: a nucleus accumbens activity hypothesis. Neuropharmacology 56(Suppl 1):122–132PubMedCentralPubMedCrossRef
Zurück zum Zitat Carvalho AF, Van Bockstaele EJ (2011) Direct intra-accumbal infusion of a beta-adrenergic receptor antagonist abolishes WIN 55,212-2-induced aversion. Neurosci Lett 500(1):82–85PubMedCentralPubMedCrossRef Carvalho AF, Van Bockstaele EJ (2011) Direct intra-accumbal infusion of a beta-adrenergic receptor antagonist abolishes WIN 55,212-2-induced aversion. Neurosci Lett 500(1):82–85PubMedCentralPubMedCrossRef
Zurück zum Zitat Carvalho AF, Reyes AR, Sterling RC, Unterwald E, Van Bockstaele EJ (2010) Contribution of limbic norepinephrine to cannabinoid-induced aversion. Psychopharmacology 211(4):479–491PubMedCentralPubMedCrossRef Carvalho AF, Reyes AR, Sterling RC, Unterwald E, Van Bockstaele EJ (2010) Contribution of limbic norepinephrine to cannabinoid-induced aversion. Psychopharmacology 211(4):479–491PubMedCentralPubMedCrossRef
Zurück zum Zitat Casey BJ, Giedd JN, Thomas KM (2000) Structural and functional brain development and its relation to cognitive development. Biol Psychol 54(1–3):241–257PubMedCrossRef Casey BJ, Giedd JN, Thomas KM (2000) Structural and functional brain development and its relation to cognitive development. Biol Psychol 54(1–3):241–257PubMedCrossRef
Zurück zum Zitat Caspi A, Moffitt TE, Cannon M, McClay J, Murray R, Harrington H, Taylor A, Arseneault L, Williams B, Braithwaite A, Poulton R, Craig IW (2005) Moderation of the effect of adolescent-onset cannabis use on adult psychosis by a functional polymorphism in the catechol-O-methyltransferase gene: longitudinal evidence of a gene × environment interaction. Biol Psychiatry 57(10):1117–1127PubMedCrossRef Caspi A, Moffitt TE, Cannon M, McClay J, Murray R, Harrington H, Taylor A, Arseneault L, Williams B, Braithwaite A, Poulton R, Craig IW (2005) Moderation of the effect of adolescent-onset cannabis use on adult psychosis by a functional polymorphism in the catechol-O-methyltransferase gene: longitudinal evidence of a gene × environment interaction. Biol Psychiatry 57(10):1117–1127PubMedCrossRef
Zurück zum Zitat Castellanos D, Singh S, Thornton G, Avila M, Moreno A (2011) Synthetic cannabinoid use: a case series of adolescents. J Adolesc Health 49(4):347–349PubMedCrossRef Castellanos D, Singh S, Thornton G, Avila M, Moreno A (2011) Synthetic cannabinoid use: a case series of adolescents. J Adolesc Health 49(4):347–349PubMedCrossRef
Zurück zum Zitat Cerqueira JJ, Taipa R, Uylings HB, Almeida FO, Sousa N (2007) Specific configuration of dendritic degeneration in pyramidal neurons of the medial prefrontal cortex induced by differing corticosteroid regimens. Cereb Cortex 17(9):1998–2006PubMedCrossRef Cerqueira JJ, Taipa R, Uylings HB, Almeida FO, Sousa N (2007) Specific configuration of dendritic degeneration in pyramidal neurons of the medial prefrontal cortex induced by differing corticosteroid regimens. Cereb Cortex 17(9):1998–2006PubMedCrossRef
Zurück zum Zitat Chambers RA, Taylor JR, Potenza MN (2003) Developmental neurocircuitry of motivation in adolescence: a critical period of addiction vulnerability. Am J Psychiatry 160(6):1041–1052PubMedCentralPubMedCrossRef Chambers RA, Taylor JR, Potenza MN (2003) Developmental neurocircuitry of motivation in adolescence: a critical period of addiction vulnerability. Am J Psychiatry 160(6):1041–1052PubMedCentralPubMedCrossRef
Zurück zum Zitat Clark LR, Cools R, Robbins TW (2004) The neuropsychology of ventral prefrontal cortex: decision-making and reversal learning. Brain Cogn 55(1):41–53PubMedCrossRef Clark LR, Cools R, Robbins TW (2004) The neuropsychology of ventral prefrontal cortex: decision-making and reversal learning. Brain Cogn 55(1):41–53PubMedCrossRef
Zurück zum Zitat Crowley TJ, Macdonald MJ, Whitmore EA, Mikulich SK (1998) Cannabis dependence, withdrawal, and reinforcing effects among adolescents with conduct symptoms and substance use disorders. Drug Alcohol Depend 50(1):27–37PubMedCrossRef Crowley TJ, Macdonald MJ, Whitmore EA, Mikulich SK (1998) Cannabis dependence, withdrawal, and reinforcing effects among adolescents with conduct symptoms and substance use disorders. Drug Alcohol Depend 50(1):27–37PubMedCrossRef
Zurück zum Zitat Cullen TJ, Walker MA, Eastwood SL, Esiri MM, Harrison PJ, Crow TJ (2006) Anomalies of asymmetry of pyramidal cell density and structure in dorsolateral prefrontal cortex in schizophrenia. Br J Psychiatry 188:26–31PubMedCrossRef Cullen TJ, Walker MA, Eastwood SL, Esiri MM, Harrison PJ, Crow TJ (2006) Anomalies of asymmetry of pyramidal cell density and structure in dorsolateral prefrontal cortex in schizophrenia. Br J Psychiatry 188:26–31PubMedCrossRef
Zurück zum Zitat Cunningham CL, Gremel CM (2006) Proximal ethanol pretreatment interferes with acquisition of ethanol-induced conditioned place preference. Pharmacol Biochem Behav 85(3):612–619PubMedCentralPubMedCrossRef Cunningham CL, Gremel CM (2006) Proximal ethanol pretreatment interferes with acquisition of ethanol-induced conditioned place preference. Pharmacol Biochem Behav 85(3):612–619PubMedCentralPubMedCrossRef
Zurück zum Zitat Cunningham CL, Gremel CM, Groblewski PA (2006) Drug-induced conditioned place preference and aversion in mice. Nat Protoc 1(4):1662–1670PubMedCrossRef Cunningham CL, Gremel CM, Groblewski PA (2006) Drug-induced conditioned place preference and aversion in mice. Nat Protoc 1(4):1662–1670PubMedCrossRef
Zurück zum Zitat Dalton VS, Wang H, Zavitsanou K (2009) HU210-induced downregulation in cannabinoid CB1 receptor binding strongly correlates with body weight loss in the adult rat. Neurochem Res 34(7):1343–1353PubMedCrossRef Dalton VS, Wang H, Zavitsanou K (2009) HU210-induced downregulation in cannabinoid CB1 receptor binding strongly correlates with body weight loss in the adult rat. Neurochem Res 34(7):1343–1353PubMedCrossRef
Zurück zum Zitat Dalton VS, Wang H, Zavitsanou K (2010) Cannabinoid effects on CB1 receptor density in the adolescent brain: an autoradiographic study using the synthetic cannabinoid HU210. Synapse 64(11):845–854PubMedCrossRef Dalton VS, Wang H, Zavitsanou K (2010) Cannabinoid effects on CB1 receptor density in the adolescent brain: an autoradiographic study using the synthetic cannabinoid HU210. Synapse 64(11):845–854PubMedCrossRef
Zurück zum Zitat Davidson RJ (2002) Anxiety and affective style: role of prefrontal cortex and amygdala. Biol Psychiatry 51(1):68–80PubMedCrossRef Davidson RJ (2002) Anxiety and affective style: role of prefrontal cortex and amygdala. Biol Psychiatry 51(1):68–80PubMedCrossRef
Zurück zum Zitat De Bellis MD, Keshavan MS, Beers SR, Hall J, Frustaci K, Masalehdan A, Noll J, Boring AM (2001) Sex differences in brain maturation during childhood and adolescence. Cereb Cortex 11:552–557PubMedCrossRef De Bellis MD, Keshavan MS, Beers SR, Hall J, Frustaci K, Masalehdan A, Noll J, Boring AM (2001) Sex differences in brain maturation during childhood and adolescence. Cereb Cortex 11:552–557PubMedCrossRef
Zurück zum Zitat de Fonseca FR, Schneider M (2008) The endogenous cannabinoid system and drug addiction: 20 years after the discovery of the CB1 receptor. Addict Biol 13:143–146PubMedCrossRef de Fonseca FR, Schneider M (2008) The endogenous cannabinoid system and drug addiction: 20 years after the discovery of the CB1 receptor. Addict Biol 13:143–146PubMedCrossRef
Zurück zum Zitat D’Souza DC, Perry E, MacDougall L, Ammerman Y, Cooper T, Wu YT, Braley G, Gueorguieva R, Krystal JH (2004) The psychotomimetic effects of intravenous delta-9-tetrahydrocannabinol in healthy individuals: implications for psychosis. Neuropsychopharmacology 29(8):1558–1572PubMedCrossRef D’Souza DC, Perry E, MacDougall L, Ammerman Y, Cooper T, Wu YT, Braley G, Gueorguieva R, Krystal JH (2004) The psychotomimetic effects of intravenous delta-9-tetrahydrocannabinol in healthy individuals: implications for psychosis. Neuropsychopharmacology 29(8):1558–1572PubMedCrossRef
Zurück zum Zitat D’Souza DC, Abi-Saab WM, Madonick S, Forselius-Bielen K, Doersch A, Braley G, Gueorguieva R, Cooper TB, Krystal JH (2005) Delta-9-tetrahydrocannabinol effects in schizophrenia: implications for cognition, psychosis, and addiction. Biol Psychiatry 57(6):594–608PubMedCrossRef D’Souza DC, Abi-Saab WM, Madonick S, Forselius-Bielen K, Doersch A, Braley G, Gueorguieva R, Cooper TB, Krystal JH (2005) Delta-9-tetrahydrocannabinol effects in schizophrenia: implications for cognition, psychosis, and addiction. Biol Psychiatry 57(6):594–608PubMedCrossRef
Zurück zum Zitat Dumitriu D, Laplant Q, Grossman YS, Dias C, Janssen WG, Russo SJ, Morrison JH, Nestler EJ (2012) Subregional, dendritic compartment, and spine subtype specificity in cocaine regulation of dendritic spines in the nucleus accumbens. J Neurosci 32(20):6957–6966PubMedCentralPubMedCrossRef Dumitriu D, Laplant Q, Grossman YS, Dias C, Janssen WG, Russo SJ, Morrison JH, Nestler EJ (2012) Subregional, dendritic compartment, and spine subtype specificity in cocaine regulation of dendritic spines in the nucleus accumbens. J Neurosci 32(20):6957–6966PubMedCentralPubMedCrossRef
Zurück zum Zitat Ellgren M, Artmann A, Tkalych O, Gupta A, Hansen HS, Hansen SH, Devi LA, Hurd YL (2008) Dynamic changes of the endogenous cannabinoid and opioid mesocorticolimbic systems during adolescence: THC effects. Eur Neuropsychopharmacol 18(11):826–834PubMedCentralPubMedCrossRef Ellgren M, Artmann A, Tkalych O, Gupta A, Hansen HS, Hansen SH, Devi LA, Hurd YL (2008) Dynamic changes of the endogenous cannabinoid and opioid mesocorticolimbic systems during adolescence: THC effects. Eur Neuropsychopharmacol 18(11):826–834PubMedCentralPubMedCrossRef
Zurück zum Zitat Falowski SM, Sharan A, Reyes BA, Sikkema C, Szot P, Van Bockstaele EJ (2011) An evaluation of neuroplasticity and behavior after deep brain stimulation of the nucleus accumbens in an animal model of depression. Neurosurgery 69:1281–1290PubMedCentralPubMedCrossRef Falowski SM, Sharan A, Reyes BA, Sikkema C, Szot P, Van Bockstaele EJ (2011) An evaluation of neuroplasticity and behavior after deep brain stimulation of the nucleus accumbens in an animal model of depression. Neurosurgery 69:1281–1290PubMedCentralPubMedCrossRef
Zurück zum Zitat Fernández-Espejo E (2013) How does the nucleus accumbens function? Revista de Neurologia 30(9):845–849 Fernández-Espejo E (2013) How does the nucleus accumbens function? Revista de Neurologia 30(9):845–849
Zurück zum Zitat Fortin DA, Levine ES (2007) Differential effects of endocannabinoids on glutamatergic and GABAergic inputs to layer 5 pyramidal neurons. Cereb Cortex 17(1):163–174PubMedCrossRef Fortin DA, Levine ES (2007) Differential effects of endocannabinoids on glutamatergic and GABAergic inputs to layer 5 pyramidal neurons. Cereb Cortex 17(1):163–174PubMedCrossRef
Zurück zum Zitat Fox KM, Sterling RC, Van Bockstaele EJ (2009) Cannabinoids and novelty investigation: influence of age and duration of exposure. Behav Brain Res 196(2):248–253PubMedCentralPubMedCrossRef Fox KM, Sterling RC, Van Bockstaele EJ (2009) Cannabinoids and novelty investigation: influence of age and duration of exposure. Behav Brain Res 196(2):248–253PubMedCentralPubMedCrossRef
Zurück zum Zitat French SJ, Totterdell D (2002) Hippocampal and prefrontal cortical inputs monosynaptically converge with individual projection neurons of the nucleus. J Comp Neurol 446(2):151–165PubMedCrossRef French SJ, Totterdell D (2002) Hippocampal and prefrontal cortical inputs monosynaptically converge with individual projection neurons of the nucleus. J Comp Neurol 446(2):151–165PubMedCrossRef
Zurück zum Zitat Grant BF, Dawson DA (1997) Age at onset of alcohol use and its association with DSM-IV alcohol abuse and dependence: results from the National Longitudinal Alcohol Epidemiologic Survey. J Subst Abuse 9:103–110PubMedCrossRef Grant BF, Dawson DA (1997) Age at onset of alcohol use and its association with DSM-IV alcohol abuse and dependence: results from the National Longitudinal Alcohol Epidemiologic Survey. J Subst Abuse 9:103–110PubMedCrossRef
Zurück zum Zitat Heng L, Beverley JA, Steiner H, Tseng KY (2011) Differential developmental trajectories for CB1 cannabinoid receptor expression in limbic/associative and sensorimotor cortical areas. Synapse 65(4):278–286PubMedCentralPubMedCrossRef Heng L, Beverley JA, Steiner H, Tseng KY (2011) Differential developmental trajectories for CB1 cannabinoid receptor expression in limbic/associative and sensorimotor cortical areas. Synapse 65(4):278–286PubMedCentralPubMedCrossRef
Zurück zum Zitat Henquet C, Murray R, Linszen D, van Os J (2005) The environment and schizophrenia: the role of cannabis use. Schizophr Bull 31(3):608–612PubMedCrossRef Henquet C, Murray R, Linszen D, van Os J (2005) The environment and schizophrenia: the role of cannabis use. Schizophr Bull 31(3):608–612PubMedCrossRef
Zurück zum Zitat Herkenham M, Lynn AB, Johnson MR, Melvin LS, de Costa BR, Rice KC (1991) Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J Neurosci 11(2):563–583PubMed Herkenham M, Lynn AB, Johnson MR, Melvin LS, de Costa BR, Rice KC (1991) Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J Neurosci 11(2):563–583PubMed
Zurück zum Zitat Hughes RN (1968) Behaviour of male and female rats with free choice of two environments differing in novelty. Anim Behav 16(1):92–96PubMedCrossRef Hughes RN (1968) Behaviour of male and female rats with free choice of two environments differing in novelty. Anim Behav 16(1):92–96PubMedCrossRef
Zurück zum Zitat Hurd YL, Michaelides M, Miller ML, Jutras-Aswad D (2014) Trajectory of adolescent cannabis use on addiction vulnerability. Neuropharmacology 76(Pt B):416–424 Hurd YL, Michaelides M, Miller ML, Jutras-Aswad D (2014) Trajectory of adolescent cannabis use on addiction vulnerability. Neuropharmacology 76(Pt B):416–424
Zurück zum Zitat Jentsch JD, Andrusiak E, Tran A, Bowers MB Jr, Roth RH (1997) Delta 9-tetrahydrocannabinol increases prefrontal cortical catecholaminergic utilization and impairs spatial working memory in the rat: blockade of dopaminergic effects with HA966. Neuropsychopharmacology 16:426–432PubMedCrossRef Jentsch JD, Andrusiak E, Tran A, Bowers MB Jr, Roth RH (1997) Delta 9-tetrahydrocannabinol increases prefrontal cortical catecholaminergic utilization and impairs spatial working memory in the rat: blockade of dopaminergic effects with HA966. Neuropsychopharmacology 16:426–432PubMedCrossRef
Zurück zum Zitat Kandel D, Chen K, Warner LA, Kessler RC, Grant B (1997) Prevalence and demographic correlates of symptoms of last year dependence on alcohol, nicotine, marijuana and cocaine in the U.S. population. Drug Alcohol Depend 44:11–29PubMedCrossRef Kandel D, Chen K, Warner LA, Kessler RC, Grant B (1997) Prevalence and demographic correlates of symptoms of last year dependence on alcohol, nicotine, marijuana and cocaine in the U.S. population. Drug Alcohol Depend 44:11–29PubMedCrossRef
Zurück zum Zitat Kelly BC, Wells BE, Pawson M, Leclair A, Parsons JT, Golub SA (2013) Novel psychoactive drug use among younger adults involved in US nightlife scenes. Drug Alcohol Rev 32(6):588–593PubMedCrossRef Kelly BC, Wells BE, Pawson M, Leclair A, Parsons JT, Golub SA (2013) Novel psychoactive drug use among younger adults involved in US nightlife scenes. Drug Alcohol Rev 32(6):588–593PubMedCrossRef
Zurück zum Zitat Kohn N, Eickhoff SB, Scheller M, Laird AR, Fox PT, Habel U (2014) Neural network of cognitive emotion regulation—an ALE meta-analysis and MACM analysis. NeuroImage 87:345–355PubMedCrossRef Kohn N, Eickhoff SB, Scheller M, Laird AR, Fox PT, Habel U (2014) Neural network of cognitive emotion regulation—an ALE meta-analysis and MACM analysis. NeuroImage 87:345–355PubMedCrossRef
Zurück zum Zitat Kolb B, Gorny G, Li Y, Samaha AN, Robinson TE (2003) Amphetamine or cocaine limits the ability of later experience to promote structural plasticity in the neocortex and nucleus accumbens. Proc Natl Acad Sci USA 100:10523–10528PubMedCentralPubMedCrossRef Kolb B, Gorny G, Li Y, Samaha AN, Robinson TE (2003) Amphetamine or cocaine limits the ability of later experience to promote structural plasticity in the neocortex and nucleus accumbens. Proc Natl Acad Sci USA 100:10523–10528PubMedCentralPubMedCrossRef
Zurück zum Zitat Kolb B, Gorny G, Limebeer CL, Parker LA (2006) Chronic treatment with delta-9-tetrahydrocannabinol alters the structure of neurons in the nucleus accumbens shell and medial prefrontal cortex of rats. Synapse 60(6):429–436PubMedCrossRef Kolb B, Gorny G, Limebeer CL, Parker LA (2006) Chronic treatment with delta-9-tetrahydrocannabinol alters the structure of neurons in the nucleus accumbens shell and medial prefrontal cortex of rats. Synapse 60(6):429–436PubMedCrossRef
Zurück zum Zitat Koss WA, Belden CE, Hristov AD, Juraska JM (2014) Dendritic remodeling in the adolescent medial prefrontal cortex and the basolateral amygdala of male and female rats. Synapse 68:61–72PubMedCrossRef Koss WA, Belden CE, Hristov AD, Juraska JM (2014) Dendritic remodeling in the adolescent medial prefrontal cortex and the basolateral amygdala of male and female rats. Synapse 68:61–72PubMedCrossRef
Zurück zum Zitat Li Y, Kolb B, Robinson TE (2003) The location of persistent amphetamine-induced changes in the density of dendritic spines on medium spiny neurons in the nucleus accumbens and caudate-putamen. Neuropsychopharmacology 28:1082–1085PubMedCrossRef Li Y, Kolb B, Robinson TE (2003) The location of persistent amphetamine-induced changes in the density of dendritic spines on medium spiny neurons in the nucleus accumbens and caudate-putamen. Neuropsychopharmacology 28:1082–1085PubMedCrossRef
Zurück zum Zitat Li Y, Acerbo MJ, Robinson TE (2004) The induction of behavioural sensitization is associated with cocaine-induced structural plasticity in the core (but not shell) of the nucleus accumbens. Eur J Neurosci 20(6):1647–1654PubMedCrossRef Li Y, Acerbo MJ, Robinson TE (2004) The induction of behavioural sensitization is associated with cocaine-induced structural plasticity in the core (but not shell) of the nucleus accumbens. Eur J Neurosci 20(6):1647–1654PubMedCrossRef
Zurück zum Zitat Libersat F (2005) Maturation of dendritic architecture: lessons from insect identified neurons. J Neurobiol 64(1):11–23PubMedCrossRef Libersat F (2005) Maturation of dendritic architecture: lessons from insect identified neurons. J Neurobiol 64(1):11–23PubMedCrossRef
Zurück zum Zitat Lu D, He L, Xiang W, Ai WM, Cao Y, Wang XS, Pan A, Luo XG, Li Z, Yan XX (2013) Somal and dendritic development of human CA3 pyramidal neurons from midgestation to middle childhood: a quantitative Golgi study. Anat Rec (Hoboken) 296:123–132CrossRef Lu D, He L, Xiang W, Ai WM, Cao Y, Wang XS, Pan A, Luo XG, Li Z, Yan XX (2013) Somal and dendritic development of human CA3 pyramidal neurons from midgestation to middle childhood: a quantitative Golgi study. Anat Rec (Hoboken) 296:123–132CrossRef
Zurück zum Zitat Luna B, Garver KE, Urban TA, Lazar NA, Sweeney JA (2004) Maturation of cognitive processes from late childhood to adulthood. Child Dev 75(5):1357–1372PubMedCrossRef Luna B, Garver KE, Urban TA, Lazar NA, Sweeney JA (2004) Maturation of cognitive processes from late childhood to adulthood. Child Dev 75(5):1357–1372PubMedCrossRef
Zurück zum Zitat Mailleux P, Vanderhaeghen JJ (1992a) Distribution of neuronal cannabinoid receptor in the adult rat brain: a comparative receptor binding radioautography and in situ hybridization histochemistry. Neuroscience 48(3):655–668PubMedCrossRef Mailleux P, Vanderhaeghen JJ (1992a) Distribution of neuronal cannabinoid receptor in the adult rat brain: a comparative receptor binding radioautography and in situ hybridization histochemistry. Neuroscience 48(3):655–668PubMedCrossRef
Zurück zum Zitat Mailleux P, Vanderhaeghen JJ (1992b) Localization of cannabinoid receptor in the human developing and adult basal ganglia. Higher levels in the striatonigral neurons. Neurosci Lett 148(1–2):173–176PubMedCrossRef Mailleux P, Vanderhaeghen JJ (1992b) Localization of cannabinoid receptor in the human developing and adult basal ganglia. Higher levels in the striatonigral neurons. Neurosci Lett 148(1–2):173–176PubMedCrossRef
Zurück zum Zitat Matsuda LA, Bonner TI, Lolait SJ (1993) Localization of cannabinoid receptor mRNA in rat brain. J Comp Neurol 327(4):535–550PubMedCrossRef Matsuda LA, Bonner TI, Lolait SJ (1993) Localization of cannabinoid receptor mRNA in rat brain. J Comp Neurol 327(4):535–550PubMedCrossRef
Zurück zum Zitat McGuinness TM, Newell D (2012) Risky recreation: synthetic cannabinoids have dangerous effects. J Psychosoc Nurs Ment Health Serv 50(8):16–18PubMedCrossRef McGuinness TM, Newell D (2012) Risky recreation: synthetic cannabinoids have dangerous effects. J Psychosoc Nurs Ment Health Serv 50(8):16–18PubMedCrossRef
Zurück zum Zitat Moore NL, Greenleaf AL, Acheson SK, Wilson WA, Swartzwelder SH, Kuhn CM (2010) Role of cannabinoid receptor type 1 desensitization in greater tetrahydrocannabinol impairment of memory in adolescent rats. J Pharmacol Exp Ther 335(2):294–301PubMedCentralPubMedCrossRef Moore NL, Greenleaf AL, Acheson SK, Wilson WA, Swartzwelder SH, Kuhn CM (2010) Role of cannabinoid receptor type 1 desensitization in greater tetrahydrocannabinol impairment of memory in adolescent rats. J Pharmacol Exp Ther 335(2):294–301PubMedCentralPubMedCrossRef
Zurück zum Zitat Mucha RF, Herz A (1985) Motivational properties of kappa and mu opioid receptor agonists studied with place and taste preference conditioning. Psychopharmacology 86(3):274–280PubMedCrossRef Mucha RF, Herz A (1985) Motivational properties of kappa and mu opioid receptor agonists studied with place and taste preference conditioning. Psychopharmacology 86(3):274–280PubMedCrossRef
Zurück zum Zitat Mucha RF, Iversen SD (1984) Reinforcing properties of morphine and naloxone revealed by conditioned place preferences: a procedural examination. Psychopharmacology 82(3):241–247PubMedCrossRef Mucha RF, Iversen SD (1984) Reinforcing properties of morphine and naloxone revealed by conditioned place preferences: a procedural examination. Psychopharmacology 82(3):241–247PubMedCrossRef
Zurück zum Zitat Nugent AC, Milham MP, Bain EE, Mah L, Cannon DM, Marrett S, Zarate CA, Pine DS, Price JL, Drevets WC (2006) Cortical abnormalities in bipolar disorder investigated with MRI and voxel-based morphometry. NeuroImage 30:485–497PubMedCrossRef Nugent AC, Milham MP, Bain EE, Mah L, Cannon DM, Marrett S, Zarate CA, Pine DS, Price JL, Drevets WC (2006) Cortical abnormalities in bipolar disorder investigated with MRI and voxel-based morphometry. NeuroImage 30:485–497PubMedCrossRef
Zurück zum Zitat Oropeza VC, Page ME, Van Bockstaele EJ (2005) Systemic administration of WIN 55,212-2 increases norepinephrine release in the rat frontal cortex. Brain Res 1046(1–2):45–54PubMedCrossRef Oropeza VC, Page ME, Van Bockstaele EJ (2005) Systemic administration of WIN 55,212-2 increases norepinephrine release in the rat frontal cortex. Brain Res 1046(1–2):45–54PubMedCrossRef
Zurück zum Zitat O'Shea M, McGregor IS, Mallet PE (2006) Repeated cannabinoid exposure during perinatal, adolescent or early adult ages produces similar longlasting deficits in object recognition and reduced social interaction in rats. J Psychopharmacol 20:611–621PubMedCrossRef O'Shea M, McGregor IS, Mallet PE (2006) Repeated cannabinoid exposure during perinatal, adolescent or early adult ages produces similar longlasting deficits in object recognition and reduced social interaction in rats. J Psychopharmacol 20:611–621PubMedCrossRef
Zurück zum Zitat O'Shea M, Singh ME, McGregor IS, Mallet PE (2004) Chronic cannabinoid exposure produces lasting memory impairment and increased anxiety in adolescent but not adult rats. J Psychopharmacol 18:502–508PubMedCrossRef O'Shea M, Singh ME, McGregor IS, Mallet PE (2004) Chronic cannabinoid exposure produces lasting memory impairment and increased anxiety in adolescent but not adult rats. J Psychopharmacol 18:502–508PubMedCrossRef
Zurück zum Zitat Page ME, Oropeza VC, Sparks SE, Qian Y, Menko AS, Van Bockstaele EJ (2007) Repeated cannabinoid administration increases indices of noradrenergic activity in rats. Pharmacol Biochem Behav 86(1):162–168PubMedCentralPubMedCrossRef Page ME, Oropeza VC, Sparks SE, Qian Y, Menko AS, Van Bockstaele EJ (2007) Repeated cannabinoid administration increases indices of noradrenergic activity in rats. Pharmacol Biochem Behav 86(1):162–168PubMedCentralPubMedCrossRef
Zurück zum Zitat Page ME, Oropeza VC, Van Bockstaele EJ (2008) Local administration of a cannabinoid agonist alters norepinephrine efflux in the rat frontal cortex. Neurosci Lett 431(1):1–5PubMedCentralPubMedCrossRef Page ME, Oropeza VC, Van Bockstaele EJ (2008) Local administration of a cannabinoid agonist alters norepinephrine efflux in the rat frontal cortex. Neurosci Lett 431(1):1–5PubMedCentralPubMedCrossRef
Zurück zum Zitat Parker LA (1992) Place conditioning in a three- or four-choice apparatus: role of stimulus novelty in drug-induced place conditioning. Behav Neurosci 106(2):294–306PubMedCrossRef Parker LA (1992) Place conditioning in a three- or four-choice apparatus: role of stimulus novelty in drug-induced place conditioning. Behav Neurosci 106(2):294–306PubMedCrossRef
Zurück zum Zitat Pickel VM, Towle AC, Joh TH, Chan J (1988) Gamma-aminobutyric acid in the medial rat nucleus accumbens: ultrastructural localization in neurons receiving monosynaptic input from catecholaminergic afferents. J Comp Neurol 272(1):1–14PubMedCrossRef Pickel VM, Towle AC, Joh TH, Chan J (1988) Gamma-aminobutyric acid in the medial rat nucleus accumbens: ultrastructural localization in neurons receiving monosynaptic input from catecholaminergic afferents. J Comp Neurol 272(1):1–14PubMedCrossRef
Zurück zum Zitat Philpot RM, Badanich KA, Kirstein CL (2003) Place conditioning: age-related changes in the rewarding and aversive effects of alcohol. Alcohol Clin Exp Res 27:593–599PubMedCrossRef Philpot RM, Badanich KA, Kirstein CL (2003) Place conditioning: age-related changes in the rewarding and aversive effects of alcohol. Alcohol Clin Exp Res 27:593–599PubMedCrossRef
Zurück zum Zitat Piomelli D (2003) The molecular logic of endocannabinoid signalling. Nat Rev Neurosci 4:873–884PubMedCrossRef Piomelli D (2003) The molecular logic of endocannabinoid signalling. Nat Rev Neurosci 4:873–884PubMedCrossRef
Zurück zum Zitat Quinn HR, Matsumoto I, Callaghan PD, Long LE, Arnold JC, Gunasekaran N, Thompson MR, Dawson B, Mallet PE, Kashem MA, Matsuda-Matsumoto H, Iwazaki T, McGregot IS (2008) Adolescent rats find repeated delta(9)-THC less aversive than adult rats but display greater residual cognitive deficits and changes in hippocampal protein expression following exposure. Neuropsychopharmacology 33(5):1113–1126PubMedCrossRef Quinn HR, Matsumoto I, Callaghan PD, Long LE, Arnold JC, Gunasekaran N, Thompson MR, Dawson B, Mallet PE, Kashem MA, Matsuda-Matsumoto H, Iwazaki T, McGregot IS (2008) Adolescent rats find repeated delta(9)-THC less aversive than adult rats but display greater residual cognitive deficits and changes in hippocampal protein expression following exposure. Neuropsychopharmacology 33(5):1113–1126PubMedCrossRef
Zurück zum Zitat Realini N, Rubino T, Parolaro D (2009) Neurobiological alterations at adult age triggered by adolescent exposure to cannabinoids. Pharmacol Res 60(2):132–138PubMedCrossRef Realini N, Rubino T, Parolaro D (2009) Neurobiological alterations at adult age triggered by adolescent exposure to cannabinoids. Pharmacol Res 60(2):132–138PubMedCrossRef
Zurück zum Zitat Renard J, Krebs MO, Jay TM, Le Pen G (2013) Long-term cognitive impairments induced by chronic cannabinoid exposure during adolescence in rats: a strain comparison. Psychopharmacology 225(4):781–790PubMedCrossRef Renard J, Krebs MO, Jay TM, Le Pen G (2013) Long-term cognitive impairments induced by chronic cannabinoid exposure during adolescence in rats: a strain comparison. Psychopharmacology 225(4):781–790PubMedCrossRef
Zurück zum Zitat Reyes BA, Rosario JC, Piana PM, Van Bockstaele EJ (2009) Cannabinoid modulation of cortical adrenergic receptors and transporters. J Neurosci Res 87(16):3671–3678PubMedCentralPubMedCrossRef Reyes BA, Rosario JC, Piana PM, Van Bockstaele EJ (2009) Cannabinoid modulation of cortical adrenergic receptors and transporters. J Neurosci Res 87(16):3671–3678PubMedCentralPubMedCrossRef
Zurück zum Zitat Robinson TE, Kolb B (2004) Structural plasticity associated with exposure to drugs of abuse. Neuropharmacology 47(Suppl 1):33–46PubMedCrossRef Robinson TE, Kolb B (2004) Structural plasticity associated with exposure to drugs of abuse. Neuropharmacology 47(Suppl 1):33–46PubMedCrossRef
Zurück zum Zitat Rodríguez de Fonseca F, Ramos JA, Bonnin A, Fernández-Ruiz JJ (1993) Presence of cannabinoid binding sites in the brain from early postnatal ages. NeuroReport 4(2):135–138PubMedCrossRef Rodríguez de Fonseca F, Ramos JA, Bonnin A, Fernández-Ruiz JJ (1993) Presence of cannabinoid binding sites in the brain from early postnatal ages. NeuroReport 4(2):135–138PubMedCrossRef
Zurück zum Zitat Rosenbaum CD, Carreiro SP, Babu KM (2012) Here today, gone tomorrow…and back again? A review of herbal marijuana alternatives (K2, Spice), synthetic cathinones (bath salts), kratom, Salvia divinorum, methoxetamine, and piperazines. J Med Toxicol 8(1):15–32PubMedCentralPubMedCrossRef Rosenbaum CD, Carreiro SP, Babu KM (2012) Here today, gone tomorrow…and back again? A review of herbal marijuana alternatives (K2, Spice), synthetic cathinones (bath salts), kratom, Salvia divinorum, methoxetamine, and piperazines. J Med Toxicol 8(1):15–32PubMedCentralPubMedCrossRef
Zurück zum Zitat Rubino T, Realini N, Braida D, Alberio T, Capurro V, Vigano D, Guidali C, Sala M, Fasano M, Parolaro D (2009a) The depressive phenotype induced in adult female rats by adolescent exposure to THC is associated with cognitive impairment and altered neuroplasticity in the prefrontal cortex. Neurotox Res 15(4):291–302PubMedCrossRef Rubino T, Realini N, Braida D, Alberio T, Capurro V, Vigano D, Guidali C, Sala M, Fasano M, Parolaro D (2009a) The depressive phenotype induced in adult female rats by adolescent exposure to THC is associated with cognitive impairment and altered neuroplasticity in the prefrontal cortex. Neurotox Res 15(4):291–302PubMedCrossRef
Zurück zum Zitat Rubino T, Realini N, Braida D, Guidi S, Capurro V, Vigano D, Guidali C, Pinter M, Sala M, Bartesaghi R, Parolaro D (2009b) Changes in hippocampal morphology and neuroplasticity induced by adolescent THC treatment are associated with cognitive impairment in adulthood. Hippocampus 19(8):763–772PubMedCrossRef Rubino T, Realini N, Braida D, Guidi S, Capurro V, Vigano D, Guidali C, Pinter M, Sala M, Bartesaghi R, Parolaro D (2009b) Changes in hippocampal morphology and neuroplasticity induced by adolescent THC treatment are associated with cognitive impairment in adulthood. Hippocampus 19(8):763–772PubMedCrossRef
Zurück zum Zitat Sánchez F, Gómez-Villalobos Mde J, Juarez I, Quevedo L, Flores G (2011) Dendritic morphology of neurons in medial prefrontal cortex, hippocampus, and nucleus accumbens in adult SH rats. Synapse 65(3):198–206PubMedCrossRef Sánchez F, Gómez-Villalobos Mde J, Juarez I, Quevedo L, Flores G (2011) Dendritic morphology of neurons in medial prefrontal cortex, hippocampus, and nucleus accumbens in adult SH rats. Synapse 65(3):198–206PubMedCrossRef
Zurück zum Zitat Schneider M (2008) Puberty as a highly vulnerable developmental period for the consequences of cannabis exposure. Addict Biol 13:253–263PubMedCrossRef Schneider M (2008) Puberty as a highly vulnerable developmental period for the consequences of cannabis exposure. Addict Biol 13:253–263PubMedCrossRef
Zurück zum Zitat Schneider M, Koch M (2003) Chronic pubertal, but not adult chronic cannabinoid treatment impairs sensorimotor gating, recognition memory, and the performance in a progressive ratio task in adult rats. Neuropsychopharmacology 28:1760–1769PubMedCrossRef Schneider M, Koch M (2003) Chronic pubertal, but not adult chronic cannabinoid treatment impairs sensorimotor gating, recognition memory, and the performance in a progressive ratio task in adult rats. Neuropsychopharmacology 28:1760–1769PubMedCrossRef
Zurück zum Zitat Schneider M, Drews E, Koch M (2005) Behavioral effects in adult rats of chronic prepubertal treatment with the cannabinoid receptor agonist WIN 55,212–2. Behav Pharmacol 16:447–454PubMedCrossRef Schneider M, Drews E, Koch M (2005) Behavioral effects in adult rats of chronic prepubertal treatment with the cannabinoid receptor agonist WIN 55,212–2. Behav Pharmacol 16:447–454PubMedCrossRef
Zurück zum Zitat Schneider M, Schomig E, Leweke FM (2008) Acute and chronic cannabinoid treatment differentially affects recognition memory and social behavior in pubertal and adult rats. Addict Biol 13:345–357PubMedCrossRef Schneider M, Schomig E, Leweke FM (2008) Acute and chronic cannabinoid treatment differentially affects recognition memory and social behavior in pubertal and adult rats. Addict Biol 13:345–357PubMedCrossRef
Zurück zum Zitat Schramm-Sapyta NL, Cha YM, Chaudhry S, Wilson WA, Scott Swartzwelder HS, Kuhn CM (2007) Differential anxiogenic, aversive, and locomotor effects of THC in adolescent and adult rats. Psychopharmacology 191(4):867–877PubMedCrossRef Schramm-Sapyta NL, Cha YM, Chaudhry S, Wilson WA, Scott Swartzwelder HS, Kuhn CM (2007) Differential anxiogenic, aversive, and locomotor effects of THC in adolescent and adult rats. Psychopharmacology 191(4):867–877PubMedCrossRef
Zurück zum Zitat Seely KA, Patton AL, Moran CL, Womack ML, Prather PL, Fantegrossi WE, Radominska-Pandya A, Endres GW, Channell KB, Smith NH, McCain KR, James LP, Moran JH (2013) Forensic investigation of K2, spice, and “bath salt” commercial preparations: a three-year study of new designer drug products containing synthetic cannabinoid, stimulant, and hallucinogenic compounds. For Sci Int 233(1–3):416–422 Seely KA, Patton AL, Moran CL, Womack ML, Prather PL, Fantegrossi WE, Radominska-Pandya A, Endres GW, Channell KB, Smith NH, McCain KR, James LP, Moran JH (2013) Forensic investigation of K2, spice, and “bath salt” commercial preparations: a three-year study of new designer drug products containing synthetic cannabinoid, stimulant, and hallucinogenic compounds. For Sci Int 233(1–3):416–422
Zurück zum Zitat Segalowitz SJ, Davies PL (2004) Charting the maturation of the frontal lobe: an electrophysiological strategy. Brain Cogn 55(1):116–133PubMedCrossRef Segalowitz SJ, Davies PL (2004) Charting the maturation of the frontal lobe: an electrophysiological strategy. Brain Cogn 55(1):116–133PubMedCrossRef
Zurück zum Zitat Singh ME, McGregor IS, Mallet PE (2006) Perinatal exposure to delta(9)-tetrahydrocannabinol alters heroin-induced place conditioning and fos-immunoreactivity. Neuropsychopharmacology 31(1):58–69PubMed Singh ME, McGregor IS, Mallet PE (2006) Perinatal exposure to delta(9)-tetrahydrocannabinol alters heroin-induced place conditioning and fos-immunoreactivity. Neuropsychopharmacology 31(1):58–69PubMed
Zurück zum Zitat Solowij N, Stephens RS, Roffman RA, Babor T, Kadden R, Miller M, Christiansen K, McRee B, Vendetti J (2002) Cognitive functioning of long-term heavy cannabis users seeking treatment. JAMA 287:1123–1131PubMedCrossRef Solowij N, Stephens RS, Roffman RA, Babor T, Kadden R, Miller M, Christiansen K, McRee B, Vendetti J (2002) Cognitive functioning of long-term heavy cannabis users seeking treatment. JAMA 287:1123–1131PubMedCrossRef
Zurück zum Zitat Spear LP (2000) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24(4):417–463PubMedCrossRef Spear LP (2000) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24(4):417–463PubMedCrossRef
Zurück zum Zitat Tepper JM, Sharpe NA, Koós TZ, Trent F (1998) Postnatal development of the rat neostriatum: electrophysiological, light- and electron-microscopic studies. Dev Neurosci 20(2–3):125–145PubMedCrossRef Tepper JM, Sharpe NA, Koós TZ, Trent F (1998) Postnatal development of the rat neostriatum: electrophysiological, light- and electron-microscopic studies. Dev Neurosci 20(2–3):125–145PubMedCrossRef
Zurück zum Zitat Tzschentke TM (2007) Measuring reward with the conditioned place preference (CPP) paradigm: update of the last decade. Addict Biol 12:227–462PubMedCrossRef Tzschentke TM (2007) Measuring reward with the conditioned place preference (CPP) paradigm: update of the last decade. Addict Biol 12:227–462PubMedCrossRef
Zurück zum Zitat Urbanska M, Blazejczyk M, Jaworski J (2008) Molecular basis of dendritic arborization. Acta Neurobiol Exp (Wars) 68(2):264–288 Urbanska M, Blazejczyk M, Jaworski J (2008) Molecular basis of dendritic arborization. Acta Neurobiol Exp (Wars) 68(2):264–288
Zurück zum Zitat Varlinskaya EI, Spear LP (2008) Social interactions in adolescent and adult Sprague–Dawley rats: impact of social deprivation and test context familiarity. Behav Brain Res 188(2):398–405PubMedCentralPubMedCrossRef Varlinskaya EI, Spear LP (2008) Social interactions in adolescent and adult Sprague–Dawley rats: impact of social deprivation and test context familiarity. Behav Brain Res 188(2):398–405PubMedCentralPubMedCrossRef
Zurück zum Zitat Verslegers M, Van Hove I, Dekeyster E, Gantois I, Hu TT, D'Hooge R, Arckens L, Moons L (2014) MMP-2 mediates Purkinje cell morphogenesis and spine development in the mouse cerebellum. Brain Struct Funct [Epub ahead of print] Verslegers M, Van Hove I, Dekeyster E, Gantois I, Hu TT, D'Hooge R, Arckens L, Moons L (2014) MMP-2 mediates Purkinje cell morphogenesis and spine development in the mouse cerebellum. Brain Struct Funct [Epub ahead of print]
Zurück zum Zitat Wagner FA, Anthony JC (2002) From first drug use to drug dependence; developmental periods of risk for dependence upon marijuana, cocaine, and alcohol. Neuropsychopharmacology 26:479–488PubMedCrossRef Wagner FA, Anthony JC (2002) From first drug use to drug dependence; developmental periods of risk for dependence upon marijuana, cocaine, and alcohol. Neuropsychopharmacology 26:479–488PubMedCrossRef
Zurück zum Zitat Warner LA, Kessler RC, Hughes M, Anthony JC, Nelson CB (1995) Prevalence and correlates of drug use and dependence in the United States. Results from the National Comorbidity Survey. Arch Gen Psychiatry 52:219–229PubMedCrossRef Warner LA, Kessler RC, Hughes M, Anthony JC, Nelson CB (1995) Prevalence and correlates of drug use and dependence in the United States. Results from the National Comorbidity Survey. Arch Gen Psychiatry 52:219–229PubMedCrossRef
Zurück zum Zitat Wilmouth CE, Spear LP (2004) Adolescent and adult rats' aversion to flavors previously paired with nicotine. Ann N Y Acad Sci 1021:462–464PubMedCrossRef Wilmouth CE, Spear LP (2004) Adolescent and adult rats' aversion to flavors previously paired with nicotine. Ann N Y Acad Sci 1021:462–464PubMedCrossRef
Zurück zum Zitat Winters BD, Kruger JM, Huang X, Gallaher ZR, Ishikawa M, Czaja K, Krueger JM, Huang YH, Schluter OM, Dong Y (2012) Cannabinoid receptor 1-expressing neurons in the nucleus accumbens. Proc Natl Acad Sci USA 109(40):E2717–E2725PubMedCentralPubMedCrossRef Winters BD, Kruger JM, Huang X, Gallaher ZR, Ishikawa M, Czaja K, Krueger JM, Huang YH, Schluter OM, Dong Y (2012) Cannabinoid receptor 1-expressing neurons in the nucleus accumbens. Proc Natl Acad Sci USA 109(40):E2717–E2725PubMedCentralPubMedCrossRef
Zurück zum Zitat Yuan WX, Heng LJ, Ma J, Wang XQ, Qu LJ, Duan L, Kang JJ, Chen LW, Gao GD (2013) Increased expression of cannabinoid receptor 1 in the nucleus accumbens core in a rat model with morphine withdrawal. Brain Res 1531:102–112PubMedCrossRef Yuan WX, Heng LJ, Ma J, Wang XQ, Qu LJ, Duan L, Kang JJ, Chen LW, Gao GD (2013) Increased expression of cannabinoid receptor 1 in the nucleus accumbens core in a rat model with morphine withdrawal. Brain Res 1531:102–112PubMedCrossRef
Zurück zum Zitat Zilles K, Wree A (1995) Cortex: areal and laminar structure. In: Paxinos G (ed) The rat nervous system, 2nd edn. Academic Press, San Diego, CA, pp p 649–688 Zilles K, Wree A (1995) Cortex: areal and laminar structure. In: Paxinos G (ed) The rat nervous system, 2nd edn. Academic Press, San Diego, CA, pp p 649–688
Metadaten
Titel
Repeated administration of a synthetic cannabinoid receptor agonist differentially affects cortical and accumbal neuronal morphology in adolescent and adult rats
verfasst von
A. F. Carvalho
B. A. S. Reyes
F. Ramalhosa
N. Sousa
E. J. Van Bockstaele
Publikationsdatum
01.01.2016
Verlag
Springer Berlin Heidelberg
Erschienen in
Brain Structure and Function / Ausgabe 1/2016
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-014-0914-6

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