Effect of cannabis on glutamate signalling in the brain: A systematic review of human and animal evidence

Ames, 1979, Effects of the oral administration of Cannabis sativa (dagga) on chacma baboons (Papio ursinus), S. Afr. Med. J., 55, 1127 Appiah-Kusi, 2016, Abnormalities in neuroendocrine stress response in psychosis: the role of endocannabinoids, Psychol. Med., 46, 27, 10.1017/S0033291715001786 Bhattacharyya, 2009, Modulation of mediotemporal and ventrostriatal function in humans by Delta 9-tetrahydrocannabinol a neural basis for the effects of cannabis sativa on learning and psychosis, Arch. Gen. Psychiatry, 66, 442, 10.1001/archgenpsychiatry.2009.17 Bhattacharyya, 2009, Imaging the neural effects of cannabinoids: current status and future opportunities for psychopharmacology, Curr. Pharm. Des, 15, 2603, 10.2174/138161209788957465 Bhattacharyya, 2010, Opposite effects of delta-9-tetrahydrocannabinol and cannabidiol on human brain function and psychopathology, Neuropsychopharmacology, 35, 764, 10.1038/npp.2009.184 Bhattacharyya, 2012, Preliminary report of biological basis of sensitivity to the effects of cannabis on psychosis: aKT1 and DAT1 genotype modulates the effects of delta-9-tetrahydrocannabinol on midbrain and striatal function, Mol. Psychiatry, 17, 1152, 10.1038/mp.2011.187 Bhattacharyya, 2012, Induction of psychosis by ∆9-tetrahydrocannabinol reflects modulation of prefrontal and striatal function during attentional salience processing, Arch. Gen. Psychiatry, 69, 27, 10.1001/archgenpsychiatry.2011.161 Bhattacharyya, 2012, Neural mechanisms for the cannabinoid modulation of cognition and affect in man: a critical review of neuroimaging studies, Curr. Pharm. Des., 18, 5045, 10.2174/138161212802884636 Bhattacharyya, 2014, Protein kinase B (AKT1) genotype mediates sensitivity to cannabis-induced impairments in psychomotor control, Psychol. Med., 44, 3315, 10.1017/S0033291714000920 Bhattacharyya, 2015, Impairment of inhibitory control processing related to acute psychotomimetic effects of cannabis, Eur. Neuropsychopharmacol., 25, 26, 10.1016/j.euroneuro.2014.11.018 Bhattacharyya, 2015, Cannabinoid modulation of functional connectivity within regions processing attentional salience, Neuropsychopharmacology, 40, 1343, 10.1038/npp.2014.258 Brown, 2003, Cannabinoids decrease corticostriatal synaptic transmission via an effect on glutamate uptake, J. Neurosci., 23, 11073, 10.1523/JNEUROSCI.23-35-11073.2003 Campolongo, 2007, Perinatal exposure to delta-9-tetrahydrocannabinol causes enduring cognitive deficits associated with alteration of cortical gene expression and neurotransmission in rats, Addict. Biol., 12, 485, 10.1111/j.1369-1600.2007.00074.x Castaldo, 2007, Prenatal exposure to the cannabinoid receptor agonist WIN 55,212-2 increases glutamate uptake through overexpression of GLT1 and EAAC1 glutamate transporter subtypes in rat frontal cerebral cortex, Neuropharmacology, 53, 369, 10.1016/j.neuropharm.2007.05.019 Castaldo, 2010, Altered regulation of glutamate release and decreased functional activity and expression of GLT1 and GLAST glutamate transporters in the hippocampus of adolescent rats perinatally exposed to delta(9)-THC, Pharmacol. Res., 61, 334, 10.1016/j.phrs.2009.11.008 Ceccarini, 2015, [F-18]MK-9470 PET measurement of cannabinoid CB1 receptor availability in chronic cannabis users, Addict. Biol., 20, 357, 10.1111/adb.12116 Chang, 2006, Combined and independent effects of chronic marijuana use and HIV on brain metabolites, J. Neuroimmune Pharmacol., 1, 65, 10.1007/s11481-005-9005-z Chen, 2013, Delta9-THC-caused synaptic and memory impairments are mediated through COX-2 signaling, Cell, 155, 1154, 10.1016/j.cell.2013.10.042 Colizzi, 2015, Interaction between DRD2 and AKT1 genetic variations on risk of psychosis in cannabis users: a case–control study, Npj Schizophr., 1, 15025, 10.1038/npjschz.2015.25 Colizzi, 2015, Interaction between functional genetic variation of DRD2 and cannabis use on risk of psychosis, Schizophr. Bull., 41, 1171, 10.1093/schbul/sbv032 Colizzi, 2015, Functional genetic variation of the cannabinoid receptor 1 and cannabis use interact on prefrontal connectivity and related working memory behavior, Neuropsychopharmacology, 40, 640, 10.1038/npp.2014.213 Colizzi, 2016, Substance use, medication adherence and outcome one year following a first episode of psychosis, Schizophr. Res., 170, 311, 10.1016/j.schres.2015.11.016 Di Forti, 2009, High-potency cannabis and the risk of psychosis, Br. J. Psychiatry, 195, 488, 10.1192/bjp.bp.109.064220 Edery, 1975, The gamma-aminobutyric acid system in rat cerebellum during cannabinoid-induced cataleptoid state, Br. J. Pharmacol, 54, 406, 10.1111/j.1476-5381.1975.tb07584.x Fan, 2010, Reduced expression of glutamate receptors and phosphorylation of CREB are responsible for in vivo Delta9-THC exposure-impaired hippocampal synaptic plasticity, J. Neurochem., 112, 691, 10.1111/j.1471-4159.2009.06489.x Galanopoulos, 2011, ∆(9)-THC and WIN55,212-2 affect brain tissue levels of excitatory amino acids in a phenotype- compound-, Dose-, and region-specific manner, Behav. Brain Res., 224, 65, 10.1016/j.bbr.2011.05.018 Garcia-Gil, 1999, Perinatal Delta9-tetrahydrocannabinol exposure augmented the magnitude of motor inhibition caused by GABA(B) but not GABA(A), receptor agonists in adult rats, Neurotoxicol. Teratol., 21, 277, 10.1016/S0892-0362(98)00058-0 Ghazzaoui, 2014, Imaging dopamine transmission parameters in cannabis dependence, Prog. Neuropsychopharmacol. Biol. Psychiatry, 52, 28, 10.1016/j.pnpbp.2013.10.013 Ghoneim, 1980, Effect of hashish smoke on some blood and serum parameters in rabbits, Pharmazie, 35, 226 Gonzales, 1997, Alcohol and glutamate, Alcohol Health Res. World, 21, 120 Good, 2010, Afferent-specific AMPA receptor subunit composition and regulation of synaptic plasticity in midbrain dopamine neurons by abused drugs, J. Neurosci., 30, 7900, 10.1523/JNEUROSCI.1507-10.2010 Gu, 2013, Quantification of glutamate and glutamine using constant-time point-resolved spectroscopy at 3T, NMR Biomed., 26, 164, 10.1002/nbm.2831 Hamilton, 2015, Cannabis psychosis gender matters, Adv. Dual Diagn., 8, 153, 10.1108/ADD-12-2014-0039 Han, 2012, Acute cannabinoids impair working memory through astroglial CB1 receptor modulation of hippocampal LTD, Cell, 148, 1039, 10.1016/j.cell.2012.01.037 Hikal, 1988, Determination of amino acids in different regions of the rat brain: application to the acute effects of tetrahydrocannabinol (THC) and trimethyltin (TMT), Life Sci., 42, 2029, 10.1016/0024-3205(88)90503-6 Hirvonen, 2012, Reversible and regionally selective downregulation of brain cannabinoid CB1 receptors in chronic daily cannabis smokers, Mol. Psychiatry, 17, 642, 10.1038/mp.2011.82 Hoffman, 2003, Functional tolerance and blockade of long-term depression at synapses in the nucleus accumbens after chronic cannabinoid exposure, J. Neurosci., 23, 4815, 10.1523/JNEUROSCI.23-12-04815.2003 Hoffman, 2007, Opposing actions of chronic Delta9-tetrahydrocannabinol and cannabinoid antagonists on hippocampal long-term potentiation, Learn. Mem., 14, 63, 10.1101/lm.439007 Hoffman, 2010, Control of cannabinoid CB1 receptor function on glutamate axon terminals by endogenous adenosine acting at A1 receptors, J. Neurosci., 30, 545, 10.1523/JNEUROSCI.4920-09.2010 Howes, 2009, The dopamine hypothesis of schizophrenia: version III—the final common pathway, Schizophr. Bull., 35, 549, 10.1093/schbul/sbp006 Howes, 2015, Glutamate and dopamine in schizophrenia: an update for the 21st century, J. Psychopharmacol., 29, 97, 10.1177/0269881114563634 Irie, 2015, MAM-2201, a synthetic cannabinoid drug of abuse, suppresses the synaptic input to cerebellar Purkinje cells via activation of presynaptic CB1 receptors, Neuropharmacology, 95, 479, 10.1016/j.neuropharm.2015.02.025 Kuepper, 2010, Does dopamine mediate the psychosis-inducing effects of cannabis? A review and integration of findings across disciplines, Schizophr. Res., 121, 107, 10.1016/j.schres.2010.05.031 Liechti, 2008, Glutamate and the reinforcing effects of nicotine, Eur. Neuropsychopharm., 18, S56, 10.1016/S0924-977X(08)70065-8 Liu, 2010, Synaptic neurotransmission depression in ventral tegmental dopamine neurons and cannabinoid-associated addictive learning, PLoS One, 5, e15634, 10.1371/journal.pone.0015634 Long, 2013, Transmembrane domain Nrg1 mutant mice show altered susceptibility to the neurobehavioural actions of repeated THC exposure in adolescence, Int. J. Neuropsychopharmacol., 16, 163, 10.1017/S1461145711001854 Mato, 2005, Presynaptic homeostatic plasticity rescues long-term depression after chronic Delta 9-tetrahydrocannabinol exposure, J. Neurosci., 25, 11619, 10.1523/JNEUROSCI.2294-05.2005 Monnet-Tschudi, 2008, Delta-9-tetrahydrocannabinol accumulation: metabolism and cell-type-specific adverse effects in aggregating brain cell cultures, Toxicol. Appl. Pharmacol., 228, 8, 10.1016/j.taap.2007.11.007 Moore, 2007, Cannabis use and risk of psychotic or affective mental health outcomes: a systematic review, Lancet, 370, 319, 10.1016/S0140-6736(07)61162-3 Muetzel, 2013, In vivo H magnetic resonance spectroscopy in young-adult daily marijuana users, NeuroImage Clin., 2, 581, 10.1016/j.nicl.2013.04.011 Murray, 2007, Cannabis: the mind and society: the hash realities, Nat. Rev. Neurosci., 8, 885, 10.1038/nrn2253 Orru, 2011, Pharmacological evidence for different populations of postsynaptic adenosine A2A receptors in the rat striatum, Neuropharmacology, 61, 967, 10.1016/j.neuropharm.2011.06.025 Patel, 2016, Association of cannabis use with hospital admission and antipsychotic treatment failure in first episode psychosis: an observational study, BMJ Open, 6, e009888, 10.1136/bmjopen-2015-009888 Pertwee, 2008, The diverse CB1 and CB2 receptor pharmacology of three plant cannabinoids: delta9-tetrahydrocannabinol: cannabidiol and delta9-tetrahydrocannabivarin, Br. J. Pharmacol., 153, 199, 10.1038/sj.bjp.0707442 Pistis, 2002, Delta(9)-tetrahydrocannabinol decreases extracellular GABA and increases extracellular glutamate and dopamine levels in the rat prefrontal cortex: an in vivo microdialysis study, Brain Res., 948, 155, 10.1016/S0006-8993(02)03055-X Poels, 2014, Glutamatergic abnormalities in schizophrenia: a review of proton MRS findings, Schizophr. Res., 152, 325, 10.1016/j.schres.2013.12.013 Prescot, 2011, Neurochemical alterations in adolescent chronic marijuana smokers: a proton MRS study, Neuroimage, 57, 69, 10.1016/j.neuroimage.2011.02.044 Prescot, 2013, γ-Amino butyric acid and glutamate abnormalities in adolescent chronic marijuana smokers, Drug Alcohol Depend., 129, 232, 10.1016/j.drugalcdep.2013.02.028 Romero, 1998, The activation of cannabinoid receptors in striatonigral GABAergic neurons inhibited GABA uptake, Life Sci., 62, 351, 10.1016/S0024-3205(97)01117-X Rubino, 2015, Adolescent exposure to THC in female rats disrupts developmental changes in the prefrontal cortex, Neurobiol. Dis., 73, 60, 10.1016/j.nbd.2014.09.015 Sami, 2015, Does cannabis affect dopaminergic signaling in the human brain? A systematic review of evidence to date, Eur. Neuropsychopharmacol., 25, 1201, 10.1016/j.euroneuro.2015.03.011 Sanacora, 2012, Towards a glutamate hypothesis of depression An emerging frontier of neuropsychopharmacology for mood disorders, Neuropharmacology, 62, 63, 10.1016/j.neuropharm.2011.07.036 Sano, 2008, Delta 9-tetrahydrocannabinol-induced catalepsy-like immobilization is mediated by decreased 5-HT neurotransmission in the nucleus accumbens due to the action of glutamate-containing neurons, Neuroscience, 151, 320, 10.1016/j.neuroscience.2007.10.026 Schoeler, 2016, Continued versus discontinued cannabis use in patients with psychosis: a systematic review and meta-analysis, Lancet Psychiatry, 3, 215, 10.1016/S2215-0366(15)00363-6 Shen, 1999, Delta9-tetrahydrocannabinol acts as a partial agonist to modulate glutamatergic synaptic transmission between rat hippocampal neurons in culture, Mol. Pharmacol., 55, 8, 10.1124/mol.55.1.8 Snyder, 2008, Schizophrenia therapy: beyond atypical antipsychotics, Nat. Rev. Drug Discov., 7, 471, 10.1038/nrd2571 Spencer, 2013, Novel molecular changes induced by Nrg1 hypomorphism and Nrg1-cannabinoid interaction in adolescence: a hippocampal proteomic study in mice, Front. Cell. Neurosci., 7, 15, 10.3389/fncel.2013.00015 Straiker, 2005, Depolarization-induced suppression of excitation in murine autaptic hippocampal neurones, J. Physiol., 569, 501, 10.1113/jphysiol.2005.091918 Suarez, 2002, Reduced glial fibrillary acidic protein and glutamine synthetase expression in astrocytes and Bergmann glial cells in the rat cerebellum caused by delta(9)-tetrahydrocannabinol administration during development, Dev. Neurosci., 24, 300, 10.1159/000066744 Suarez, 2004, Down-regulation of the AMPA glutamate receptor subunits GluR1 and GluR2/3 in the rat cerebellum following pre- and perinatal delta9-tetrahydrocannabinol exposure, Cerebellum, 3, 66, 10.1080/14734220310017230 Suarez, 2004, Prenatal cannabinoid exposure down- regulates glutamate transporter expressions (GLAST and EAAC1) in the rat cerebellum, Dev. Neurosci., 26, 45, 10.1159/000080711 Sung, 2013, Decreased frontal N-acetylaspartate levels in adolescents concurrently using both methamphetamine and marijuana, Behav. Brain Res., 246, 154, 10.1016/j.bbr.2013.02.028 Tomasini, 2002, Delta(9)-tetrahydrocannabinol increases endogenous extracellular glutamate levels in primary cultures of rat cerebral cortex neurons: involvement of CB(1) receptors, J. Neurosci. Res., 68, 449, 10.1002/jnr.10242 Tonini, 2006, ERK-dependent modulation of cerebellar synaptic plasticity after chronic Delta9-tetrahydrocannabinol exposure, J. Neurosci., 26, 5810, 10.1523/JNEUROSCI.5469-05.2006 West, 2002, Systems to rate the strength of scientific evidence, Evid. Rep. Technol. Assess. (Summ.), 1 Zamberletti, 2014, Alterations of prefrontal cortex GABAergic transmission in the complex psychotic-like phenotype induced by adolescent delta-9-tetrahydrocannabinol exposure in rats, Neurobiol. Dis., 63, 35, 10.1016/j.nbd.2013.10.028 van Winkel, 2014, Epidemiological neurobiological, and genetic clues to the mechanisms linking cannabis use to risk for nonaffective psychosis, Annu. Rev. Clin. Psychol., 10, 767, 10.1146/annurev-clinpsy-032813-153631