Adolescent cannabinoid exposure permanently suppresses cortical oscillations in adult mice

Neuropsychopharmacology

Volumn 38, Issue 12, 2013, Pages 2338-2347

  Raver, Sylvina M ^a   Haughwout, Sarah P ^a   Keller, Asaf ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

D 9 tetrahydrocannabinol; development; marijuana; neural synchrony; novel object recognition; schizophrenia

Indexed keywords

CANNABINOID; CANNABIS; ENDOCANNABINOID; KETAMINE; TETRAHYDROCANNABINOL;

ADOLESCENT; ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; BRAIN CORTEX; BRAIN SLICE; COGNITIVE BEHAVIOR; COGNITIVE DEFECT; CONTROLLED STUDY; CORTICAL OSCILLATION; DRUG EXPOSURE; ELECTRIC POTENTIAL; ELECTROCORTICOGRAPHY; HYPOTHESIS; LOCAL FIELD POTENTIAL; MEDIAL PREFRONTAL CORTEX; MOTOR DYSFUNCTION; MOUSE; NEUROMODULATION; NONHUMAN; OSCILLATION; PREDICTION; PREFRONTAL CORTEX; PRIMARY SOMATOSENSORY CORTEX; PRIORITY JOURNAL; WORKING MEMORY;

AGE FACTORS; ANIMALS; BENZOXAZINES; BRAIN WAVES; CANNABINOID RECEPTOR AGONISTS; CANNABINOIDS; CEREBRAL CORTEX; DRONABINOL; ELECTROENCEPHALOGRAPHY; EXPLORATORY BEHAVIOR; MALE; MICE; MORPHOLINES; NAPHTHALENES; RECOGNITION (PSYCHOLOGY);

EID: 84888329823     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2013.164     Document Type: Article

References (50)

1. AnDErsen SL (2003). Trajectories of brain DEvelopment: point of vulnerability or window of opportunity Neurosci Biobehav Rev 27: 3-18. (Pubitemid 36535387)
2. Arseneault L, Canno M, Whitton J, Murray RM (2004). Causal association between cannabis and psychosis: an examination of the eviDEnce. Br J Psychiatry 325: 1212-1213.
3. Breivogel CS, Griffin G, Di Marzo V, Martin BR (2001). EviDEnce for a new G protein-coupled cannabinoid receptor in mouse brain. Mol Pharm 60: 155-163. (Pubitemid 32595243)
4. Buhl EH, Tamas G, Fisahn A (1998). Cholinergic activation and tonic excitation induce persistent gamma oscillations in mouse somatosensory cortex in vitro. J Physiol 513: 117-126. (Pubitemid 28528570)
5. Buzsaki G, Draguhn A (2004). Neuronal oscillations in cortical networks. Science 304: 1926-1929.
6. Buzsaki G (2006). Rhythms of the Brain. Oxford University Press: New York, NY, USA.
7. Cao Z, Lickey ME, Liu L, Kirk E, Gordon B (2000). Postnatal DEvelopment of NR1, NR2A and NR2B immunoreactivity in the visual cortex of the rat. Brain Res 859: 26-37. (Pubitemid 30138190)
8. Cardin JA, Carlén M, Meletis K, Knoblich U, Zhang F, DEisseroth K et al (2009). Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459: 663-667.
9. Cunningham MO, Davies CH, Buhl EH, Kopell N, Whittington MA (2003). Gamma oscillations induced by kainate receptor activation in the entorhinal cortex in vitro. J Neurosci 23: 9761-9769. (Pubitemid 37371588)
10. DEshmukh S, Onozuka K, BenDEr KJ, BenDEr VA, Lutz B, Mackie K et al (2007). Postnatal DEvelopment of cannabinoid receptor type 1 expression in roDEnt somatosensory cortex. Neuroscience 145: 279-287. (Pubitemid 46227719)
11. Fisahn A, Pike FG, Buh EH, Paulsen O (1998). Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature 394: 186-189. (Pubitemid 28325972)
12. Fries P (2005). A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn 9: 474-480. (Pubitemid 41338822)
13. Fries P, Reynolds JH, Rorie AE, DEsimone R (2001). Modulation of oscillatory neuronal synchronization by selective visual attention. Science 291: 1560-1563. (Pubitemid 32179225)
14. Giedd JN, Blumenthal J, Jeffries NO, Rajapakse JC, Vaituzis AC, Liu U et al (1999). DEvelopment of the human corpus callosum during childhood and adolescence: a longitudinal MRI study. Prog Neuropsychopharmacol Biol Psychiatry 23: 571-588. (Pubitemid 29268403)
15. Gogtay N, Giedd JN, Lusk L, Hayashi KM, Greenstein D, Vaituzis AC et al (2004). Dynamic mapping of human cortical DEvelopment during childhood through early adulthood. Proc Natl Acad Sci USA 101: 8174-8179. (Pubitemid 38698073)
16. Gonzalez-Burgos G, Lewis DA (2008). GABA neurons and the mechanisms of network oscillations: implications for unDErstanding cortical dysfunction in schizophrenia. Schizophr Bull 34: 944-961.
17. Gulyás AI, Szabó GG, Ulbert I, HolDErith H, Monyer H, ErDÉlyi F et al (2010). Parvalbumin-containing fast-spiking basket cells generate the field potential oscillations induced by cholinergic receptor activation in the hippocampus. J Neurosci 30: 15134-15145.
18. Hajós M, Hoffmann WE, Kocsis B (2008). Activation of cannabinoid-1 receptors disrupts sensory gating and neuronal oscillation: relevance to schizophrenia. Biol Psychiatry 63: 1075-1083.
19. Hajós N, Katona I, Naiem SS, Mackie K, LeDEnt C, Mody I et al (2000). Cannabinoids inhibit hippocampal GABAergic transmission and network oscillations. Eur J Neurosci 12: 3239-3249.
20. Hakami T, Jones NC, Tolmacheva EA, Gaudias J, Chaumont J, Salzberg M et al (2009). NMDA receptor hypofunction leads to generalized and persistent aberrant gamma oscillations inDEpenDEnt of hyperlocomotion and the state of consciousness. PLoS One 4: e6755.
21. Hashimoto T, Nguyen QL, Rotaru D, Keenan T, Arion D, Beneyto M et al (2009). Protracted DEvelopmental trajectories of GABAA receptor alpha1 and alpha2 subunit expression in primate prefrontal cortex. Biol Psychiatry 65: 1015-1023.
22. 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: 278-286.
23. Hoaglin DC, Iglewicz B, Tukey JW (1986). Performance of some resistant rules for outlier labeling. J Am Stat Assoc 81: 991-999.
24. HolDErith N, Nemeth B, Papp OI, Veres JM, Nagy GA, Hajós N (2011). Cannabinoids attenuate hippocampal gamma oscillations by suppressing excitatory synaptic input onto CA3 pyramidal neurons and fast spiking basket cells. J Physiol 589: 4921-4934.
25. Kucewicz MT, Tricklebank MD, Bogacz R, Jones MW (2011). Dysfunctional prefrontal cortical network activity and interactions following cannabinoid receptor activation. J Neurosci 31: 15560-15568.
26. Long LE, Lind J, Webster M, Weickert CS (2012). DEvelopmental trajectory of the endocannabinoid system in human dorsolateral prefrontal cortex. BMC Neurosci 13: 87.
27. Luna B (2009). DEvelopmental changes in cognitive control through adolescence. Adv Child DEv Behav 37: 233-278.
28. Meier MH, Caspi A, Ambler A, Harrington H, Houts R, Keefe RSE et al (2012). Persistent cannabis users show neuropsychological DEcline from childhood to midlife. Proc Natl Acad Sci USA 109: E2657-E2664.
29. Mitra P, Bokil H (2008). Observed Brain Dynamics. Oxford University Press: New York, NY, USA.
30. Oke OO, Magony A, Anver H, Ward PD, Jiruska P, Jeffrys JGR et al (2010). High-frequency gamma oscillations coexist with lowfrequency gamma oscillations in the rat visual cortex in vitro. Eur J Neurosci 31: 1435-1445.
31. 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: 502-508. (Pubitemid 39665118)
32. Phillips KG, Cotel MC, McCarthy AP, Edgar DM, Tricklebank M, O'Neill MJ et al (2012). Differential effects of NMDA antagonists on high frequency and gamma EEG oscillations in a neuroDEvelopmental moDEl of schizophrenia. Neuropharmacology 62: 1359-1370.
33. PlourDE G, Baribeau J, Bonhomme V (1997). Ketamine increases the amplituDE of the 40-Hz auditory steady-state response in humans. Br J Anaesthesia 78: 524-529. (Pubitemid 27226364)
34. Quinn HR, Matsumoto I, Callaghan PD, Long LE, Arnold JC, Gunasekaran N et al (2008). Adolescent rats find repeated D9-THC less aversive than adult rats but display greater residual cognitive DEficits and changes in hippocampal protein exposure following exposure. Neuropsychopharmacology 33: 1113-1126. (Pubitemid 351367534)
35. Robbe D, Montgomery SM, Thome A, Rueda-Orozco PE, McNaughton BL, Buzsaki G (2006). Cannabinoids reveal importance of spike timing coordination in hippocampal function. Nat Neurosci 9: 1526-1533. (Pubitemid 44862661)
36. Roux F, Wibral M, Mohn HM, Singer W, Uhlhaas PJ (2012). Gamma-band activity in human prefrontal cortex coDEs for the number of relevant items maintained in working memory. J Neurosci 32: 12411-12420.
37. Ryberg E, Larsson N, Sjögren S, Hjorth S, Hermannson N-O, Leonova J et al (2007). The orphan receptor GPR55 is a novel cannabinoid receptor. Br J Pharmacol 152: 1092-1101. (Pubitemid 350166046)
38. Sales-Carbonell C, Rueda-Orozco PE, Soria-Gómez E, Buzsáki G, Marsicano G, Robbe D (2013). Striatal GABAergic and cortical glutamatergic neurons mediate contrasting effects of cannabinoids on cortical network synchrony. Proc Natl Acad Sci USA 110: 719-724.
39. 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: 1760-1769. (Pubitemid 41070841)
40. Showalter VM, Compton DR, Martin BR, Abood ME (1996). Evaluation of binding in a transfected cell line expressing a peripheral cannabinoid receptor (CB2): iDEntification of cannabinoid receptor subtype selective ligands. J Pharmacol Exp Ther 278: 989-999. (Pubitemid 27166944)
41. Singer W, Gray CM (1995). Visual feature integration and the temporal correlation hypothesis. Annu Rev Neurosci 18: 555-586.
42. Skosnik PD, D'Souza DC, Steinmetz AB, Edwards CR, Vollmer JM, Hetrick WP et al (2012). The effect of chronic cannabinoids on broadband EEG neural oscillations in humans. Neuropsychopharmacology 37: 2184-2193.
43. SteriaDE M, Amzica F, Contreras D (1996). Synchronization of fast (30-40 Hz) spontaneous cortical rhythms during brain activation. J Neurosci 16: 392-417. (Pubitemid 26010725)
44. Solowij N, Stephens RS, Roffman RA, Babor T, KadDEn R, Miller M et al (2002). Cognitive functioning of long-term heavy cannabis users seeking treatment. JAMA 287: 1123-1131. (Pubitemid 34252081)
45. Substance Abuse and Mental Health Services Administration (SAMHSA) (2011): Results from the 2011 National Survey on Drug Use and Health: Summary of National Findings http://www.samhsa.gov/data/nsduh/2k11results/ nsduhresults2011.pdf.
46. Uhlhaas PJ, Roux F, Rodriguez E, Rotarska-Jagiela A, Singer W (2010). Neural synchrony and the DEvelopment of cortical networks. Trends Cogn Sci 14: 72-80.
47. Uhlhaas PJ, Roux F, Singer W, Haenschel C, Sireteanu R, Rodriguez E (2009). The DEvelopment of neural synchrony reflects late maturation and restructuring of functional networks in humans. Proc Natl Acad Sci USA 106: 9866-9871.
48. Uhlhaas PJ, Singer W (2010). Abnormal neural oscillations and synchrony in schizophrenia. Nat Rev Neurosci 11: 100-113.
49. Wang XJ (2010). Neurophysiological and computational principles of cortical rhythms in cognition. Physiol Rev 90: 1195-1268.
50. Whittington MA, Traub RD, Kopell N, Ermentrout B, Buhl EH (2000). Inhibition-based rhythms: experimental and mathematical observations on network dynamics. Int J Psychophysiol 38: 315-336.