Effect of JWH-250, JWH-073 and their interaction on "tetrad", sensorimotor, neurological and neurochemical responses in mice

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 67, Issue , 2016, Pages 31-50

  Ossato, Andrea ^a   Canazza, Isabella ^a   Trapella, Claudio ^a   Vincenzi, Fabrizio ^a   De Luca, Maria Antonietta ^e   Rimondo, Claudia ^d   Varani, Katia ^a   Borea, Pier Andrea ^a   Serpelloni, Giovanni ^c   Marti, Matteo ^a,b  

^a UNIVERSITY OF FERRARA   (Italy)

^b Center for Neuroscience and Istituto Nazionale di Neuroscienze   (Italy)

^c UNIVERSITY OF FLORENCE   (Italy)

^d UNIVERSITY OF VERONA   (Italy)

^e UNIVERSITY OF CAGLIARI   (Italy)

Author keywords

JWH 018; JWH 073; JWH 250; Microdialysis; 9 THC

Indexed keywords

1 BUTYL 3 (1 NAPHTHOYL)INDOLE; CANNABINOID RECEPTOR AGONIST; JWH 250; UNCLASSIFIED DRUG; 1-(1- PENTYL-1H-INDOL-3-YL)-2-(2-METHOXYPHENYL)ETHANONE; 3-(2-HYDROXY-4-(1,1-DIMETHYLHEPTYL)PHENYL)-4-(3-HYDROXYPROPYL)CYCLOHEXANOL; ANISOLE DERIVATIVE; CYCLOHEXANOL DERIVATIVE; INDOLE DERIVATIVE; JWH-073; NAPHTHALENE DERIVATIVE;

AGGRESSION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUDITORY THRESHOLD; CATALEPSY; CONTROLLED STUDY; DOPAMINE RELEASE; DOPAMINERGIC TRANSMISSION; DRUG DETERMINATION; DRUG EFFECT; DRUG MECHANISM; DRUG POTENCY; HYPERREFLEXIA; HYPOTHERMIA; IN VIVO STUDY; LIMBIC CORTEX; MALE; MOTOR ACTIVITY; MOUSE; MYOCLONUS; NEUROCHEMISTRY; NONHUMAN; NUCLEUS ACCUMBENS; PAIN THRESHOLD; SEIZURE; SENSORIMOTOR FUNCTION; TACTILE FEEDBACK; VISUAL THRESHOLD; ACOUSTIC REFLEX; ANIMAL; BRAIN; CELL CULTURE; CHEMICALLY INDUCED; CYTOLOGY; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; DRUG POTENTIATION; HUMAN; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; NEUROLOGIC DISEASE; NEUROLOGIC GAIT DISORDER; SENSORY FEEDBACK; SPLEEN; VISION;

ANIMALS; ANISOLES; BRAIN; CELLS, CULTURED; CYCLOHEXANOLS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SYNERGISM; FEEDBACK, SENSORY; GAIT DISORDERS, NEUROLOGIC; HUMANS; HYPOTHERMIA; INDOLES; MALE; MICE; MICE, INBRED ICR; NAPHTHALENES; NERVOUS SYSTEM DISEASES; PAIN THRESHOLD; REFLEX, ACOUSTIC; SPLEEN; VISION, OCULAR;

EID: 84961306432     PISSN: 02785846     EISSN: 18784216     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2016.01.007     Document Type: Article

References (96)

1. Adriaan Bouwknecht J., Olivier B., Paylor R.E. The stress-induced hyperthermia paradigm as a physiological animal model for anxiety: a review of pharmacological and genetic studies in the mouse. Neurosci. Biobehav. Rev. 2007, 31(1):41-59.
2. Aung M.M., Griffin G., Huffman J.W., Wu M., Keel C., Yang B., et al. Influence of the N-1 alkyl chain length of cannabimimetic indoles upon CB(1) and CB(2) receptor binding. Drug Alcohol Depend. 2000, 60:133-140.
3. Auwarter V., Dresen S., Weinmann W., Muller M., Putz M., Ferreiros N. 'Spice' and other herbal blends: harmless incense or cannabinoid designer drugs?. J. Mass Spectrom. 2009, 44:832-837.
4. Bereiter D.A., Bereiter D.F., Hirata H. Topical cannabinoid agonist, WIN55,212-2, reduces cornea-evoked trigeminal brainstem activity in the rat. Pain 2002, 99:547-556.
5. Bortolato M., Aru G.N., Frau R., Orru M., Luckey G.C., Boi G., et al. The CB receptor agonist WIN 55,212-2 fails to elicit disruption of prepulse inhibition of the startle in Sprague-Dawley rats. Psychopharmacology 2005, 177:264-271.
6. Brents L.K., Gallus-Zawada A., Radominska-Pandya A., Vasiljevik T., Prisinzano T.E., Fantegrossi W.E., et al. Monohydroxylated metabolites of the K2 synthetic cannabinoid JWH-073 retain intermediate to high cannabinoid 1 receptor (CB1R) affinity and exhibit neutral antagonist to partial agonist activity. Biochem. Pharmacol. 2012, 83:952-961.
7. Brents L.K., Zimmerman S.M., Saffell A.R., Prather P.L., Fantegrossi W.E. Differential drug-drug interactions of the synthetic Cannabinoids JWH-018 and JWH-073: implications for drug abuse liability and pain therapy. J. Pharmacol. Exp. Ther. 2013, 346:350-361.
8. Carder B., Olson J. Marihuana and shock induced aggression in rats. Physiol. Behav. 1972, 8:599-602.
9. Carlini E.A., Gonzales C. Aggressive behaviour induced by marihuana compounds and amphetamine in rats previously made dependent on morphine. Experientia 1972, 28:542-544.
10. Carlini E.A., Lindsey C.J., Tufik S. Environmental and drug interference with effects of marihuana* Ann. N. Y. Acad. Sci. 1976, 281:229-243.
11. Cha H.J., Lee K.W., Song M.J., Hyeon Y.J., Hwang J.Y., Jang C.G., et al. Dependence potential of the synthetic cannabinoids JWH-073, JWH-081, and JWH-210: in vivo and in vitro approaches. Biomol. Ther. 2014, 22:363-369.
12. Compton D.R., Johnson M.R., Melvin L.S., Martin B.R. Pharmacological profile of a series of bicyclic cannabinoid analogs: classification as cannabimimetic agents. J. Pharmacol. Exp. Ther. 1992, 260:201-209.
13. Cristino L., de Petrocellis L., Pryce G., Baker D., Guglielmotti V., Di Marzo V. Immunohistochemical localization of cannabinoid type 1 and vanilloid transient receptor potential vanilloid type 1 receptors in the mouse brain. Neuroscience 2006, 139:1405-1415.
14. Dasilva M.A., Grieve K.L., Cudeiro J., Rivadulla C. Endocannabinoid CB1 receptors modulate visual output from the thalamus. Psychopharmacology 2012, 219:835-845.
15. De Luca M.A., Bimpisidis Z., Melis M., Marti M., Caboni P., Valentini V., et al. Stimulation OF IN VIVO dopamine transmission and intravenous self-administration in rats and mice by JWH-018, a Spice cannabinoid. Neuropharmacology 2015, 99:705-714.
16. Dhawan J., Deng H., Gatley S.J., Makriyannis A., Akinfeleye T., Bruneus M., et al. Evaluation of the in vivo receptor occupancy for the behavioral effects of cannabinoids using a radiolabeled cannabinoid receptor agonist, R-[125/131I]AM2233. Synapse 2006, 60:93-101.
17. Di Chiara G., Bassareo V., Fenu S., De Luca M.A., Spina L., Cadoni C., et al. Dopamine and drug addiction: the nucleus accumbens shell connection. Neuropharmacology 2004, 47(Suppl. 1):227-241.
18. Dresen S., Ferreiros N., Putz M., Westphal F., Zimmermann R., Auwarter V. Monitoring of herbal mixtures potentially containing synthetic cannabinoids as psychoactive compounds. J. Mass Spectrom. 2010, 45:1186-1194.
19. EMCDDA Understanding the 'Spice' phenomenon. Thematic Papers 2009, European Monitoring Centre for Drugs and Drug Addiction, (http://www.emcdda.europa.eu/publications/thematic-papers/spice).
20. Fantegrossi W.E., Moran J.H., Radominska-Pandya A., Prather P.L. Distinct pharmacology and metabolism of K2 synthetic cannabinoids compared to Delta(9)-THC: mechanism underlying greater toxicity?. Life Sci. 2014, 97:45-54.
21. Fattore L., Fratta W. Beyond THC: the new generation of cannabinoid designer drugs. Front. Behav. Neurosci. 2011, 5:60.
22. Garkun Y., Maffei A. Cannabinoid-dependent potentiation of inhibition at eye opening in mouse V1. Front. Cell. Neurosci. 2014, 8:46.
23. Ginsburg B.C., Schulze D.R., Hruba L., McMahon L.R. JWH-018 and JWH-073: delta(9)-tetrahydrocannabinol-like discriminative stimulus effects in monkeys. J. Pharmacol. Exp. Ther. 2012, 340:37-45.
24. Gomez-Nieto R., Horta-Junior Jde A., Castellano O., Millian-Morell L., Rubio M.E., Lopez D.E. Origin and function of short-latency inputs to the neural substrates underlying the acoustic startle reflex. Front. Neurosci. 2014, 8:216.
25. Gottardo R., Chiarini A., Dal Pra I., Seri C., Rimondo C., Serpelloni G., et al. Direct screening of herbal blends for new synthetic cannabinoids by MALDI-TOF MS. J. Mass Spectrom. 2012, 47:141-146.
26. Govaerts S.J., Hermans E., Lambert D.M. Comparison of cannabinoid ligands affinities and efficacies in murine tissues and in transfected cells expressing human recombinant cannabinoid receptors. Eur. J. Pharm. Sci. 2004, 23:233-243.
27. Grigoryev A., Melnik A., Savchuk S., Simonov A., Rozhanets V. Gas and liquid chromatography-mass spectrometry studies on the metabolism of the synthetic phenylacetylindole cannabimimetic JWH-250, the psychoactive component of smoking mixtures. J. Chromatogr. B Anal. Technol. Biomed. Life Sci. 2011, 879:2519-2526.
28. Grotenhermen F. Pharmacokinetics and pharmacodynamics of cannabinoids. Clin. Pharmacokinet. 2003, 42:327-360.
29. Guindon J., Hohmann A.G. Cannabinoid CB2 receptors: a therapeutic target for the treatment of inflammatory and neuropathic pain. Br. J. Pharmacol. 2008, 153:319-334.
30. Gurney S.M.R., Scott K.S., Kacinko S.L., Presley B.C., Logan B.K. Pharmacology, toxicology, and adverse effects of synthetic cannabinoid drugs. Forensic Sci. Rev. 2014, 26.
31. Ham M.T., De Jong Y. Absence of interaction between delta9-tetrahydrocannabinol (delta-THC) and cannabidiol (CBD) in aggression, muscle control and body temperature experiments in mice. Psychopharmacologia 1975, 41:169-174.
32. Hamdam J., Sethu S., Smith T., Alfirevic A., Alhaidari M., Atkinson J., et al. Safety pharmacology - current and emerging concepts. Toxicol. Appl. Pharmacol. 2013, 273:229-241.
33. Hemelt M.E., Keller Superior colliculus control of vibrissa movements. J. Neurophysiol. 2008, 100:1245-1254.
34. Herkenham M., Lynn A.B., Johnson M.R., Melvin L.S., de Costa B.R., Rice K.C. Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J. Neurosci. 1991, 11:563-583.
35. Hermanns-Clausen M., Kneisel S., Szabo B., Auwarter V. Acute toxicity due to the confirmed consumption of synthetic cannabinoids: clinical and laboratory findings. Addiction 2013, 108:534-544.
36. Ho W.S., Patel S., Thompson J.R., Roberts C.J., Stuhr K.L., Hillard C.J. Endocannabinoid modulation of hyperaemia evoked by physiologically relevant stimuli in the rat primary somatosensory cortex. Br. J. Pharmacol. 2010, 160:736-746.
37. Hohmann A.G., Tsou K., Walker J.M. Cannabinoid suppression of noxious heat-evoked activity in wide dynamic range neurons in the lumbar dorsal horn of the rat. J. Neurophysiol. 1999, 81:575-583.
38. Huffman J.W., Dai D., Martin B.R., Compton D.R. Design, synthesis and pharmacology of cannabimimetic indoles. Bioorg. Med. Chem. Lett. 1994, 4:563-566.
39. Huffman J.W., Szklennik P.V., Almond A., Bushell K., Selley D.E., He H., et al. 1-Pentyl-3-phenylacetylindoles, a new class of cannabimimetic indoles. Bioorg. Med. Chem. Lett. 2005, 15:4110-4113.
40. ICH S7A, 2001. US Food and Drug Administration Guidance for industry: safety pharmacology studies for human pharmaceuticals (S7A). http://www.fda.gov/downloads/drugs/guidancecomplianceregulatoryinformation/guidances/ucm074959.pdf.
41. Irwin S. Comprehensive observational assessment: Ia. A systematic, quantitative procedure for assessing the behavioral and physiologic state of the mouse. Psychopharmacologia 1968, 13:222-257.
42. Jenkins S., Worthington M., Harris J., Clarke R.W. Differential modulation of withdrawal reflexes by a cannabinoid in the rabbit. Brain Res. 2004, 1012:146-153.
43. Koch M. The neurobiology of startle. Prog. Neurobiol. 1999, 59:107-128.
44. Kozlov A.Y., Abramova A.Y., Chekhlov V.V., Grigorchuk O.S., Pertsov S.S. Nociceptive reactions in rats during repeated stress exposure. Bull. Exp. Biol. Med. 2015, 159(6):708-711.
45. Lecca D., Cacciapaglia F., Valentini V., Di Chiara G. Monitoring extracellular dopamine in the rat nucleus accumbens shell and core during acquisition and maintenance of intravenous WIN 55,212-2 self-administration. Psychopharmacology 2006, 188:63-74.
46. Liu C.H., Heynen A.J., Shuler M.G., Bear M.F. Cannabinoid receptor blockade reveals parallel plasticity mechanisms in different layers of mouse visual cortex. Neuron 2008, 58:340-345.
47. Macri S., Lanuzza L., Merola G., Ceci C., Gentili S., Valli A., et al. Behavioral responses to acute and sub-chronic administration of the synthetic cannabinoid JWH-018 in adult mice prenatally exposed to corticosterone. Neurotox. Res. 2013, 24:15-28.
48. Malone D.T., Taylor D.A. The effect of Delta9-tetrahydrocannabinol on sensorimotor gating in socially isolated rats. Behav. Brain Res. 2006, 166:101-109.
49. Mansbach R.S., Rovetti C.C., Winston E.N., Lowe J.A. Effects of the cannabinoid CB1 receptor antagonist SR141716A on the behavior of pigeons and rats. Psychopharmacology 1996, 124:315-322.
50. Marshell R., Kearney-Ramos T., Brents L.K., Hyatt W.S., Tai S., Prather P.L., et al. In vivo effects of synthetic cannabinoids JWH-018 and JWH-073 and phytocannabinoid delta-THC in mice: inhalation versus intraperitoneal injection. Pharmacol. Biochem. Behav. 2014, 124C:40-47.
51. Marsicano G., Lutz B. Expression of the cannabinoid receptor CB1 in distinct neuronal subpopulations in the adult mouse forebrain. Eur. J. Neurosci. 1999, 11:4213-4225.
52. Marti M., Mela F., Veronesi C., Guerrini R., Salvadori S., Federici M., et al. Blockade of nociceptin/orphanin FQ receptor signaling in rat substantia nigra pars reticulata stimulates nigrostriatal dopaminergic transmission and motor behavior. J. Neurosci. 2004, 24:6659-6666.
53. Marti M., Mela F., Fantin M., Zucchini S., Brown J.M., Witta J., et al. Blockade of nociceptin/orphanin FQ transmission attenuates symptoms and neurodegeneration associated with Parkinson's Disease. Eur. J. Neurosci. 2005, 25:9591-9601.
54. Marti M., Ossato A., Trapella C., Seri C., Rimondo C., Serpelloni G. JWH-018 and its N-pentyl-halogenated derivates impair sensory motor functions in mice. First Monothematic Congress of the Italian Society of Pharmacology: "Old and New Drugs of Abuse, Issues and Research Approaches" Verona, Italy 2013.
55. Martin W.J., Hohmann A.G., Walker J.M. Suppression of noxious stimulus-evoked activity in the ventral posterolateral nucleus of the thalamus by a cannabinoid agonist: correlation between electrophysiological and antinociceptive effects. J. Neurosci. 1996, 16:6601-6611.
56. Martin R.S., Secchi R.L., Sung E., Lemaire M., Bonhaus D.W., Hedley L.R., et al. Effects of cannabinoid receptor ligands on psychosis-relevant behavior models in the rat. Psychopharmacology 2003, 165:128-135.
57. Mattsson J.L., Spencer P.J., Albee R.R. A performance standard for clinical and functional observational battery examinations of rats. Int. J. Toxicol. 1996, 15:239-254.
58. Miczek K.A. Delta9-tetrahydrocannabinol: antiaggressive effects in mice, rats, and squirrel monkeys. Science 1978, 199:1459-1461.
59. Miczek K.A., de Almeida R.M.M., Kravitz E.A., Rissman E.F., de Boer S.F., Raine A. Neurobiology of escalated aggression and violence. J. Neurosci. 2007, 27:11803-11806.
60. Morales M., Bonci A. Getting to the core of addiction: Hooking CB2 receptor into drug abuse?. Nat. Med. 2012, 18:504-505.
61. Nagai H., Egashira N., Sano K., Ogata A., Mizuki A., Mishima K., et al. Antipsychotics improve Delta9-tetrahydrocannabinol-induced impairment of the prepulse inhibition of the startle reflex in mice. Pharmacol. Biochem. Behav. 2006, 84:330-336.
62. Ossato A., Vigolo A., Trapella C., Seri C., Rimondo C., Serpelloni G., et al. JWH-018 impairs sensorimotor functions in mice. Neuroscience 2015, 300:174-188.
63. Papanastassiou A.M., Fields H.L., Meng I.D. Local application of the cannabinoid receptor agonist, WIN 55,212-2, to spinal trigeminal nucleus caudalis differentially affects nociceptive and non-nociceptive neurons. Pain 2004, 107:267-275.
64. Papanti D., Schifano F., Botteon G., Bertossi F., Mannix J., Vidoni D., et al. "Spiceophrenia": a systematic overview of "Spice"-related psychopathological issues and a case report. Hum. Psychopharmacol. Clin. Exp. 2013, 28:379-389.
65. Paronis C.A., Nikas S.P., Shukla V.G., Makriyannis A. Delta(9)-Tetrahydrocannabinol acts as a partial agonist/antagonist in mice. Behav. Pharmacol. 2012, 23:802-805.
66. Patel S., Gerrits R., Muthian S., Greene A.S., Hillard C.J. The CB1 receptor antagonist SR141716 enhances stimulus-induced activation of the primary somatosensory cortex of the rat. Neurosci. Lett. 2002, 335:95-98.
67. Penn H.J., Langman L.J., Unold D., Shields J., Nichols J.H. Detection of synthetic cannabinoids in herbal incense products. Clin. Biochem. 2011, 44:1163-1165.
68. Pietr M.D., Knutsen P.M., Shore D.I., Ahissar E., Vogel Z. Cannabinoids reveal separate controls for whisking amplitude and timing in rats. J. Neurophysiol. 2010, 104:2532-2542.
69. Porsolt R.D., Lemaire M., Dürmüller N., Roux S. New perspectives in CNS safety pharmacology. Fundam. Clin. Pharmacol. 2002, 16:197-207.
70. Price T.J., Helesic G., Parghi D., Hargreaves K.M., Flores C.M. The neuronal distribution of cannabinoid receptor type 1 in the trigeminal ganglion of the rat. Neuroscience 2003, 120:155-162.
71. Rajasekaran M., Brents L.K., Franks L.N., Moran J.H., Prather P.L. Human metabolites of synthetic cannabinoids JWH-018 and JWH-073 bind with high affinity and act as potent agonists at cannabinoid type-2 receptors. Toxicol. Appl. Pharmacol. 2013, 269:100-108.
72. Redfern W.S., Strang I., Storey S., Heys C., Barnard C., Lawton K., et al. Spectrum of effects detected in the rat functional observational battery following oral administration of non-CNS targeted compounds. J. Pharmacol. Toxicol. Methods 2005, 52:77-82.
73. Reig R., Silberberg G. Multisensory integration in the mouse striatum. Neuron 2014, 83:1200-1212.
74. Schifano F., Corazza O., Deluca P., Davey Z., Di Furia L., Farre M., et al. Psychoactive drug or mystical incense? Overview of the online available information on Spice products. Int. J. Cult. Ment. Health 2009, 2:137-144.
75. Schneider M., Koch M. The cannabinoid agonist WIN 55,212-2 reduces sensorimotor gating and recognition memory in rats. Behav. Pharmacol. 2002, 13:29-37.
76. Sedlacek M., Tipton P.W., Brenowitz S.D. Sustained firing of cartwheel cells in the dorsal cochlear nucleus evokes endocannabinoid release and retrograde suppression of parallel fiber synapses. J. Neurosci. 2011, 31:15807-15817.
77. Seely K.A., Lapoint J., Moran J.H., Fattore L. Spice drugs are more than harmless herbal blends: a review of the pharmacology and toxicology of synthetic cannabinoids. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 2012, 39:234-243.
78. Showalter V.M., Compton D.R., Martin B.R., Abood M.E. 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. 1996, 278:989-999.
79. Takahashi A., Miczek K.A. Neurogenetics of aggressive behavior: studies in rodents. Curr. Top. Behav. Neurosci. 2014, 17:3-44.
80. Tanda G., Pontieri F.E., Frau R., Di Chiara G. Contribution of blockade of the noradrenaline carrier to the increase of extracellular dopamine in the rat prefrontal cortex by amphetamine and cocaine. Eur. J. Neurosci. 1997, 9:2077-2085.
81. Tsou K., Brown S., Sanudo-Pena M.C., Mackie K., Walker J.M. Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience 1998, 83:393-411.
82. Tzounopoulos T., Rubio M.E., Keen J.E., Trussell L.O. Coactivation of pre- and postsynaptic signaling mechanisms determines cell-specific spike-timing-dependent plasticity. Neuron 2007, 54:291-301.
83. Uchiyama N., Kawamura M., Kikura-Hanajiri R., Goda Y. Identification and quantitation of two cannabimimetic phenylacetylindoles JWH-251 and JWH-250, and four cannabimimetic naphthoylindoles JWH-081, JWH-015, JWH-200, and JWH-073 as designer drugs in illegal products. Forensic Toxicol. 2011, 29:25-37.
84. van Ree J.M., Niesink R.J., Nir I. Delta 1-Tetrahydrocannabinol but not cannabidiol reduces contact and aggressive behavior of rats tested in dyadic encounters. Psychopharmacology 1984, 84:561-565.
85. Vigolo A., Ossato A., Trapella C., Vincenzi F., Rimondo C., Seri C., et al. Novel halogenated derivates of JWH-018: behavioral and binding studies in mice. Neuropharmacology 2015, 95:68-82.
86. Vincenzi F., Targa M., Corciulo C., Tabrizi M.A., Merighi S., Gessi S., et al. Antinociceptive effects of the selective CB2 agonist MT178 in inflammatory and chronic rodent pain models. Pain 2013, 154:864-873.
87. Wegener N., Kuhnert S., Thuns A., Roese R., Koch M. Effects of acute systemic and intra-cerebral stimulation of cannabinoid receptors on sensorimotor gating, locomotion and spatial memory in rats. Psychopharmacology 2008, 198:375-385.
88. Wiebelhaus J.M., Poklis J.L., Poklis A., Vann R.E., Lichtman A.H., Wise L.E. Inhalation exposure to smoke from synthetic "marijuana" produces potent cannabimimetic effects in mice. Drug Alcohol Depend. 2012, 126:316-323.
89. Wiley J.L., Compton D.R., Dai D., Lainton J.A., Phillips M., Huffman J.W., et al. Structure-activity relationships of indole- and pyrrole-derived cannabinoids. J. Pharmacol. Exp. Ther. 1998, 285:995-1004.
90. Wiley J.L., Marusich J.A., Huffman J.W. Moving around the molecule: relationship between chemical structure and in vivo activity of synthetic cannabinoids. Life Sci. 2014, 97:55-63.
91. Wintermeyer A., Moller I., Thevis M., Jubner M., Beike J., Rothschild M.A., et al. In vitro phase I metabolism of the synthetic cannabimimetic JWH-018. Anal. Bioanal. Chem. 2010, 398:2141-2153.
92. Winton-Brown T.T., Allen P., Bhattacharyya S., Borgwardt S.J., Fusar-Poli P., Crippa J.A., et al. Modulation of auditory and visual processing by delta-9-tetrahydrocannabinol and cannabidiol: an FMRI study. Neuropsychopharmacology 2011, 36:1340-1348.
93. Xi Z.X., Peng X.Q., Li X., Song R., Zhang H.Y., Liu Q.R., et al. Brain cannabinoid CB(2) receptors modulate cocaine's actions in mice. Nat. Neurosci. 2011, 14:1160-1166.
94. Yoneda T., Kameyama K., Esumi K., Daimyo Y., Watanabe M., Hata Y. Developmental and visual input-dependent regulation of the CB1 cannabinoid receptor in the mouse visual cortex. PLoS One 2013, 8.
95. Zawilska J.B., Wojcieszak J. Spice/K2 drugs-more than innocent substitutes for marijuana. Int. J. Neuropsychopharmacol. 2014, 17:509-525.
96. Zhao Y., Rubio M., Tzounopoulos T. Mechanisms underlying input-specific expression of endocannabinoid-mediated synaptic plasticity in the dorsal cochlear nucleus. Hear. Res. 2011, 279:67-73.