Br J Pharmacol. 2021 Aug 12; doi: 10.1111/bph.15658. Epub 2021 Aug 12.

Diazepam attenuates the effects of cocaine on locomotion, 50-kHz ultrasonic vocalizations and phasic dopamine in the nucleus accumbens of rats.

British journal of pharmacology

William N Sanchez, Jose A Pochapski, Leticia F Jessen, Marek Ellenberger, Rainer K Schwarting, Donita L Robinson, Roberto Andreatini, Claudio Da Cunha

PMID: 34389975 DOI: 10.1111/bph.15658

Abstract

BACKGROUND AND PURPOSE: Currently, there is no effective drug to treat cocaine-use disorder, which affects millions of people worldwide. Benzodiazepines are potential therapeutic candidates, as microdialysis and voltammetry studies have shown that they can decrease dopamine concentrations in the nucleus accumbens of rodents and block the increase in dopamine levels and appetitive 50-kHz ultrasonic vocalizations (USVs) induced by amphetamine in rats.

EXPERIMENTAL APPROACH: Here, we tested whether administration of 2.5-mg·kg

KEY RESULTS: Cocaine injection increased evoked dopamine signals up to threefold within 5 min, and the increase was significantly higher than baseline for at least 75 min. The injection of diazepam, 5 min after cocaine, attenuated the cocaine effect by nearly 50%, and this attenuation was maintained for at least 40 min. Behaviourally, cocaine increased the number of appetitive 50-kHz calls by about 12-fold. Diazepam significantly blocked this effect for the entire duration of the session. Also, cocaine-treated rats were more active than controls and diazepam significantly attenuated cocaine-induced locomotion, by up to 50%.

CONCLUSION AND IMPLICATIONS: These results suggest that the neurochemical and psychostimulant effects of cocaine can be mitigated by diazepam.

© 2021 The British Pharmacological Society.

Keywords: addiction; benzodiazepines; dopamine; psychostimulants

References

1. Alexander, S. P. H., Christopoulos, A., Davenport, A. P., Kelly, E., Mathie, A., Peters, J. A., Veale, E. L., Armstrong, J. F., Faccenda, E., Harding, S. D., Pawson, A. J., Sharman, J. L., Southan, C., Davies, J. A., Abbracchio, M. P., Alexander, W., Al-hosaini, K., Bäck, M., Beaulieu, J., … Yao, C. (2019). The Concise Guide to PHARMACOLOGY 2019/20: G protein-coupled receptors. British Journal of Pharmacology, 176, S21-S141. https://doi.org/10.1111/bph.14748 - PubMed
2. Alexander, S. P. H., Kelly, E., Mathie, A., Peters, J. A., Veale, E. L., Armstrong, J. F., Faccenda, E., Harding, S. D., Pawson, A. J., Sharman, J. L., Southan, C., Davies, J. A., & CGTP Collaborators. (2019). The Concise Guide to PHARMACOLOGY 2019/20: Transporters. British Journal of Pharmacology, 176, S397-S493. https://doi.org/10.1111/bph.14753 - PubMed
3. Alexander, S. P. H., Mathie, A., Peters, J. A., Veale, E. L., Striessnig, J., Kelly, E., Armstrong, J. F., Faccenda, E., Harding, S. D., Pawson, A. J., Sharman, J. L., Southan, C., Davies, J. A., & CGTP Collaborators. (2019). The Concise Guide to PHARMACOLOGY 2019/20: Ion channels. British Journal of Pharmacology, 176, S142-S228. https://doi.org/10.1111/bph.14749 - PubMed
4. Ashby, C., Rohatgi, R., Ngosuwan, J., Borda, T., Gerasimov, M. R., Morgan, A. E., Kushner, S., Brodie, J. D., & Dewey, S. L. (1999). Implication of the GABAb receptor in gamma vinyl-GABA's inhibition of cocaine-induced increases in nucleus accumbens dopamine. Synapse, 153, 151-153. - PubMed
5. Augier, E., Vouillac, C., & Ahmed, S. H. (2012). Diazepam promotes choice of abstinence in cocaine self-administering rats. Addiction Biology, 17, 378-391. https://doi.org/10.1111/j.1369-1600.2011.00368.x - PubMed
6. Auta, J., Kadriu, B., Giusti, P., Costa, E., & Guidotti, A. (2010). Anticonvulsant, anxiolytic, and non-sedating actions of imidazenil and other imidazo-benzodiazepine carboxamide derivatives. Pharmacology, Biochemistry, and Behavior, 95, 383-389. https://doi.org/10.1016/j.pbb.2010.02.016 - PubMed
7. Avvisati, R., Contu, L., Stendardo, E., Michetti, C., Montanari, C., Scattoni, M. L., & Badiani, A. (2016). Ultrasonic vocalization in rats self-administering heroin and cocaine in different settings: Evidence of substance-specific interactions between drug and setting. Psychopharmacology, 233, 1501-1511. https://doi.org/10.1007/s00213-016-4247-4 - PubMed
8. Baldaçara, L., Cogo-Moreira, H., Parreira, B. L., Diniz, T. A., Milhomem, J. J., Fernandes, C. C., & Lacerda, A. L. T. (2016). Efficacy of topiramate in the treatment of crack cocaine dependence: A double-blind, randomized, placebo-controlled trial. The Journal of Clinical Psychiatry, 77, 398-406. https://doi.org/10.4088/JCP.14m09377 - PubMed
9. Barker, D. J., Root, D. H., Ma, S., Jha, S., Megehee, L., Pawlak, A. P., & West, M. O. (2010). Dose-dependent differences in short ultrasonic vocalizations emitted by rats during cocaine self-administration. Psychopharmacology, 211, 435-442. https://doi.org/10.1007/s00213-010-1913-9 - PubMed
10. Barker, D. J., Simmons, S. J., & West, M. O. (2015). Ultrasonic vocalizations as a measure of affect in preclinical models of drug abuse: A review of current findings. Current Neuropharmacology, 13, 193-210. https://doi.org/10.2174/1570159X13999150318113642 - PubMed
11. Barrett, A. C., Stevens Negus, S., Mello, N. K., & Barak Caine, S. (2005). Effect of GABA agonists and GABA-A receptor modulators on cocaine- and food-maintained responding and cocaine discrimination in rats. The Journal of Pharmacology and Experimental Therapeutics, 315, 858-871. https://doi.org/10.1124/jpet.105.086033 - PubMed
12. Bledsoe, J. M., Kimble, C. J., Covey, D. P., Blaha, C. D., Agnesi, F., Mohseni, P., Whitlock, S., Johnson, D. M., Horne, A., Bennet, K. E., Lee, K. H., & Garris, P. A. (2009). Development of the Wireless Instantaneous Neurotransmitter Concentration System for intraoperative neurochemical monitoring using fast-scan cyclic voltammetry: Technical note. Journal of Neurosurgery, 111, 712-723. https://doi.org/10.3171/2009.3.JNS081348 - PubMed
13. Brenes, J. C., Lackinger, M., Höglinger, G. U., Schratt, G., Schwarting, R. K. W., & Wöhr, M. (2016). Differential effects of social and physical environmental enrichment on brain plasticity, cognition, and ultrasonic communication in rats. The Journal of Comparative Neurology, 524, 1586-1607. https://doi.org/10.1002/cne.23842 - PubMed
14. Brenes, J. C., & Schwarting, R. K. W. (2015). Individual differences in anticipatory activity to food rewards predict cue-induced appetitive 50-kHz calls in rats. Physiology & Behavior, 149, 107-118. https://doi.org/10.1016/j.physbeh.2015.05.012 - PubMed
15. Brodnik, Z. D., Batra, A., Oleson, E. B., & Espana, R. A. (2019). Local GABAA receptor-mediated suppression of dopamine release within the nucleus accumbens. ACS Chemical Neuroscience, 10, 1978-1985. https://doi.org/10.1021/acschemneuro.8b00268 - PubMed
16. Browning, J. R., Browning, D. A., Maxwell, A. O., Dong, Y., Jansen, H. T., Panksepp, J., & Sorg, B. A. (2011). Positive affective vocalizations during cocaine and sucrose self-administration: A model for spontaneous drug desire in rats. Neuropharmacology, 61, 268-275. https://doi.org/10.1016/j.neuropharm.2011.04.012 - PubMed
17. Brudzynski, S. (2015). Pharmacology of ultrasonic vocalizations in adult rats: Significance, call classification and neural substrate. Current Neuropharmacology, 13, 180-192. https://doi.org/10.2174/1570159X13999150210141444 - PubMed
18. Brudzynski, S. M., Komadoski, M., & Pierre, J. S. (2012). Quinpirole-induced 50 kHz ultrasonic vocalization in the rat: Role of D2 and D3 dopamine receptors. Behavioural Brain Research, 226, 511-518. https://doi.org/10.1016/j.bbr.2011.10.004 - PubMed
19. Budygin, E. A., Bass, C. E., Grinevich, V. P., Deal, A. L., Bonin, K. D., & Weiner, J. L. (2020). Opposite consequences of tonic and phasic increases in accumbal dopamine on alcohol-seeking behavior. iScience, 23, 100877. https://doi.org/10.1016/j.isci.2020.100877 - PubMed
20. Burgdorf, J., Knutson, B., Panksepp, J., & Ikemoto, S. (2001). Nucleus accumbens amphetamine microinjections unconditionally elicit 50-kHz ultrasonic vocalizations in rats. Behavioral Neuroscience, 115, 940-944. https://doi.org/10.1037/0735-7044.115.4.940 - PubMed
21. Burgdorf, J., Kroes, R. A., Moskal, J. R., Pfaus, J. G., Brudzynski, S. M., & Panksepp, J. (2008). Ultrasonic vocalizations of rats (Rattus norvegicus) during mating, play, and aggression: Behavioral concomitants, relationship to reward, and self-administration of playback. Journal of Comparative Psychology, 122, 357-367. https://doi.org/10.1037/a0012889 - PubMed
22. Burgdorf, J., Wood, P. L., Kroes, R. A., Moskal, J. R., & Panksepp, J. (2007). Neurobiology of 50-kHz ultrasonic vocalizations in rats: Electrode mapping, lesion, and pharmacology studies. Behavioural Brain Research, 182, 274-283. https://doi.org/10.1016/j.bbr.2007.03.010 - PubMed
23. Calcaterra, N. E., & Barrow, J. C. (2014). Classics in chemical neuroscience: Diazepam (valium). ACS Chemical Neuroscience, 5, 253-260. https://doi.org/10.1021/cn5000056 - PubMed
24. Çelik, T., Deniz, G., Uzbay, I. T., Palaoǧlu, Ö., & Ayhan, I. H. (1999). The effects of flumazenil on two way active avoidance and locomotor activity in diazepam-treated rats. European Neuropsychopharmacology, 9, 45-50. https://doi.org/10.1016/S0924-977X(97)00101-6 - PubMed
25. Church, W. H., Justice, J. B., & Byrd, L. D. (1987). Extracellular dopamine in rat striatum following uptake inhibition by cocaine, nomifensine and benztropine. European Journal of Pharmacology, 139, 345-348. https://doi.org/10.1016/0014-2999(87)90592-9 - PubMed
26. Coffey, K. R., Marx, R. G., & Neumaier, J. F. (2019). DeepSqueak: A deep learning-based system for detection and analysis of ultrasonic vocalizations. Neuropsychopharmacology, 44, 859-868. https://doi.org/10.1038/s41386-018-0303-6 - PubMed
27. Curtis, M. J., Alexander, S., Cirino, G., Docherty, J. R., George, C. H., Giembycz, M. A., Hoyer, D., Insel, P. A., Izzo, A. A., Ji, Y., MacEwan, D. J., Sobey, C. G., Stanford, S. C., Teixeira, M. M., Wonnacott, S., & Ahluwalia, A. (2018). Experimental design and analysis and their reporting II: Updated and simplified guidance for authors and peer reviewers. British Journal of Pharmacology, 175, 987-993. https://doi.org/10.1111/bph.14153 - PubMed
28. De Guglielmo, G., Cippitelli, A., Somaini, L., Gerra, G., Li, H., Stopponi, S., Ubaldi, M., Kallupi, M., & Ciccocioppo, R. (2013). Pregabalin reduces cocaine self-administration and relapse to cocaine seeking in the rat. Addiction Biology, 18, 644-653. https://doi.org/10.1111/j.1369-1600.2012.00468.x - PubMed
29. de Oliveira Guaita, G., Dalla Vecchia, D., Andreatini, R., Robinson, D. L., Schwarting, R. K., & Da Cunha, C. (2018). Diazepam blocks 50 kHz ultrasonic vocalizations and stereotypies but not the increase in locomotor activity induced in rats by amphetamine. Psychopharmacology, 235, 1887-1896. https://doi.org/10.1007/s00213-018-4878-8 - PubMed
30. Delfs, J. M., Schreiber, L., & Kelley, A. E. (1990). Microinjection of cocaine into the nucleus accumbens elicits locomotor activation in the rat. The Journal of Neuroscience, 10, 303-310. https://doi.org/10.1523/JNEUROSCI.10-01-00303.1990 - PubMed
31. Dewey, S. L., Chaurasia, C. S., Chen, C. E. N., Volkow, N. D., Clarkson, F. A., Porter, S. P., Straughter-Moore, R. M., Alexoff, D. L., Tedeschi, D., Russo, N. B., & Fowler, J. S. (1997). GABAergic attenuation of cocaine-induced dopamine release and locomotor activity. Synapse, 25, 393-398. https://doi.org/10.1002/(SICI)1098-2396(199704)25:4<393::AID-SYN11>3.0.CO;2-W - PubMed
32. Dewey, S. L., Smith, G. S., Logan, J., Brodie, J. D., Yu, D. W., Ferrieri, R. A., King, P. T., MacGregor, R., Martin, T. P., & Wolf, A. P. (1992). GABAergic inhibition of endogenous dopamine release measured in vivo with 11C-raclopride and positron emission tomography. The Journal of Neuroscience, 12, 3773-3780. https://doi.org/10.1523/JNEUROSCI.12-10-03773.1992 - PubMed
33. Divljaković, J., Milić, M., Timić, T., & Savić, M. M. (2012). Tolerance liability of diazepam is dependent on the dose used for protracted treatment. Pharmacological Reports, 64, 1116-1125. https://doi.org/10.1016/S1734-1140(12)70908-8 - PubMed
34. Dornellas, A. P. S., Macedo, G. C., McFarland, M. H., Gómez-A, A., O'Buckley, T. K., Da Cunha, C., Morrow, A. L., & Robinson, D. L. (2021). Allopregnanolone decreases evoked dopamine release differently in rats by sex and estrous stage. Frontiers in Pharmacology, 11, 608887. https://doi.org/10.3389/fphar.2020.608887 - PubMed
35. Engelhardt, K. A., Fuchs, E., Schwarting, R. K. W., & Wöhr, M. (2017). Effects of amphetamine on pro-social ultrasonic communication in juvenile rats: Implications for mania models. European Neuropsychopharmacology, 27, 261-273. https://doi.org/10.1016/j.euroneuro.2017.01.003 - PubMed
36. Farrell, M., Martin, N. K., Stockings, E., Bórquez, A., Cepeda, J. A., Degenhardt, L., Ali, R., Tran, L. T., Rehm, J., Torrens, M., Shoptaw, S., & McKetin, R. (2019). Responding to global stimulant use: Challenges and opportunities. Lancet, 394, 1652-1667. https://doi.org/10.1016/S0140-6736(19)32230-5 - PubMed
37. Fernandes, C., File, S. E., & Berry, D. (1996). Evidence against oppositional and pharmacokinetic mechanisms of tolerance to diazepam's sedative effects. Brain Research, 734, 236-242. https://doi.org/10.1016/0006-8993(96)00644-0 - PubMed
38. Finlay, J. M., Damsma, G., & Fibiger, H. C. (1992). Benzodiazepine-induced decreases in extracellular concentrations of dopamine in the nucleus accumbens after acute and repeated administration. Psychopharmacology, 106, 202-208. https://doi.org/10.1007/BF02801973 - PubMed
39. Finn, I. B., & Holtzman, S. G. (1987). Pharmacologic specificity of tolerance to caffeine-induced stimulation of locomotor activity. Psychopharmacology, 93, 428-434. https://doi.org/10.1007/BF00207230 - PubMed
40. Fotros, A., Casey, K. F., Larcher, K., Verhaeghe, J. A. J., Cox, S. M. L., Gravel, P., Reader, A. J., Dagher, A., Benkelfat, C., & Leyton, M. (2013). Cocaine cue-induced dopamine release in amygdala and hippocampus: A high-resolution PET [18F]fallypride study in cocaine dependent participants. Neuropsychopharmacology, 38, 1780-1788. https://doi.org/10.1038/npp.2013.77 - PubMed
41. Garris, P. A., Budygin, E. A., Phillips, P. E. M., Venton, B. J., Robinson, D. L., Bergstrom, B. P., Rebec, G. V., & Wightman, R. M. (2003). A role for presynaptic mechanisms in the actions of nomifensine and haloperidol. Neuroscience, 118, 819-829. https://doi.org/10.1016/S0306-4522(03)00005-8 - PubMed
42. Garris, P. A., & Wightman, R. M. (1995). Distinct pharmacological regulation of evoked dopamine efflux in the amygdala and striatum of the rat in vivo. Synapse, 20, 269-279. https://doi.org/10.1002/syn.890200311 - PubMed
43. Giorgetti, M., Hotsenpiller, G., Froestl, W., & Wolf, M. E. (2002). In vivo modulation of ventral tegmental area dopamine and glutamate efflux by local GABAB receptors is altered after repeated amphetamine treatment. Neuroscience, 109, 585-595. https://doi.org/10.1016/S0306-4522(01)00510-3 - PubMed
44. Giorgetti, M., Javaid, J. I., Davis, J. M., Costa, E., Guidotti, A., Appel, S. B., & Brodie, M. S. (1998). Imidazenil, a positive allosteric GABAA receptor modulator, inhibits the effects of cocaine on locomotor activity and extracellular dopamine in the nucleus accumbens shell without tolerance liability. Journal of Pharmacology and Experimental Therapeutics, 287, 58-66. - PubMed
45. Goeders, N. E., Clampitt, D. M., Keller, C., Sharma, M., & Guerin, G. F. (2009). Alprazolam and oxazepam block the cue-induced reinstatement of extinguished cocaine seeking in rats. Psychopharmacology, 201, 581-588. https://doi.org/10.1007/s00213-008-1326-1 - PubMed
46. Goeders, N. E., McNulty, M. A., & Guerin, G. F. (1993). Effects of alprazolam on intravenous cocaine self-administration in rats. Pharmacology, Biochemistry, and Behavior, 44, 471-474. https://doi.org/10.1016/0091-3057(93)90493-D - PubMed
47. Gomez-A, A., Fiorenza, A. M., Boschen, S. L., Sugi, A. H., Beckman, D., Ferreira, S. T., Lee, K., Blaha, C. D., & da Cunha, C. (2017). Diazepam inhibits electrically evoked and tonic dopamine release in the nucleus accumbens and reverses the effect of amphetamine. ACS Chemical Neuroscience, 8, 300-309. https://doi.org/10.1021/acschemneuro.6b00358 - PubMed
48. Heien, M. L. A. V., Khan, A. S., Ariansen, J. L., Cheer, J. F., Phillips, P. E. M., Wassum, K. M., & Wightman, R. M. (2005). Real-time measurement of dopamine fluctuations after cocaine in the brain of behaving rats. Proceedings of the National Academy of Sciences of the United States of America, 102, 10023-10028. https://doi.org/10.1073/pnas.0504657102 - PubMed
49. Hernandez, L., & Hoebel, B. G. (1988). Food reward and cocaine increase extracellular dopamine in the nucleus accumbens as measured by microdialysis. Life Sciences, 42, 1705-1712. https://doi.org/10.1016/0024-3205(88)90036-7 - PubMed
50. Ikemoto, S. (2002). Ventral striatal anatomy of locomotor activity induced by cocaine, D-amphetamine, dopamine and D1/D2 agonists. Neuroscience, 113, 939-955. https://doi.org/10.1016/S0306-4522(02)00247-6 - PubMed
51. Kablinger, A. S., Lindner, M. A., Casso, S., Hefti, F., Demuth, G., Fox, B. S., McNair, L. A., McCarthy, B. G., & Goeders, N. E. (2012). Effects of the combination of metyrapone and oxazepam on cocaine craving and cocaine taking: A double-blind, randomized, placebo-controlled pilot study. Journal of Psychopharmacology, 26, 973-981. https://doi.org/10.1177/0269881111430745 - PubMed
52. Kalivas, P. W. (2007). Cocaine and amphetamine-like psychostimulants: Neurocircuitry and glutamate neuroplasticity. Dialogues in Clinical Neuroscience, 9, 389-397. - PubMed
53. Kampman, K. M. (2019). The treatment of cocaine use disorder. Science Advances, 5, 1-9. - PubMed
54. Kampman, K. M., Pettinati, H., Lynch, K. G., Dackis, C., Sparkman, T., Weigley, C., & O'Brien, C. P. (2004). A pilot trial of topiramate for the treatment of cocaine dependence. Drug and Alcohol Dependence, 75, 233-240. https://doi.org/10.1016/j.drugalcdep.2004.03.008 - PubMed
55. Keller, C. M., Cornett, E. M., Guerin, G. F., & Goeders, N. E. (2013). Combinations of oxazepam and metyrapone attenuate cocaine and methamphetamine cue reactivity. Drug and Alcohol Dependence, 133, 405-412. https://doi.org/10.1016/j.drugalcdep.2013.06.025 - PubMed
56. Keller, C. M., & Goeders, N. E. (2019). Lack of effect of the combination of metyrapone and oxazepam on brain dopamine. Brain Research, 1724, 146435. https://doi.org/10.1016/j.brainres.2019.146435 - PubMed
57. Kiyatkin, E. A., & Bae, D. (2008). Behavioral and brain temperature responses to salient environmental stimuli and intravenous cocaine in rats: Effects of diazepam. Psychopharmacology, 196, 343-356. https://doi.org/10.1007/s00213-007-0965-y - PubMed
58. Kramar, C. P., Chefer, V. I., Wise, R. A., Medina, J. H., & Barbano, M. F. (2014). Dopamine in the dorsal hippocampus impairs the late consolidation of cocaine-associated memory. Neuropsychopharmacology, 39, 1645-1653. https://doi.org/10.1038/npp.2014.11 - PubMed
59. Kramer, P. F., Twedell, E. L., Shin, J. H., Zhang, R., & Khaliq, Z. M. (2020). Axonal mechanisms mediating GABA-A receptor inhibition of striatal dopamine release. eLife, 9, e55729. - PubMed
60. Lilley, E., Stanford, S. C., Kendall, D. E., Alexander, S. P. H., Cirino, G., Docherty, J. R., George, C. H., Insel, P. A., Izzo, A. A., Ji, Y., Panettieri, R. A., Sobey, C. G., Stefanska, B., Stephens, G., Teixeira, M., & Ahluwalia, A. (2020). ARRIVE 2.0 and the British Journal of Pharmacology: Updated guidance for 2020. British Journal of Pharmacology, 177, 3611-3616. https://doi.org/10.1111/bph.15178 - PubMed
61. Lopes, E. F., Roberts, B. M., Siddorn, R. E., Clements, M. A., & Cragg, S. J. (2019). Inhibition of nigrostriatal dopamine release by striatal GABAA and GABAB receptors. The Journal of Neuroscience, 39, 1058-1065. https://doi.org/10.1523/JNEUROSCI.2028-18.2018 - PubMed
62. Maier, E. Y., Ahrens, A. M., Ma, S. T., Schallert, T., & Duvauchelle, C. L. (2010). Cocaine deprivation effect: Cue abstinence over weekends boosts anticipatory 50-kHz ultrasonic vocalizations in rats. Behavioural Brain Research, 214, 75-79. https://doi.org/10.1016/j.bbr.2010.04.057 - PubMed
63. Maier, E. Y., Ledesma, R. T., Seiwell, A. P., & Duvauchelle, C. L. (2008). Diazepam alters cocaine self-administration, but not cocaine-stimulated locomotion or nucleus accumbens dopamine. Pharmacology, Biochemistry, and Behavior, 91, 202-207. https://doi.org/10.1016/j.pbb.2008.07.008 - PubMed
64. Masiulis, S., Desai, R., Uchański, T., Serna Martin, I., Laverty, D., Karia, D., Malinauskas, T., Zivanov, J., Pardon, E., Kotecha, A., Steyaert, J., Miller, K. W., & Aricescu, A. R. (2019). GABAA receptor signalling mechanisms revealed by structural pharmacology. Nature, 565, 454-459. https://doi.org/10.1038/s41586-018-0832-5 - PubMed
65. Meririnne, E., Kankaanpää, A., Lillsunde, P., & Seppälä, T. (1999). The effects of diazepam and zolpidem on cocaine- and amphetamine-induced place preference. Pharmacology, Biochemistry, and Behavior, 62, 159-164. https://doi.org/10.1016/S0091-3057(98)00139-7 - PubMed
66. Mohebi, A., Pettibone, J. R., Hamid, A. A., Wong, J.-M. T., Vinson, L. T., Patriarchi, T., Tian, L., Kennedy, R. T., & Berke, J. D. (2019). Dissociable dopamine dynamics for learning and motivation. Nature, 570, 65-70. https://doi.org/10.1038/s41586-019-1235-y - PubMed
67. Mu, P., Fuchs, T., Saal, D. B., Sorg, B. A., Dong, Y., & Panksepp, J. (2009). Repeated cocaine exposure induces sensitization of ultrasonic vocalization in rats. Neuroscience Letters, 453, 31-35. https://doi.org/10.1016/j.neulet.2009.02.007 - PubMed
68. Murai, T., Koshikawa, N., Kanayama, T., Takada, K., Tomiyama, K., & Kobayashi, M. (1994). Opposite effects of midazolam and β-carboline-3-carboxylate ethyl ester on the release of dopamine from rat nucleus accumbens measured by in vivo mudialysis. European Journal of Pharmacology, 261, 65-71. https://doi.org/10.1016/0014-2999(94)90301-8 - PubMed
69. Negus, S. S., Mello, N. K., & Fivel, P. A. (2000). Effects of GABA agonists and GABA-A receptor modulators on cocaine discrimination in rhesus monkeys. Psychopharmacology, 152, 398-407. https://doi.org/10.1007/s002130000543 - PubMed
70. Nicola, S. M., & Deadwyler, S. A. (2000). Firing rate of nucleus accumbens neurons is dopamine-dependent and reflects the timing of cocaine-seeking behavior in rats on a progressive ratio schedule of reinforcement. The Journal of Neuroscience, 20, 5526-5537. https://doi.org/10.1523/JNEUROSCI.20-14-05526.2000 - PubMed
71. Paxinos, G., & Watson, C. (1998). The rat brain in stereotaxic coordinates. Academic Press. - PubMed
72. Percie du Sert, N., Hurst, V., Ahluwalia, A., Alam, S., Avey, M. T., Baker, M., Browne, W. J., Clark, A., Cuthill, I. C., Dirnagl, U., Emerson, M., Garner, P., Holgate, S. T., Howells, D. W., Karp, N. A., Lazic, S. E., Lidster, K., MacCallum, C. J., Macleod, M., … Würbel, H. (2020). The ARRIVE guidelines 2.0: Updated guidelines for reporting animal research. PLoS Biology, 18(7), e3000410. https://doi.org/10.1371/journal.pbio.3000410 - PubMed
73. Pereira, M., Andreatini, R., Schwarting, R. K. W., & Brenes, J. C. (2014). Amphetamine-induced appetitive 50-kHz calls in rats: A marker of affect in mania? Psychopharmacology, 231, 2567-2577. https://doi.org/10.1007/s00213-013-3413-1 - PubMed
74. Quinones-Jenab, V., & Jenab, S. (2010). Progesterone attenuates cocaine-induced responses. Hormones and Behavior, 58, 22-32. https://doi.org/10.1016/j.yhbeh.2009.10.002 - PubMed
75. Quinton, M. S., Gerak, L. R., Moerschbaecher, J. M., & Winsauer, P. J. (2005). Interaction of cocaine with positive GABAA modulators on the repeated acquisition and performance of response sequences in rats. Psychopharmacology, 181, 217-226. https://doi.org/10.1007/s00213-005-2241-3 - PubMed
76. Quinton, M. S., Gerak, L. R., Moerschbaecher, J. M., & Winsauer, P. J. (2006). Effects of pregnanolone in rats discriminating cocaine. Pharmacology, Biochemistry, and Behavior, 85, 385-392. https://doi.org/10.1016/j.pbb.2006.09.006 - PubMed
77. Ringel, L. E., Basken, J. N., Grant, L. M., & Ciucci, M. R. (2013). Dopamine D1 and D2 receptor antagonism effects on rat ultrasonic vocalizations. Behavioural Brain Research, 252, 252-259. https://doi.org/10.1016/j.bbr.2013.06.006 - PubMed
78. Rippberger, H., van Gaalen, M., Schwarting, R., & Wohr, M. (2015). Environmental and pharmacological modulation of amphetamine-induced 50-kHz ultrasonic vocalizations in rats. Current Neuropharmacology, 13, 220-232. https://doi.org/10.2174/1570159X1302150525124408 - PubMed
79. Roberts, B. M., Lopes, E. F., & Cragg, S. J. (2021). Axonal modulation of striatal dopamine release by local γ-aminobutyric acid (GABA) signalling. Cell, 709, 1-17. - PubMed
80. Scardochio, T., Trujillo-Pisanty, I., Conover, K., Shizgal, P., & Clarke, P. B. S. (2015). The effects of electrical and optical stimulation of midbrain dopaminergic neurons on rat 50-kHz ultrasonic vocalizations. Frontiers in Behavioral Neuroscience, 9, 1-15. - PubMed
81. Schelp, S. A., Brodnik, Z. D., Rakowski, D. R., Pultorak, K. J., Sambells, A. T., España, R. A., & Oleson, E. B. (2018). Diazepam concurrently increases the frequency and decreases the amplitude of transient dopamine release events in the nucleus accumbens. The Journal of Pharmacology and Experimental Therapeutics, 364, 145-155. https://doi.org/10.1124/jpet.117.241802 - PubMed
82. Schmoutz, C. D., Guerin, G. F., Runyon, S. P., Dhungana, S., & Goeders, N. E. (2015). A therapeutic combination of metyrapone and oxazepam increases brain levels of GABA-active neurosteroids and decreases cocaine self-administration in male rats. Behavioural Brain Research, 291, 108-111. https://doi.org/10.1016/j.bbr.2015.05.019 - PubMed
83. Schultz, W. (2007). Multiple dopamine functions at different time courses. Annual Review of Neuroscience, 30, 259-288. https://doi.org/10.1146/annurev.neuro.28.061604.135722 - PubMed
84. Sellings, L. H. L., McQuade, L. E., & Clarke, P. B. S. (2006). Evidence for multiple sites within rat ventral striatum mediating cocaine-conditioned place preference and locomotor activation. The Journal of Pharmacology and Experimental Therapeutics, 317, 1178-1187. https://doi.org/10.1124/jpet.105.100339 - PubMed
85. Simola, N., & Brudzynski, S. M. (2018). Rat 50-kHz ultrasonic vocalizations as a tool in studying neurochemical mechanisms that regulate positive emotional states. Journal of Neuroscience Methods, 310, 33-44. https://doi.org/10.1016/j.jneumeth.2018.06.018 - PubMed
86. Takada, K., Murai, T., Kanayama, T., & Koshikawa, N. (1993). Effects of midazolam and flunitrazepam on the release of dopamine from rat striatum measured by in vivo microdialysis. British Journal of Anaesthesia, 70, 181-185. https://doi.org/10.1093/bja/70.2.181 - PubMed
87. Tan, K. R., Brown, M., Labouébe, G., Yvon, C., Creton, C., Fritschy, J. M., Rudolph, U., & Lüscher, C. (2010). Neural bases for addictive properties of benzodiazepines. Nature, 463, 769-774. https://doi.org/10.1038/nature08758 - PubMed
88. Thompson, B., Leonard, K. C., & Brudzynski, S. M. (2006). Amphetamine-induced 50 kHz calls from rat nucleus accumbens: A quantitative mapping study and acoustic analysis. Behavioural Brain Research, 168, 64-73. https://doi.org/10.1016/j.bbr.2005.10.012 - PubMed
89. Tripi, J. A., Dent, M. L., & Meyer, P. J. (2017). Individual differences in food cue responsivity are associated with acute and repeated cocaine-induced vocalizations, but not cue-induced vocalizations. Psychopharmacology, 234, 437-446. https://doi.org/10.1007/s00213-016-4476-6 - PubMed
90. Uusi-Oukari, M., & Korpi, E. R. (2010). Regulation of GABAA receptor subunit expression by pharmacological agents. Pharmacological Reviews, 62, 97-135. https://doi.org/10.1124/pr.109.002063 - PubMed
91. Volkow, N. D., Fowler, J. S., & Wang, G. J. (1999). Imaging studies on the role of dopamine in cocaine reinforcement and addiction in humans. Behavioural Pharmacology, 13, 355-366. - PubMed
92. Wang, K. H., Penmatsa, A., & Gouaux, E. (2015). Neurotransmitter and psychostimulant recognition by the dopamine transporter. Nature, 521, 322-327. https://doi.org/10.1038/nature14431 - PubMed
93. Weerts, E. M., Froestl, W., & Griffiths, R. R. (2005). Effects of GABAergic modulators on food and cocaine self-administration in baboons. Drug and Alcohol Dependence, 80, 369-376. https://doi.org/10.1016/j.drugalcdep.2005.05.006 - PubMed
94. Wendler, E., de Souza, C. P., Vecchia, D. D., Kanazawa, L. K. S., de Almeida Soares Hocayen, P., Wöhr, M., Schwarting, R. K. W., & Andreatini, R. (2016). Evaluation of 50-kHz ultrasonic vocalizations in animal models of mania: Ketamine and lisdexamfetamine-induced hyperlocomotion in rats. European Neuropsychopharmacology, 26, 1900-1908. https://doi.org/10.1016/j.euroneuro.2016.10.012 - PubMed
95. Williams, S. N., & Undieh, A. S. (2010). Brain-derived neurotrophic factor signaling modulates cocaine induction of reward-associated ultrasonic vocalization in rats. The Journal of Pharmacology and Experimental Therapeutics, 332, 463-468. https://doi.org/10.1124/jpet.109.158535 - PubMed
96. Wise, R. A., & Robble, M. A. (2020). Dopamine and addiction. Annual Review of Psychology, 71, 79-106. https://doi.org/10.1146/annurev-psych-010418-103337 - PubMed
97. Wöhr, M. (2021). Measuring mania-like elevated mood through amphetamine-induced 50-kHz ultrasonic vocalizations in rats. British Journal of Pharmacology, 1-19. https://doi.org/10.1111/bph.15487 Online ahead of print - PubMed
98. Wöhr, M., Rippberger, H., Schwarting, R. K. W., & Van Gaalen, M. M. (2015). Critical involvement of 5-HT2C receptor function in amphetamine-induced 50-kHz ultrasonic vocalizations in rats. Psychopharmacology, 232, 1817-1829. https://doi.org/10.1007/s00213-014-3814-9 - PubMed
99. Wright, J., Dobosiewicz, M., & Clarke, P. (2012). α- and β-adrenergic receptors differentially modulate the emission of spontaneous and amphetamine-induced 50-kHz ultrasonic vocalizations in adult rats. Neuropsychopharmacology, 37, 808-821. https://doi.org/10.1038/npp.2011.258 - PubMed
100. Yang, H., de Jong, J. W., Tak, Y. E., Peck, J., Bateup, H. S., & Lammel, S. (2018). Nucleus accumbens subnuclei regulate motivated behavior via direct inhibition and disinhibition of VTA dopamine subpopulations. Neuron, 97, 434-449.e4. - PubMed
101. Yoshida, Y., Koide, S., Hirose, N., Takada, K., Saigusa, T., & Koshikawa, N. (1999). In vivo microdialysis evidence that midazolam facilitates propofol-induced reduction in rat accumbal dopamine release. Neuroscience Research Communications, 25, 121-127. https://doi.org/10.1002/(SICI)1520-6769(199911/12)25:3<121::AID-NRC1>3.0.CO;2-Q - PubMed
102. Zarrindast, M. R., & Dibayan, M. (1989). Involvement of GABAA receptor sites in diazepam hypothermia. General Pharmacology, 20, 855-859. https://doi.org/10.1016/0306-3623(89)90343-1 - PubMed
103. Zetterström, T., & Fillenz, M. (1990). Local administration of flurazepam has different effects on dopamine release in striatum and nucleus accumbens: A microdialysis study. Neuropharmacology, 29, 129-134. https://doi.org/10.1016/0028-3908(90)90052-S - PubMed
104. Zhu, S., Noviello, C. M., Teng, J., Walsh, R. M., Kim, J. J., & Hibbs, R. E. (2018). Structure of a human synaptic GABAA receptor. Nature, 559, 67-88. https://doi.org/10.1038/s41586-018-0255-3 - PubMed

Publication Types

• Journal Article

Grant support

• 306855/2017-8/Conselho Nacional de Desenvolvimento Científico e Tecnológico
• 432061/2018-5/Conselho Nacional de Desenvolvimento Científico e Tecnológico
• 465346/2014-60/Conselho Nacional de Desenvolvimento Científico e Tecnológico
• 312201/2019-2/Conselho Nacional de Desenvolvimento Científico e Tecnológico
• 01.19.0153-00/Financiadora de Estudos e Projetos
• 57446778/Deutscher Akademischer Austauschdienst
• SCHW 559/15-1/Deutsche Forschungsgemeinschaft
• 88881.198683/2018-01/Coordenação de Aperfeiçoamento de Pessoal de Nível Superior