Withdrawal from Acute Amphetamine Induces an Amygdala-Driven Attenuation of Dopamine Neuron Activity: Reversal by Ketamine

Neuropsychopharmacology

Volumn 41, Issue 2, 2016, Pages 619-627

  Belujon, Pauline ^a,b   Jakobowski, Nicole L ^a   Dollish, Hannah K ^a   Grace, Anthony A ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHETAMINE; KETAMINE; AMINO ACID RECEPTOR BLOCKING AGENT; CENTRAL STIMULANT AGENT; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASOLATERAL AMYGDALA; CONTROLLED STUDY; DOPAMINERGIC ACTIVITY; DOPAMINERGIC NERVE CELL; ELECTROPHYSIOLOGICAL PROCEDURES; FORCED SWIM TEST; IMMOBILITY; IN VIVO STUDY; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; VENTRAL TEGMENTUM; WITHDRAWAL SYNDROME; ACTION POTENTIAL; AMPHETAMINE-RELATED DISORDERS; ANIMAL; ANTAGONISTS AND INHIBITORS; DISEASE MODEL; DRUG EFFECTS; METABOLISM; MOTOR ACTIVITY; PATHOPHYSIOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT; SUBSTANCE WITHDRAWAL SYNDROME; TIME FACTOR;

ACTION POTENTIALS; AMPHETAMINE; AMPHETAMINE-RELATED DISORDERS; ANIMALS; BASOLATERAL NUCLEAR COMPLEX; CENTRAL NERVOUS SYSTEM STIMULANTS; DISEASE MODELS, ANIMAL; DOPAMINERGIC NEURONS; EXCITATORY AMINO ACID ANTAGONISTS; KETAMINE; MALE; MOTOR ACTIVITY; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; SUBSTANCE WITHDRAWAL SYNDROME; TIME FACTORS; VENTRAL TEGMENTAL AREA;

EID: 84949625339     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2015.191     Document Type: Article

References (58)

1. Bardo MT, Valone JM, Bevins RA (1999). Locomotion and conditioned place preference produced by acute intravenous amphetamine: role of dopamine receptors and individual differences in amphetamine self-administration. Psychopharmacology (Berl) 143: 39-46.
2. Belujon P, Grace AA (2014). Restoring mood balance in depression: ketamine reverses deficit in dopamine-dependent synaptic plasticity. Biol Psychiatry 76: 927-936.
3. Berridge KC, Robinson TE, Aldridge JW (2009). Dissecting components of reward: 'liking', 'wanting', and learning. Curr Opin Pharmacol 9: 65-73.
4. Bradberry CW, Roth RH (1989). Cocaine increases extracellular dopamine in rat nucleus accumbens and ventral tegmental area as shown by in vivo microdialysis. Neurosci Lett 103: 97-102.
5. Carboni E, Imperato A, Perezzani L, Di Chiara G (1989). Amphetamine, cocaine, phencyclidine and nomifensine increase extracellular dopamine concentrations preferentially in the nucleus accumbens of freely moving rats. Neuroscience 28: 653-661.
6. Carelli RM, Williams JG, Hollander JA (2003). Basolateral amygdala neurons encode cocaine self-administration and cocaineassociated cues. J Neurosci 23: 8204-8211.
7. Chang CH, Grace AA (2014). Amygdala-ventral pallidum pathway decreases dopamine activity after chronic mild stress in rats. Biol Psychiatry 76: 223-230.
8. Conway KP, Compton W, Stinson FS, Grant BF (2006). Lifetime comorbidity of DSM-IV mood and anxiety disorders and specific drug use disorders: results from the National Epidemiologic Survey on Alcohol and Related Conditions. J Clin Psychiatry 67: 247-257.
9. Cryan JF, Hoyer D, Markou A (2003). Withdrawal from chronic amphetamine induces depressive-like behavioral effects in rodents. Biol Psychiatry 54: 49-58.
10. Cryan JF, Lucki I (2000). 5-HT4 receptors do not mediate the antidepressant-like behavioral effects of fluoxetine in a modified forced swim test. Eur J Pharmacol 409: 295-299.
11. Cryan JF, Markou A, Lucki I (2002). Assessing antidepressant activity in rodents: recent developments and future needs. Trends Pharmacol Sci 23: 238-245.
12. Der-Avakian A, Markou A (2010). Withdrawal from chronic exposure to amphetamine, but not nicotine, leads to an immediate and enduring deficit in motivated behavior without affecting social interaction in rats. Behav Pharmacol 21: 359-368.
13. Der-Avakian A, Markou A (2012). The neurobiology of anhedonia and other reward-related deficits. Trends Neurosci 35: 68-77.
14. Einhorn LC, Johansen PA, White FJ (1988). Electrophysiological effects of cocaine in the mesoaccumbens dopamine system: studies in the ventral tegmental area. J Neurosci 8: 100-112.
15. Floresco SB, West AR, Ash B, Moore H, Grace AA (2003). Afferent modulation of dopamine neuron firing differentially regulates tonic and phasic dopamine transmission. Nat Neurosci 6: 968-973.
16. Fox HC, Hong KI, Siedlarz K, Sinha R (2008). Enhanced sensitivity to stress and drug/alcohol craving in abstinent cocaine-dependent individuals compared to social drinkers. Neuropsychopharmacology 33: 796-805.
17. Garcia LS, Comim CM, Valvassori SS, Reus GZ, Barbosa LM, Andreazza AC et al (2008). Acute administration of ketamine induces antidepressant-like effects in the forced swimming test and increases BDNF levels in the rat hippocampus. Prog Neuropsychopharmacol Biol Psychiatry 32: 140-144.
18. Grace AA, Bunney BS (1983). Intracellular and extracellular electrophysiology of nigral dopaminergic neurons-1. Identification and characterization. Neuroscience 10: 301-315.
19. Grace AA, Bunney BS (1984). The control of firing pattern in nigral dopamine neurons: burst firing. J Neurosci 4: 2877-2890.
20. Horner KA, Noble ES, Lauterbach EC (2009). Differential regulation of prodynophin, c-fos, and serotonin transporter mRNA following withdrawal from a chronic, escalating dose regimen of D-amphetamine. Synapse 63: 257-268.
21. Huang AC, Hsiao S (2002). Haloperidol attenuates rewarding and aversively conditioned suppression of saccharin solution intake: reevaluation of the anhedonia hypothesis of dopamine blocking. Behav Neurosci 116: 646-650.
22. Koob GF (1992). Drugs of abuse: anatomy, pharmacology and function of reward pathways. Trends Pharmacol Sci 13: 177-184.
23. Koob GF (2009). Brain stress systems in the amygdala and addiction. Brain Res 1293: 61-75.
24. Koob GF, Le Moal M (2001). Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology 24: 97-129.
25. Koob GF, Le Moal M (2008). Review. Neurobiological mechanisms for opponent motivational processes in addiction. Philos Trans R Soc Lond B Biol Sci 363: 3113-3123.
26. Koob GF, Volkow ND (2010). Neurocircuitry of addiction. Neuropsychopharmacology 35: 217-238.
27. Kornetsky C, Esposito RU (1979). Euphorigenic drugs: effects on the reward pathways of the brain. Fed Proc 38: 2473-2476.
28. Kuhar MJ, Ritz MC, Boja JW (1991). The dopamine hypothesis of the reinforcing properties of cocaine. Trends Neurosci 14: 299-302.
29. Leventhal AM, Kahler CW, Ray LA, Stone K, Young D, Chelminski I et al (2008). Anhedonia and amotivation in psychiatric outpatients with fully remitted stimulant use disorder. Am J Addict 17: 218-223.
30. Lodge DJ, Grace AA (2005). Acute and chronic corticotropin-releasing factor 1 receptor blockade inhibits cocaine-induced dopamine release: correlation with dopamine neuron activity. J Pharmacol Exp Ther 314: 201-206.
31. Martinez D, Broft A, Foltin RW, Slifstein M, Hwang DR, Huang Y et al (2004). Cocaine dependence and d2 receptor availability in the functional subdivisions of the striatum: relationship with cocaineseeking behavior. Neuropsychopharmacology 29: 1190-1202.
32. Martinez D, Gil R, Slifstein M, Hwang DR, Huang Y, Perez A et al (2005). Alcohol dependence is associated with blunted dopamine transmission in the ventral striatum. Biol Psychiatry 58: 779-786.
33. Maslowski-Cobuzzi RJ, Napier TC (1994). Activation of dopaminergic neurons modulates ventral pallidal responses evoked by amygdala stimulation. Neuroscience 62: 1103-1119.
34. McAllister AK, Katz LC, Lo DC (1999). Neurotrophins and synaptic plasticity. Annu Rev Neurosci 22: 295-318.
35. McGregor A, Roberts DC (1993). Dopaminergic antagonism within the nucleus accumbens or the amygdala produces differential effects on intravenous cocaine self-administration under fixed and progressive ratio schedules of reinforcement. Brain Res 624: 245-252.
36. Moreines JL, Owrutsky WL, Grace AA (2014). Infralimbic Prefrontal Cortex Modulation of Dopaminergic System Function in Chronic Mild Stress Model of Depression. Program No 71113 Neuroscience Meeting Planner. Society for Neuroscience: Washington, DC, USA, 2014.
37. Morshedi MM, Rademacher DJ, Meredith GE (2009). Increased synapses in the medial prefrontal cortex are associated with repeated amphetamine administration. Synapse 63: 126-135.
38. Nestler EJ (2005). Is there a common molecular pathway for addiction? Nat Neurosci 8: 1445-1449.
39. Nestler EJ, Hyman SE (2010). Animal models of neuropsychiatric disorders. Nat Neurosci 13: 1161-1169.
40. Onn SP, Grace AA (2000). Amphetamine withdrawal alters bistable states and cellular coupling in rat prefrontal cortex and nucleus accumbens neurons recorded in vivo. J Neurosci 20: 2332-2345.
41. Porsolt RD, Anton G, Blavet N, Jalfre M (1978). Behavioural despair in rats: a new model sensitive to antidepressant treatments. Eur J Pharmacol 47: 379-391.
42. Rademacher DJ, Rosenkranz JA, Morshedi MM, Sullivan EM, Meredith GE (2010). Amphetamine-associated contextual learning is accompanied by structural and functional plasticity in the basolateral amygdala. J Neurosci 30: 4676-4686.
43. Schultz W (1999). The reward signal of midbrain dopamine neurons. News Physiol Sci 14: 249-255.
44. Shen F, Meredith GE, Napier TC (2006). Amphetamine-induced place preference and conditioned motor sensitization requires activation of tyrosine kinase receptors in the hippocampus. J Neurosci 26: 11041-11051.
45. Shi WX, Pun CL, Smith PL, Bunney BS (2000). Endogenous DAmediated feedback inhibition of DA neurons: involvement of both D(1)- and D(2)-like receptors. Synapse 35: 111-119.
46. Slattery DA, Cryan JF (2012). Using the rat forced swim test to assess antidepressant-like activity in rodents. Nat Protoc 7: 1009-1014.
47. Smith Y, Pare JF, Pare D (2000). Differential innervation of parvalbumin-immunoreactive interneurons of the basolateral amygdaloid complex by cortical and intrinsic inputs. J Comp Neurol 416: 496-508.
48. Swendsen J, Conway KP, Degenhardt L, Glantz M, Jin R, Merikangas KR et al (2010). Mental disorders as risk factors for substance use, abuse and dependence: results from the 10-year follow-up of the National Comorbidity Survey. Addiction 105: 1117-1128.
49. Tizabi Y, Bhatti BH, Manaye KF, Das JR, Akinfiresoye L (2012). Antidepressant-like effects of low ketamine dose is associated with increased hippocampal AMPA/NMDA receptor density ratio in female Wistar-Kyoto rats. Neuroscience 213: 72-80.
50. Tye KM, Mirzabekov JJ, Warden MR, Ferenczi EA, Tsai HC, Finkelstein J et al (2013). Dopamine neurons modulate neural encoding and expression of depression-related behaviour. Nature 493: 537-541.
51. Ungless MA, Grace AA (2012). Are you or aren't you? Challenges associated with physiologically identifying dopamine neurons. Trends Neurosci 35: 422-430.
52. Ungless MA, Whistler JL, Malenka RC, Bonci A (2001). Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons. Nature 411: 583-587.
53. Volkow ND, Wang GJ, Telang F, Fowler JS, Logan J, Jayne M et al (2007). Profound decreases in dopamine release in striatum in detoxified alcoholics: possible orbitofrontal involvement. J Neurosci 27: 12700-12706.
54. Wang Z, Rebec GV (1996). Amygdaloid neurons respond to clozapine rather than haloperidol in behaving rats pretreated with intra-amygdaloid amphetamine. Brain Res 711: 64-72.
55. Watson D, Clark LA, Tellegen A (1988). Development and validation of brief measures of positive and negative affect: the PANAS scales. J Pers Soc Psychol 54: 1063-1070.
56. Wise RA (1982). Neuroleptics and operant behavior: the anhedonia hypothesis 39-87.
57. Wu M, Hrycyshyn AW, Brudzynski SM (1996). Subpallidal outputs to the nucleus accumbens and the ventral tegmental area: anatomical and electrophysiological studies. Brain Res 740: 151-161.
58. Zarate CA Jr, Singh JB, Carlson PJ, Brutsche NE, Ameli R, Luckenbaugh DA et al (2006). A randomized trial of an N-methyl-D-aspartate antagonist in treatment-resistant major depression. Arch Gen Psychiatry 63: 856-864.