Dopamine neurons in the ventral tegmental area fire faster in adolescent rats than in adults

Journal of Neurophysiology

Volumn 108, Issue 6, 2012, Pages 1620-1630

  McCutcheon, James E ^a   Conrad, Kelly L ^a   Carr, Steven B ^a   Ford, Kerstin A ^a   McGehee, Daniel S ^b   Marinelli, Michela ^a  

^a ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

Addiction; Bursts; Development; Electrophysiology; Midbrain

Indexed keywords

AMPA RECEPTOR; POTASSIUM CHANNEL;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; CALCIUM CONDUCTANCE; DOPAMINERGIC NERVE CELL; EXCITATORY POSTSYNAPTIC POTENTIAL; HYPERPOLARIZATION; IN VIVO STUDY; MALE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RAT; RECORDING; SPIKE; VENTRAL TEGMENTUM;

ACTION POTENTIALS; AGE FACTORS; ANIMALS; DOPAMINERGIC NEURONS; EXCITATORY POSTSYNAPTIC POTENTIALS; INHIBITORY POSTSYNAPTIC POTENTIALS; MALE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; RECEPTORS, DOPAMINE D2; RECEPTORS, GABA; SMALL-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; VENTRAL TEGMENTAL AREA;

EID: 84866382220     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00077.2012     Document Type: Article

References (70)

1. Andersen SL, Thompson AT, Rutstein M, Hostetter JC, Teicher MH. Dopamine receptor pruning in prefrontal cortex during the periadolescent period in rats. Synapse 37: 167-169, 2000.
2. Anker JJ, Zlebnik NE, Navin SF, Carroll ME. Responding during signaled availability and nonavailability of iv cocaine and food in rats: age and sex differences. Psychopharmacology (Berl) 215: 785-799, 2011.
3. Anstrom KK, Miczek KA, Budygin EA. Increased phasic dopamine signaling in the mesolimbic pathway during social defeat in rats. Neuroscience 161: 3-12, 2009.
4. Anthony JC, Petronis K. Early-onset drug use and risk of later drug problems. Drug Alcohol Depend 40: 9-15, 1995.
5. Arencibia-Albite F, Vázquez R, Velásquez-Martinez MC, Jiménez-Rivera CA. Cocaine sensitization inhibits the hyperpolarization-activated cation current Ih and reduces cell size in dopamine neurons of the ventral tegmental area. J Neurophysiol 107: 2271-2282, 2012.
6. Badanich KA, Adler KJ, Kirstein CL. Adolescents differ from adults in cocaine conditioned place preference and cocaine-induced dopamine in the nucleus accumbens septi. Eur J Pharmacol 550: 95-106, 2006.
7. Beckstead MJ, Grandy DK, Wickman K, Williams JT. Vesicular dopamine release elicits an inhibitory postsynaptic current in midbrain dopamine neurons. Neuron 42: 939-946, 2004.
8. Carlsson A. Antipsychotic drugs, neurotransmitters, and schizophrenia. Am J Psychiatry 135: 165-173, 1978.
9. Carr DB, Sesack SR. Terminals from the rat prefrontal cortex synapse on mesoaccumbens vta neurons. Ann NY Acad Sci 877: 676-678, 1999.
10. Caster JM, Walker QD, Kuhn CM. Enhanced behavioral response to repeated-dose cocaine in adolescent rats. Psychopharmacology (Berl) 183: 218-225, 2005.
11. Chen CY, Storr CL, Anthony JC. Early-onset drug use and risk for drug dependence problems. Addict Behav 34: 319-322, 2009.
12. Chergui K, Suaud-Chagny MF, Gonon F. Nonlinear relationship between impulse flow, dopamine release and dopamine elimination in the rat brain in vivo. Neuroscience 62: 641-645, 1994.
13. Chieng B, Azriel Y, Mohammadi S, Christie MJ. Distinct cellular properties of identified dopaminergic and GABAergic neurons in the mouse ventral tegmental area. J Physiol 589: 3775-3787, 2011.
14. Conrad KL, McCutcheon JE, Cotterly LM, Ford KA, Beales M, Marinelli M. Persistent increases in cocaine-seeking behavior after acute exposure to cold swim stress. Biol Psychiatry 68: 303-305, 2010.
15. Diehl DJ, Gershon S. The role of dopamine in mood disorders. Compr Psychiatry 33: 115-120, 1992.
16. Dobi A, Margolis EB, Wang HL, Harvey BK, Morales M. Glutamatergic and nonglutamatergic neurons of the ventral tegmental area establish local synaptic contacts with dopaminergic and nondopaminergic neurons. J Neurosci 30: 218-229, 2010.
17. Ford CP, Mark GP, Williams JT. Properties and opioid inhibition of mesolimbic dopamine neurons vary according to target location. J Neurosci 26: 2788-2797, 2006.
18. Frantz KJ, O'Dell LE, Parsons LH. Behavioral and neurochemical responses to cocaine in periadolescent and adult rats. Neuropsychopharmacology 32: 625-637, 2007.
19. Geisler S, Derst C, Veh RW, Zahm DS. Glutamatergic afferents of the ventral tegmental area in the rat. J Neurosci 27: 5730-5743, 2007.
20. Grace AA, Bunney BS. Intracellular and extracellular electrophysiology of nigral dopaminergic neurons-1. Identification and characterization. Neuroscience 10: 301-315, 1983.
21. Grace AA, Bunney BS. The control of firing pattern in nigral dopamine neurons: single spike firing. J Neurosci 4: 2866-2876, 1984.
22. Grace AA, Floresco SB, Goto Y, Lodge DJ. Regulation of firing of dopaminergic neurons and control of goal-directed behaviors. Trends Neurosci 30: 220-227, 2007.
23. Grace AA, Onn SP. Morphology and electrophysiological properties of immunocytochemically identified rat dopamine neurons recorded in vitro. J Neurosci 9: 3463-3481, 1989.
24. Grimm JW, See RE. Cocaine self-administration in ovariectomized rats is predicted by response to novelty, attenuated by 17-beta estradiol, and associated with abnormal vaginal cytology. Physiol Behav 61: 755-761, 1997.
25. Iñiguez SD, Vialou V, Warren BL, Cao JL, Alcantara LF, Davis LC, Manojlovic Z, Neve RL, Russo SJ, Han MH, Nestler EJ, Bolaños-Guzmán CA. Extracellular signal-regulated kinase-2 within the ventral tegmental area regulates responses to stress. J Neurosci 30: 7652-7663, 2010.
26. Jhou TC, Fields HL, Baxter MG, Saper CB, Holland PC. The rostromedial tegmental nucleus (RMTg), a GABAergic afferent to midbrain dopamine neurons, encodes aversive stimuli and inhibits motor responses. Neuron 61: 786-800, 2009.
27. Johnson SW, North RA. Two types of neurone in the rat ventral tegmental area and their synaptic inputs. J Physiol 450: 455-468, 1992.
28. Kalivas PW, Alesdatter JE. Involvement of N-methyl-D-aspartate receptor stimulation in the ventral tegmental area and amygdala in behavioral sensitization to cocaine. J Pharmacol Exp Ther 267: 486-495, 1993.
29. Kerstetter KA, Kantak KM. Differential effects of self-administered cocaine in adolescent and adult rats on stimulus-reward learning. Psychopharmacology (Berl) 194: 403-411, 2007.
30. Lacey MG, Mercuri NB, North RA. Dopamine acts on D2 receptors to increase potassium conductance in neurones of the rat substantia nigra zona compacta. J Physiol 392: 397-416, 1987.
31. Lammel S, Ion DI, Roeper J, Malenka RC. Projection-specific modulation of dopamine neuron synapses by aversive and rewarding stimuli. Neuron 70: 855-862, 2011.
32. Li C, Frantz KJ. Attenuated incubation of cocaine seeking in male rats trained to self-administer cocaine during periadolescence. Psychopharmacology (Berl) 204: 725-733, 2009.
33. Lobb CJ, Wilson CJ, Paladini CA. A dynamic role for GABA receptors on the firing pattern of midbrain dopaminergic neurons. J Neurophysiol 104: 403-413, 2010.
34. Luo AH, Georges FE, Aston-Jones GS. Novel neurons in ventral tegmental area fire selectively during the active phase of the diurnal cycle. Eur J Neurosci 27: 408-422, 2008.
35. Margolis EB, Coker AR, Driscoll JR, Lemaître AI, Fields HL. Reliability in the identification of midbrain dopamine neurons. PLoS One 5: e15222, 2010.
36. Margolis EB, Lock H, Hjelmstad GO, Fields HL. The ventral tegmental area revisited: is there an electrophysiological marker for dopaminergic neurons? J Physiol 577: 907-924, 2006.
37. Marinelli M, Cooper DC, Baker LK, White FJ. Impulse activity of midbrain dopamine neurons modulates drug-seeking behavior. Psychopharmacology (Berl) 168: 84-98, 2003.
38. Marinelli M, Rudick CN, Hu XT, White FJ. Excitability of dopamine neurons: modulation and physiological consequences. CNS Neurol Disord Drug Targets 5: 79-97, 2006.
39. Marinelli M, White FJ. Enhanced vulnerability to cocaine self-administration is associated with elevated impulse activity of midbrain dopamine neurons. J Neurosci 20: 8876-8885, 2000.
40. Mathon DS, Kamal A, Smidt MP, Ramakers GM. Modulation of cellular activity and synaptic transmission in the ventral tegmental area. Eur J Pharmacol 480: 97-115, 2003.
41. McCutcheon JE, Marinelli M. Age matters. Eur J Neurosci 29: 997-1014, 2009.
42. Morikawa H, Paladini CA. Dynamic regulation of midbrain dopamine neuron activity: intrinsic, synaptic, and plasticity mechanisms. Neuroscience 198: 95-111, 2011.
43. Mueller AL, Brodie MS. Intracellular recording from putative dopaminecontaining neurons in the ventral tegmental area of Tsai in a brain slice preparation. J Neurosci Methods 28: 15-22, 1989.
44. h channels contribute to the different functional properties of identified dopaminergic subpopulations in the midbrain. J Neurosci 22: 1290-1302, 2002.
45. Omelchenko N, Sesack SR. Ultrastructural analysis of local collaterals of rat ventral tegmental area neurons: GABA phenotype and synapses onto dopamine and GABA cells. Synapse 63: 895-906, 2009.
46. Paus T, Keshavan M, Giedd J. Why do many psychiatric disorders emerge during adolescence? Nat Rev Neurosci 9: 947-957, 2008.
47. Perry JL, Anderson MM, Nelson SE, Carroll ME. Acquisition of i.v. cocaine self-administration in adolescent and adult male rats selectively bred for high and low saccharin intake. Physiol Behav 91: 126-133, 2007.
48. Piazza P, Deminière JM, Maccari S, Mormède P, Le Moal M, Simon H. Individual reactivity to novelty predicts probability of amphetamine selfadministration. Behav Pharmacol 1: 339-345, 1990.
49. Pierre P, Vezina P. Predisposition to self-administer amphetamine: the contribution of response to novelty and prior exposure to the drug. Psychopharmacology (Berl) 129: 277-284, 1997.
50. Robins LN, Przybeck TR. Age of onset of drug use as a factor in drug and other disorders. NIDA Res Monogr 56: 178-192, 1985.
51. Saitoh K, Isa T, Takakusaki K. Nigral gabaergic inhibition upon mesencephalic dopaminergic cell groups in rats. Eur J Neurosci 19: 2399-2409, 2004.
52. Sarpal D, Koenig JI, Adelman JP, Brady D, Prendeville LC, Shepard PD. Regional distribution of SK3 mRNA-containing neurons in the adult and adolescent rat ventral midbrain and their relationship to dopamine-containing cells. Synapse 53: 104-113, 2004.
53. Shaham Y, Erb S, Stewart J. Stress-induced relapse to heroin and cocaine seeking in rats: a review. Brain Res Brain Res Rev 33: 13-33, 2000.
54. Shahbazi M, Moffett AM, Williams BF, Frantz KJ. Age-and sex-dependent amphetamine self-administration in rats. Psychopharmacology (Berl) 196: 71-81, 2008.
55. Spear LP. The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24: 417-463, 2000.
56. Stoffel EC, Cunningham KA. The relationship between the locomotor response to a novel environment and behavioral disinhibition in rats. Drug Alcohol Depend 92: 69-78, 2008.
57. Tarazi FI, Baldessarini RJ. Comparative postnatal development of dopamine D1, D2, and D4 receptors in rat forebrain. Int J Dev Neurosci 18: 29-37, 2000.
58. Tirelli E, Laviola G, Adriani W. Ontogenesis of behavioral sensitization and conditioned place preference induced by psychostimulants in laboratory rodents. Neurosci Biobehav Rev 27: 163-178, 2003.
59. Ungless MA, Magill PJ, Bolam JP. Uniform inhibition of dopamine neurons in the ventral tegmental area by aversive stimuli. Science 303: 2040-2042, 2004.
60. Ungless MA, Grace AA. Are you or aren't you? Challenges associated with physiologically identifying dopamine neurons. Trends Neurosci 35: 422-430, 2012.
61. Vanderschuren LJ, Niesink RJ, Van Ree JM. The neurobiology of social play behavior in rats. Neurosci Biobehav Rev 21: 309-326, 1997.
62. Wang RY. Dopaminergic neurons in the rat ventral tegmental area. I: Identification and characterization. Brain Res Rev 3: 123-140, 1981a.
63. Wang RY. Dopaminergic neurons in the rat ventral tegmental area. II: Evidence for autoregulation. Brain Res Rev 3: 141-151, 1981b.
64. White FJ. Synaptic regulation of mesocorticolimbic dopamine neurons. Annu Rev Neurosci 19: 405-436, 1996.
65. White FJ, Wang RY. Pharmacological characterization of dopamine autoreceptors in the rat ventral tegmental area: microiontophoretic studies. J Pharmacol Exp Ther 231: 275-280, 1984.
66. Wise RA, Rompre PP. Brain dopamine and reward. Annu Rev Psychol 40: 191-225, 1989.
67. Witkovsky P, Veisenberger E, Haycock JW, Akopian A, Garcia-Espana A, Meller E. Activity-dependent phosphorylation of tyrosine hydroxylase in dopaminergic neurons of the rat retina. J Neurosci 24: 4242-4249, 2004.
68. Wolf ME, White FJ, Hu XT. Mk-801 prevents alterations in the mesoaccumbens dopamine system associated with behavioral sensitization to amphetamine. J Neurosci 14: 1735-1745, 1994.
69. Wolfart J, Neuhoff H, Franz O, Roeper J. Differential expression of the small-conductance, calcium-activated potassium channel SK3 is critical for pacemaker control in dopaminergic midbrain neurons. J Neurosci 21: 3443-3456, 2001.
70. Zhang TA, Placzek AN, Dani JA. In vitro identification and electrophysiological characterization of dopamine neurons in the ventral tegmental area. Neuropharmacology 59: 431-436, 2010.