Lesion of medial prefrontal dopamine terminals abolishes habituation of accumbens shell dopamine responsiveness to taste stimuli

European Journal of Neuroscience

Volumn 37, Issue 4, 2013, Pages 613-622

  Bimpisidis, Zisis ^a   De Luca, Maria Antonietta ^a,b   Pisanu, Augusta ^d   Di Chiara, Gaetano ^a,b,c,d  

^a UNIVERSITY OF CAGLIARI   (Italy)

^b National Institute of Neuroscience   (Italy)

^c Centre of Excellence Neurobiology of Addiction   (Italy)

^d CNR   (Italy)

Author keywords

6 OHDA; Chocolate; Immunohistochemistry; Microdialysis; Motor activity; Rat

Indexed keywords

DOPAMINE; OXIDOPAMINE; TYROSINE 3 MONOOXYGENASE;

ANIMAL TISSUE; ARTICLE; BEHAVIOR; CACAO; CONTROLLED STUDY; DIALYSATE; DOPAMINERGIC TRANSMISSION; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MALE; MEDIAL PREFRONTAL CORTEX; MICRODIALYSIS; MOTOR PERFORMANCE; NERVE ENDING; NONHUMAN; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; TASTE;

ANIMALS; BRAIN CHEMISTRY; DOPAMINE; HABITUATION, PSYCHOPHYSIOLOGIC; IMMUNOHISTOCHEMISTRY; MALE; MICRODIALYSIS; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; TASTE;

EID: 84873998433     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12068     Document Type: Article

References (64)

1. Albanese, A. & Bentivoglio, M. (1982) The organization of dopaminergic and non-dopaminergic mesencephalo-cortical neurons in the rat. Brain Res., 238, 421-425.
2. Balleine, B.W. & O'Doherty, J.P. (2010) Human and rodent homologies in action control: corticostriatal determinants of goal-directed and habitual action. Neuropsychopharmacol., 35, 48-69.
3. Banks, K.E. & Gratton, A. (1995) Possible involvement of medial prefrontal cortex in amphetamine-induced sensitization of mesolimbic dopamine function. Eur. J. Pharmacol., 282, 157-167.
4. Bassareo, V., De Luca, M.A. & Di Chiara, G. (2002) Differential expression of motivational stimulus properties by dopamine in nucleus accumbens shell versus core and prefrontal cortex. J. Neurosci., 22, 4709-4719.
5. Berridge, K.C. (2000) Measuring hedonic impact in animals and infants: microstructure of affective taste reactivity patterns. Neurosci. Biobehav. Rev., 24, 173-198.
6. Berridge, K.C. & Robinson, T.E. (1998) What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res. Brain Res. Rev., 28, 309-369.
7. Beyer, C.E. & Steketee, J.D. (1999) Dopamine depletion in the medial prefrontal cortex induces sensitized-like behavioral and neurochemical responses to cocaine. Brain Res., 833, 133-141.
8. Björklund, A., Divac, I. & Lindvall, O. (1978) Regional distribution of catecholamines in monkey cerebral cortex, evidence for a dopaminergic innervation of the primate prefrontal cortex. Neurosci. Lett., 7, 115-119.
9. Broersen, L.M., Feldon, J. & Weiner, I. (1999) Dissociative effects of apomorphine infusions into the medial prefrontal cortex of rats on latent inhibition, prepulse inhibition and amphetamine-induced locomotion. Neuroscience, 94, 39-46.
10. Bubser, M. (1994) 6-Hydroxydopamine lesions of the medial prefrontal cortex of rats do not affect dopamine metabolism in the basal ganglia at short and long postsurgical intervals. Neurochem. Res., 19, 421-425.
11. Bubser, M. & Schmidt, W.J. (1990) 6-Hydroxydopamine lesion of the rat prefrontal cortex increases locomotor activity, impairs acquisition of delayed alternation tasks, but does not affect uninterrupted tasks in the radial maze. Behav. Brain Res., 37, 157-168.
12. Cacciapaglia, F., Saddoris, M.P., Wightman, R.M. & Carelli, R.M. (2012) Differential dopamine release dynamics in the nucleus accumbens core and shell track distinct aspects of goal-directed behavior for sucrose. Neuropharmacology, 62, 2050-2056.
13. Carlson, J.N., Visker, K.E., Keller, Jr.R.W. & Glick, S.D. (1996) Left and right 6-hydroxydopamine lesions of the medial prefrontal cortex differentially alter subcortical dopamine utilization and the behavioral response to stress. Brain Res., 711, 1-9.
14. Carter, C.J. & Pycock, C.J. (1978) Lesions of the frontal cortex of the rat: changes in neurotransmitter systems in sub-cortical regions. Br. J. Pharmacol., 64, 430.
15. Carter, C.J. & Pycock, C.J. (1980) Behavioural and biochemical effects of dopamine and noradrenaline depletion within the medial prefrontal cortex of the rat. Brain Res., 192, 163-176.
16. Corbit, L.H. & Balleine, B.W. (2011) The general and outcome-specific forms of Pavlovian-instrumental transfer are differentially mediated by the nucleus accumbens core and shell. J. Neurosci., 31, 11786-11794.
17. Corbit, L.H., Muir, J.L. & Balleine, B.W. (2001) The role of the nucleus accumbens in instrumental conditioning: evidence of a functional dissociation between accumbens core and shell. J. Neurosci., 21, 3251-3260.
18. De Luca, M.A., Bimpisidis, Z., Bassareo, V. & Di Chiara, G. (2011) Influence of morphine sensitization on the responsiveness of mesolimbic and mesocortical dopamine transmission to appetitive and aversive gustatory stimuli. Psychopharmacology, 216, 345-353.
19. De Luca, M.A., Solinas, M., Bimpisidis, Z., Goldberg, S.R. & Di Chiara, G. (2012) Cannabinoid facilitation of behavioral and biochemical hedonic taste responses. Neuropharmacology, 63, 161-168.
20. Deutch, A.Y., Clark, W.A. & Roth, R.H. (1990) Prefrontal cortical dopamine depletion enhances the responsiveness of mesolimbic dopamine neurons to stress. Brain Res., 521, 311-315.
21. Di Chiara, G. & Bassareo, V. (2007) Reward system and the brain: what dopamine does and doesn't do. Curr. Opin. Pharmacol., 7, 69-76.
22. Espejo, E.F. (1997) Selective dopamine depletion within the medial prefrontal cortex induces anxiogenic-like effects in rats placed on the elevated plus maze. Brain Res., 762, 281-284.
23. Espejo, E.F. & Miñano, J. (2001) Adrenergic hyperactivity and metanephrine excess in the nucleus accumbens after prefrontocortical dopamine depletion. J. Neurophysiol., 85, 1270-1274.
24. Ferron, A., Thierry, A.M., Le Douarin, C. & Glowinski, J. (1984) Inhibitory influence of the mesocortical dopaminergic system on spontaneous activity or excitatory response induced from the thalamic mediodorsal nucleus in the rat medial prefrontal cortex. Brain Res., 302, 257-265.
25. Grill, H.J. & Norgren, R. (1978) The taste reactivity test I. Mimetic responses to gustatory stimuli in neurologically normal rats. Brain Res., 143, 263-279.
26. Groenewegen, H.J., Berendse, H.W., Wolters, J.G. & Lohman, A.H.M. (1990) The anatomical relationship of the prefrontal cortex with the striatopallidal system, the thalamus and the amygdala: evidence for a parallel organization. Prog. Brain Res., 85, 95-116.
27. Haroutunian, V., Knott, P. & Davis, K.L. (1988) Effects of mesocortical dopaminergic lesions upon subcortical dopaminegic function. Psychopharmacol. Bull., 24, 341-344.
28. Jaskiw, G.E., Weinberger, D.R. & Crawley, J.N. (1991) Microinjection of apomorphine into the prefrontal cortex of the rat reduces dopamine metabolite concentrations in microdialysate from the caudate nucleus. Biol. Psychiatry, 29, 703-706.
29. Jones, G.H. & Robbins, T.W. (1992) Differential effects of mesocortical, mesolimbic, and mesostriatal dopamine depletion on spontaneous, conditioned, and drug-induced locomotor activity. Pharmacol. Biochem. Behav., 43, 887-895.
30. Joyce, E.M., Stinus, L. & Iversen, S.D. (1983) Effect of injections of 6-OHDA into either nucleus accumbens septi or frontal cortex on spontaneous and drug-induced activity. Neuropharmacology, 22, 1141-1145.
31. King, D., Zigmond, M.J. & Finlay, J.M. (1997) Effects of dopamine depletion in the medial prefrontal cortex on the stress-induced increase in extracellular dopamine in the nucleus accumbens core and shell. Neuroscience, 77, 141-153.
32. Kolachana, B.S., Saunders, R.C. & Weinberger, D.R (1995) Augmentation of prefrontal cortical monoaminergic activity inhibits dopamine release in the caudate nucleus: an in vivo neurochemical assessment in the rhesus monkey. Neuroscience, 69, 859-868.
33. Kurachi, M., Yasui, S., Kurachi, T., Shibata, R., Murata, M., Hagino, H., Tanii, Y., Kurata, K., Suzuki, M. & Sakurai, Y. (1995) Hypofrontality does not occur with 6-hydroxydopamine lesions of the medial prefrontal cortex in rat brain. Eur. Neuropsychopharmacol., 5, 63-68.
34. Lacroix, L., Broersen, L.M., Feldon, J. & Weiner, I. (2000) Effects of local infusions of dopaminergic drugs into the medial prefrontal cortex of rats on latent inhibition, prepulse inhibition and amphetamine-induced activity. Behav. Brain Res., 107, 111-121.
35. Lanser, M.G., Ellenbroek, B.A., Zitman, F.G., Heeren, D.J. & Cools, A.R. (2001) The role of medial prefrontal cortex in spontaneous flexibility in the rat. Behav. Pharmacol., 12, 163-171.
36. Lecca, D., Cacciapaglia, F., Valentini, V., Gronli, J., Spiga, S. & Di Chiara, G. (2006) Preferential increase of extracellular dopamine in the rat nucleus accumbens shell as compared to that in the core duing acquisition and maintenance of intravenous nicotine self-administration. Psychopharmacology, 184, 435-446.
37. Lecesse, A.P. & Lyness, W.H. (1987) Lesions of dopamine neurons in the medial prefrontal cortex: effects on self-administration of amphetamine and dopamine synthesis in the brain of the rat. Neuropharmacology, 26, 1303-1308.
38. Lindvall, O, Björklund, A., Moore, R.Y. & Stenevi, U. (1974) Mesencephalic dopamine neurons projecting to neocortex. Brain Res., 81, 325-331.
39. Louilot, A., Le Moal, M. & Simon, H. (1989) Opposite influences of dopaminergic pathways to the prefrontal cortex or the septum on the dopaminergic transmission in the nucleus accumbens. An in vivo voltammetric study. Neuroscience, 29, 45-56.
40. Martin-Iverson, M.T., Szostak, C. & Fibiger, H.C. (1986) 6-Hydroxydopamine lesions of the medial prefrontal cortex fail to influence intravenous self-administration of cocaine. Psychopharmacology, 88, 310-314.
41. McGregor, A., Baker, G. & Roberts, D.C. (1996) Effect of 6-hydroxydopamine lesions of the medial prefrontal cortex on intravenous cocaine self-administration under a progressive ratio schedule of reinforcement. Pharmacol. Biochem. Behav., 53, 5-9.
42. Mitchell, J.B. & Gratton, A. (1992) Partial dopamine depletion of the prefrontal cortex lead to enhanced mesolimbic dopamine release elicited by repeated exposure to naturally reinforcing stimuli. J. Neurosci., 12, 3609-3618.
43. Murase, S., Grenhoff, J., Chouvet, G., Gonon, G.G. & Svensson, T.H. (1993) Prefrontal cortex regulates burst firing and transmitter release in rat mesolimbic dopamine neurons studies in vivo. Neurosci. Lett., 157, 53-56.
44. Naneix, F., Marchand, A.R., Di Scala, G., Pape, J.-R. & Coutureau, E. (2009) A role for medial prefrontal dopaminergic innervation in instrumental conditioning. J. Neurosci., 29, 6599-6606.
45. Nielsen, D.M., Crosley, K.J., Keller, R.W., Glick, S.D. & Carlson, J.N. (1999) Left and right 6-hydroxydopamine lesions of the medial prefrontal cortex differentially affect voluntary ethanol consumption. Brain Res., 823, 59-66.
46. Oades, R.D., Taghzouti, K., Rivet, J.M., Simon, H. & Le Moal, M. (1986) Locomotor activity in relation to dopamine and noradrenaline in the nucleus accumbens, septal and frontal areas: a 6-hydroydopamine study. Neuropsychobiology, 16, 37-42.
47. Paxinos, G. & Watson, C. (1998) The Rat Brain in Stereotaxic Coordinates, 4th edn. Academic Press, San Diego, CA.
48. Piazza, P.V., Rouge-Pont, F., Deminiere, J.M., Kharoubi, M., Le Moal, M. & Simon, H. (1991) Dopaminergic activity is reduced in the prefrontal cortex and increased in the nucleus accumbens of rats predisposed to develop amphetamine self-administration. Brain Res., 567, 169-174.
49. Pycock, C.J., Carter, C.J. & Kerwin, R.W. (1980) Effect of 6-hydroxydopamine lesions of the medial prefrontal cortex on neurotransmitter systems in subcortical sites in the rat. J. Neurochem., 34, 91-99.
50. Roberts, A.C., De Salvia, M.A., Wilkinson, L.S., Collins, P., Muir, J.L., Everitt, B.J. & Robbins, T.W. (1994) 6-Hydroxydopamie lesions of the prefrontal cortex in monkeys enhance performance on an analog of the Wisconsin Card Sort Test: possible interactions with subcortical dopamine. J. Neurosci., 14, 2531-2544.
51. Rosin, D.L., Clark, W.A., Goldstein, M., Roth, R.H. & Deutch, A.Y. (1992) Effects of 6-hydroxydopamine lesions of the prefrontal cortex on tyrosine hydroxylase activity in mesolimbic and nigrostriatal dopamine systems. Neuroscience, 48, 831-839.
52. Sawaguchi, T. & Goldman-Rakic, P.S. (1991) D1 dopamine receptors in prefrontal cortex: involvement in working memory. Science, 251, 947-950.
53. Schenk, S., Horger, B.A., Peltier, R. & Shelton, K. (1991) Supersensitivity to the reinforcing effects of cocaine following 6-hydroxydopamine lesions to the medial prefrontal cortex in rats. Brain Res., 543, 227-235.
54. Sesack, S.R. & Pickel, V.M. (1992) Prefrontal cortical efferents in the rat synapse on unlabeled neuronal targets of catecholamine terminals in the nucleus accumbens septi and on dopamine neurons in the ventral tegmental area. J. Comp. Neurol., 320, 145-160.
55. Sesack, S.R., Snyder, C.L. & Lewis, D.A. (1995) Axon terminals immunolabeled for dopamine or tyrosine hydroxylase synapse on GABA-immunoreactive dendrites in rat and monkey cortex. J. Comp. Neurol., 363, 264-280.
56. Sokolowski, J.D. & Salamone, J.D. (1994) Effects of dopamine depletions in the medial prefrontal cortex on DRL performance and motor activity in the rat. Brain Res., 642, 20-28.
57. Steketee, J.D. (2005) Cortical mechanisms of cocaine sensitization. Crit. Rev. Neurobiol., 17, 69-86.
58. Taber, M.T. & Fibiger, H.C. (1993) Electrical stimulation of the medial prefrontal cortex increases dopamine release in the striatum. Neuropsychopharmacol., 9, 271-275.
59. Taber, M.T. & Fibiger, H.C. (1995) Electrical stimulation of the prefrontal cortex increases dopamine release in the nucleus accumbens of the rat: modulation by metabotropic glutamate receptors. J. Neurosci., 15, 3896-3904.
60. Thompson, T.L. & Moss, R.L. (1995) In vivo stimulated dopamine release in the nucleus accumbens: modulation by the prefrontal cortex. Brain Res., 686, 93-98.
61. Tzschentke, T.M. (2001) Pharmacology and behavioral pharmacology of the mesocortical dopamine system. Prog. Neurobiol., 63, 241-320.
62. Vezina, P., Blanc, G., Glowinski, J. & Tassin, J.P. (1991) Opposed behavioural outputs of increased dopamine transmission in prefrontocortical and subcortical areas: a role for the cortical D-1 dopamine receptors. Eur. J. Neurosci., 10, 1001-1007.
63. Wanchoo, S.J., Lee, M.J., Swann, A.C. & Dafny, N. (2010) Bilateral six-hydroxydopamine administration to PFC prevents the expression of behavioral sensitization to methylphenidate. Brain Res., 1312, 89-100.
64. Weinberger, D.R. (1987) Implications of normal brain development for the pathogenesis of schizophrenia. Arch. Gen. Psychiatry, 44, 660-669.