Early stress and chronic methylphenidate cross-sensitize dopaminergic responses in the adolescent medial prefrontal cortex and nucleus accumbens

Journal of Neurochemistry

Volumn 103, Issue 6, 2007, Pages 2234-2244

  Jezierski, Grzegorz ^a   Zehle, Stefanie ^a   Bock, Joerg ^a   Braun, Katharina ^a   Gruss, Michael ^a  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

Author keywords

Attention deficit hyperactivity disorder; Development; Dopamine; Limbic system; Microdialysis; Parental separation

Indexed keywords

DOPAMINE; METHYLPHENIDATE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AREA UNDER THE CURVE; ARTICLE; ATTENTION DEFICIT DISORDER; CONTROLLED STUDY; CROSS ALLERGY; DRUG EFFECT; HYPERACTIVITY; IN VIVO STUDY; LIFE STRESS; LIMBIC SYSTEM; MALE; NONHUMAN; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT;

AGING; ANIMALS; ATTENTION DEFICIT DISORDER WITH HYPERACTIVITY; DISEASE MODELS, ANIMAL; DOPAMINE; DOPAMINE UPTAKE INHIBITORS; DRUG ADMINISTRATION SCHEDULE; FEMALE; MALE; MATERNAL DEPRIVATION; METHYLPHENIDATE; NEURAL PATHWAYS; NUCLEUS ACCUMBENS; OCTODON; PREFRONTAL CORTEX; PRESYNAPTIC TERMINALS; STRESS, PSYCHOLOGICAL; SYNAPTIC TRANSMISSION; TIME;

ANIMALIA; OCTODON DEGUS; RODENTIA;

EID: 36448937834     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2007.04927.x     Document Type: Article

References (58)

1. American Academy of Pediatrics (2000) Clinical practice guideline: diagnosis and evaluation of the child with attention-deficit/hyperactivity disorder. Pediatrics 105, 1158 1170.
2. 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.
3. Berridge C. W., Devilbiss D. M., Andrzejewski M. E., Arnsten A. F., Kelley A. E., Schmeichel B., Hamilton C. Spencer R. C. (2006) Methylphenidate preferentially increases catecholamine neurotransmission within the prefrontal cortex at low doses that enhance cognitive function. Biol. Psychiatry 60, 1111 1120.
4. Biederman J. (2005) Attention-deficit/hyperactivity disorder: a selective overview. Biol. Psychiatry 57, 1215 1220.
5. Bolanos C. A., Barrot M., Berton O., Wallace-Black D. Nestler E. J. (2003) Methylphenidate treatment during pre- and periadolescence alters behavioral responses to emotional stimuli at adulthood. Biol. Psychiatry 54, 1317 1329.
6. Braun K., Lange E., Metzger M. Poeggel G. (2000) Maternal separation followed by early social isolation affects the development of monoaminergic fiber systems in the medial prefrontal cortex of Octodon degus. Neuroscience 95, 309 318.
7. Braun K., Kremz P., Wetzel W., Wagner T. Poeggel G. (2003) Influence of parental deprivation on the behavioral development in Octodon degus: modulation by maternal vocalizations. Dev. Psychobiol. 42, 237 245.
8. Carboni E. Silvagni A. (2004) Experimental investigations on dopamine transmission can provide clues on the mechanism of the therapeutic effect of amphetamine and methylphenidate in ADHD. Neural Plast. 11, 77 95.
9. Castellanos F. X. Tannock R. (2002) Neuroscience of attention-deficit/ hyperactivity disorder: the search for endophenotypes. Nat. Rev. Neurosci. 3, 617 628.
10. Coulter C. L., Happe H. K. Murrin L. C. (1996) Postnatal development of the dopamine transporter: a quantitative autoradiographic study. Dev. Brain Res. 92, 172 181.
11. Dougherty D. D., Bonab A. A., Spencer T. J., Rauch S. L., Madras B. K. Fischman A. J. (1999) Dopamine transporter density in patients with attention deficit hyperactivity disorder. Lancet 354, 2132 2133.
12. Faraone S. V., Doyle A. E., Mick E. Biederman J. (2001) Meta-analysis of the association between the 7-repeat allele of the dopamine D(4) receptor gene and attention deficit hyperactivity disorder. Am. J. Psychiatry 158, 1052 1057.
13. Faraone S. V., Perlis R. H., Doyle A. E., Smoller J. W., Goralnick J. J., Holmgren M. A. Sklar P. (2005) Molecular genetics of attention-deficit/ hyperactivity disorder. Biol. Psychiatry 57, 1313 1323.
14. Feenstra M. G. (2000) Dopamine and noradrenaline release in the prefrontal cortex in relation to unconditioned and conditioned stress and reward. Prog. Brain Res. 126, 133 163.
15. Finlay J. M. Zigmond M. J. (1997) The effects of stress on central dopaminergic neurons: possible clinical implications. Neurochem. Res. 22, 1387 1394.
16. Fukui R., Svenningsson P., Matsuishi T., Higashi H., Naim A. C., Greengard P. Nishi A. (2003) Effect of methylphenidate on dopamine/DARPP signaling in adult, but not young, mice. J. Neurochem. 87, 1391 1401.
17. Fulford A. J. Marsden C. A. (1998) Effect of isolation-rearing on conditioned dopamine release in vivo in the nucleus accumbens of the rat. J. Neurochem. 70, 384 390.
18. Furukawa S., Furukawa Y., Satoyoshi E. Hayashi K. (1987) Regulation of nerve growth factor synthesis/secretion by catecholamine in cultured mouse astroglial cells. Biochem. Biophys. Res. Commun. 147, 1048 1054.
19. Gerasimov M. R., Franceschi M., Volkow N. D., Gifford A., Gatley S. J., Marsteller D., Molina P. E. Dewey S. L. (2000) Comparison between intraperitoneal and oral methylphenidate administration: a microdialysis and locomotor activity study. J. Pharmacol. Exp. Ther. 295, 51 57.
20. Gos T., Becker K., Bock J., Malecki U., Bogerts B., Poeggel G. Braun K. (2006) Early neonatal and postweaning social emotional deprivation interferes with the maturation of serotonergic and tyrosine hydroxylase-immunoreactive afferent fiber systems in the rodent nucleus accumbens, hippocampus and amygdala. Neuroscience 140, 811 821.
21. Grund T., Lehmann K., Bock N., Rothenberger A. Teuchert-Noodt G. (2006) Influence of methylphenidate on brain development - an update of recent animal experiments. Behav. Brain Funct. 2, 2.
22. Gruss M., Westphal S., Luley C. Braun K. (2006) Endocrine and behavioural plasticity in response to juvenile stress in the semi-precocial rodent Octodon degus. Psychoneuroendocrinology 31, 361 372.
23. Hall F. S., Wilkinson L. S., Humby T., Inglis W., Kendall D. A., Marsden C. A. Robbins T. W. (1998) Isolation rearing in rats: pre- and postsynaptic changes in striatal dopaminergic systems. Pharmacol. Biochem. Behav. 59, 859 872.
24. Hedou G., Homberg J., Feldon J. Heidbreder C. A. (2001) Expression of sensitization to amphetamine and dynamics of dopamine neurotransmission in different laminae of the rat medial prefrontal cortex. Neuropharmacology 40, 366 382.
25. Helmeke C., Ovtscharoff jr W., Poeggel G. Braun K. (2001a) Juvenile emotional experience alters synaptic composition in the anterior cingulate cortex. Cereb. Cortex 11, 717 727.
26. Helmeke C., Poeggel G. Braun K. (2001b) Differential emotional experience induces elevated spine densities on basal dendrites of pyramidal neurons in the anterior cingulate cortex. Neuroscience 104, 927 931.
27. Horger B. A., Valadez A., Wellman P. J. Schenk S. (1994) Augmentation of the neurochemical effects of cocaine in the ventral striatum and medial prefrontal cortex following preexposure to amphetamine, but not nicotine: an in vivo microdialysis study. Life Sci. 55, 1245 1251.
28. Huff J. K. Davies M. I. (2002) Microdialysis monitoring of methylphenidate in blood and brain correlated with changes in dopamine and rat activity. J. Pharm. Biomed. Anal. 29, 767 777.
29. Kahlig K. M., Binda F., Khoshbouei H., Blakely R. D., McMahon D. G., Javitch J. A. Galli A. (2005) Amphetamine induces dopamine efflux through a dopamine transporter channel. Proc. Natl Acad. Sci. USA 102, 3495 3500.
30. Kiyatkin E. A. Rebec G. V. (1996) Dopaminergic modulation of glutamate-induced excitations of neurons in the neostriatum and nucleus accumbens of awake, unrestrained rats. J. Neurophysiol. 75, 142 153.
31. Kuczenski R. Segal D. S. (1997) Effects of methylphenidate on extracellular dopamine, serotonin, and norepinephrine: comparison with amphetamine. J. Neurochem. 68, 2032 2037.
32. Kuczenski R. Segal D. S. (1999) Dynamic changes in sensitivity occur during the acute response to cocaine and methylphenidate. Psychopharmacology 147, 96 103.
33. Kuczenski R. Segal D. S. (2002) Exposure of adolescent rats to oral methylphenidate: preferential effects on extracellular norepinephrine and absence of sensitization and cross-sensitization to methamphetamine. J. Neurosci. 22, 7264 7271.
34. Madras B. K., Miller G. M. Fischman A. J. (2005) The dopamine transporter and attention-deficit/hyperactivity disorder. Biol. Psychiatry 57, 1397 1409.
35. Marsteller D. A., Gerasimov M. R. Schiffer W. K. (2002) Acute handling stress modulates methylphenidate-induced catecholamine overflow in the medial prefrontal cortex. Neuropsychopharmacology 27, 163 170.
36. Martins M. R., Reinke A., Petronilho F. C., Gomes K. M., Dal-Pizzol F. Quevedo J. (2006) Methylphenidate treatment induces oxidative stress in young rat brain. Brain Res. 1078, 189 197.
37. Moll G. H., Hause S., Ruther E., Rothenberger A. Huether G. (2001) Early methylphenidate administration to young rats causes a persistent reduction in the density of striatal dopamine transporters. J. Child. Adolesc. Psychopharmacol. 11, 15 24.
38. Oades R. D. (1998) Frontal, temporal and lateralized brain function in children with attention-deficit hyperactivity disorder: a psychophysiological and neuropsychological viewpoint on development. Behav. Brain Res. 94, 83 95.
39. Okazawa H., Murata M., Watanabe M., Kamei M. Kanazawa I. (1992) Dopaminergic stimulation up-regulates the in vivo expression of brain-derived neurotrophic factor (BDNF) in the striatum. FEBS Lett. 313, 138 142.
40. Paulson P. E. Robinson T. E. (1995) Amphetamine-induced time-dependent sensitization of dopamine neurotransmission in the dorsal and ventral striatum: a microdialysis study in behaving rats. Synapse 19, 56 65.
41. Penner M. P., McFadyen M. P., Pinaud R., Carrey N., Robertson H. A. Brown R. E. (2002) Age-related distribution of c-fos expression in the striatum of CD-1 mice after acute methylphenidate administration. Dev. Brain Res. 135, 71 77.
42. Pierce R. C. Kalivas P. W. (1997) Repeated cocaine modifies the mechanism by which amphetamine releases dopamine. J. Neurosci. 17, 3254 3261.
43. Poeggel G., Helmeke C., Abraham A., Schwabe T., Friedrich P. Braun K. (2003a) Juvenile emotional experience alters synaptic composition in the rodent cortex, hippocampus, and lateral amygdala. Proc. Natl Acad. Sci. USA 100, 16137 16142.
44. Poeggel G., Nowicki L. Braun K. (2003b) Early social deprivation alters monoaminergic afferents in the orbital prefrontal cortex of Octodon degus. Neuroscience 116, 617 620.
45. Sagvolden T., Russell V. A., Aase H., Johansen E. B. Farshbaf M. (2005) Rodent models of attention-deficit/hyperactivity disorder. Biol. Psychiatry 57, 1239 1247.
46. Schultz W. (2000) Multiple reward signals in the brain. Nat. Rev. Neurosci. 1, 199 207.
47. Schultz W. (2002) Getting formal with dopamine and reward. Neuron 36, 241 263.
48. Solanto M. V. (2002) Dopamine dysfunction in AD/HD: integrating clinical and basic neuroscience research. Behav. Brain Res. 130, 65 71.
49. Sowell E. R., Thompson P. M., Welcome S. E., Henkenius A. L., Toga A. W. Peterson B. S. (2003) Cortical abnormalities in children and adolescents with attention-deficit hyperactivity disorder. Lancet 362, 1699 1707.
50. Sulzer D., Sonders M. S., Poulsen N. W. Galli A. (2005) Mechanisms of neurotransmitter release by amphetamines: a review. Prog. Neurobiol. 75, 406 433.
51. Tarazi F. I. Baldessarini R. J. (2000) Comparative postnatal development of dopamine D1, D2 and D4 receptors in rat forebrain. Int. J. Dev. Neurosci. 18, 29 37.
52. Tarazi F. I., Tomasini E. C. Baldessarini R. J. (1998) Postnatal development of dopamine and serotonin transporters in rat caudate-putamen and nucleus accumbens septi. Neurosci. Lett. 254, 21 24.
53. Volkow N. D., Fowler J. S., Wang G., Ding Y. Gatley S. J. (2002) Mechanism of action of methylphenidate: insights from PET imaging studies. J. Att. Disord. 6, S31 S43.
54. Waldman I. D., Rowe D. C., Abramowitz A. et al. (1998) Association and linkage of the dopamine transporter gene and attention-deficit hyperactivity disorder in children: heterogeneity owing to diagnostic subtype and severity. Am. J. Hum. Genet. 63, 1767 1776.
55. Wright J. W. Kern M. D. (1992) Stereotaxic atlas of the brain of Octodon degus. J. Morphol. 214, 299 320.
56. Young A. M. (2004) Increased extracellular dopamine in nucleus accumbens in response to unconditioned and conditioned aversive stimuli: studies using 1 min microdialysis in rats. J. Neurosci. Methods 138, 57 63.
57. Zehle S., Braun K. Bock J. (2005) Methylphenidate treatment can partly reverse early stress related changes of behavior, brain activity and dendritic spine morphology. Dev. Psychobiol. 47, 455.
58. Zehle S., Bock J., Jezierski G., Gruss M. Braun K. (2007) Methylphenidate treatment recovers stress-induced elevated dendritic spine densities in the rodent dorsal anterior cingulate cortex. Dev. Neurobiol. in press.