Differential effects of methylphenidate and cocaine on GABA transmission in sensory thalamic nuclei

Journal of Neurochemistry

Volumn 124, Issue 5, 2013, Pages 602-612

  Goitia, Belén ^a,b   Raineri, Mariana ^a,b   González, Laura E ^a,d   Rozas, José L ^a   Garcia Rill, Edgar ^c   Bisagno, Verõnica ^b   Urbano, Francisco J ^a  

^a INSTITUTO DE FISIOLOGÍA   (Argentina)

^b Instituto de Investigaciones Farmacologicas   (Argentina)

^c UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^d INSTITUTO DE INVESTIGACIONES EN INGENIERÍA GENÉTICA Y BIOLOGÍA MOLECULAR   (Argentina)

Author keywords

cocaine; GABAergic transmission; methylphenidate; T type calcium channels; thalamic reticular nucleus; ventrobasal thalamic nucleus

Indexed keywords

4 AMINOBUTYRIC ACID; CALCIUM CHANNEL T TYPE; CALCIUM ION; COCAINE; GLUTAMATE DECARBOXYLASE 67; METHYLPHENIDATE;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM CURRENT; CONTROLLED STUDY; FACILITATION; GABAERGIC TRANSMISSION; LOCOMOTION; MALE; MOUSE; NERVE CELL INHIBITION; NERVE PROJECTION; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; THALAMUS RETICULAR NUCLEUS; THALAMUS VENTRAL NUCLEUS; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CENTRAL NERVOUS SYSTEM STIMULANTS; COCAINE; GAMMA-AMINOBUTYRIC ACID; MALE; METHYLPHENIDATE; MICE; MICE, INBRED C57BL; PATCH-CLAMP TECHNIQUES; SYNAPTIC TRANSMISSION; THALAMIC NUCLEI;

MUS;

EID: 84874116550     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12113     Document Type: Article

References (71)

1. Argento J. K., Arvanitogiannis A., and, Flores C., (2012) Juvenile exposure to methylphenidate reduces cocaine reward and alters netrin-1 receptor expression in adulthood. Behav. Brain Res. 229, 202-207.
2. Berger A. J., and, Takahashi T., (1990) Serotonin enhances a low-voltage-activated calcium current in rat spinal motoneurons. J. Neurosci. 10, 1922-1928.
3. Biederman J., Wilens T., Mick E., Spencer T., and, Faraone S. V., (1999) Pharmacotherapy of attention-deficit/hyperactivity disorder reduces risk for substance use disorder. Pediatrics 104, e20.
4. Bisagno V., Raineri M., Peskin V., Wikinski S. I., Uchitel O. D., Llinás R. R., and, Urbano F. J., (2010) Effects of T-type calcium channel blockers on cocaine-induced hyperlocomotion and thalamocortical GABAergic abnormalities in mice. Psychopharmacology (Berl) 212, 205-214.
5. Brandon C. L., Marinelli M., Baker L. K., and, White F. J., (2001) Enhanced reactivity and vulnerability to cocaine following methylphenidate treatment in adolescent rats. Neuropsychopharmacology 25, 651-661. (Pubitemid 32995947)
6. Carlezon W. A. Jr, Mague S. D., and, Andersen S. L., (2003) Enduring behavioral effects of early exposure to methylphenidate in rats. Biol. Psychiatry 54, 1330-1337. (Pubitemid 37522156)
7. Chait L. D., (1994) Reinforcing and subjective effects of methylphenidate in humans. Behav. Pharmacol. 5, 281-288. (Pubitemid 24217290)
8. Clarke A. R., Barry R. J., McCarthy R., Selikowitz M., Brown C. R., and, Croft R. J., (2003) Effects of stimulant medications on the EEG of children with attention-deficit/hyperactivity disorder predominantly inattentive type. Int. J. Psychophysiol. 47, 129-137. (Pubitemid 36144025)
9. Contreras D., Currõ Dossi R., and, Steriade M., (1993) Electrophysiological properties of cat reticular thalamic neurones in vivo. J. Physiol. (Lond.) 470, 273-294. (Pubitemid 23322489)
10. Crandall S. R., Govindaiah G., and, Cox C. L., (2010) Low-threshold Ca2+ current amplifies distal dendritic signaling in thalamic reticular neurons. J. Neurosci. 30, 15419-15429.
11. De Biasi S., Amadeo A., Arcelli P., Frassoni C., and, Spreafico R., (1997) Postnatal development of GABA-immunoreactive terminals in the reticular and ventrobasal nuclei of the rat thalamus: a light and electron microscopic study. Neuroscience 76, 503-515. (Pubitemid 27008480)
12. Devlin R. J., and, Henry J. A., (2008) Clinical review: major consequences of illicit drug consumption. Crit. Care 12, 202-208.
13. Drerup J. M., Hayashi K., Cui H., Mettlach G. L., Long M. A., Marvin M., Sun X., Goldberg M. S., Lutter M., and, Bibb J. A., (2010) Attention-deficit/ hyperactivity phenotype in mice lacking the cyclin-dependent kinase 5 cofactor p35. Biol. Psychiatry 68, 1163-1171.
14. Du C., Yu M., Volkow N. D., Koretsky A. P., Fowler J. S., and, Benveniste H., (2006) Cocaine increases the intracellular calcium concentration in brain independently of its cerebrovascular effects. J. Neurosci. 26, 11522-11531. (Pubitemid 44772123)
15. Erlij D., Acosta-García J., Rojas-Márquez M., González-Hernández B., Escartín-Perez E., Aceves J., and, Florán B., (2012) Dopamine D4 receptor stimulation in GABAergic projections of the globus pallidus to the reticular thalamic nucleus and the substantia nigra reticulata of the rat decreases locomotor activity. Neuropharmacology 62, 1111-1118.
16. Esclapez M., Tillakaratne N. J., Kaufman D. L., Tobin A. J., and, Houser C. R., (1994) Comparative localization of two forms of glutamic acid decarboxylase and their mRNAs in rat brain supports the concept of functional differences between the forms. J. Neurosci. 14, 1834-1855. (Pubitemid 24080030)
17. Federici M., Geracitano R., Bernardi G., and, Mercuri N. B., (2005) Actions of methylphenidate on dopaminergic neurons of the ventral midbrain. Biol. Psychiatry 57, 361-365. (Pubitemid 40215765)
18. Florán B., Florán L., Erlij D., and, Aceves J., (2004) Activation of dopamine D4 receptors modulates [3H]GABA release in slices of the rat thalamic reticular nucleus. Neuropharmacology 46, 497-503. (Pubitemid 38224435)
19. Fraser D. D., and, MacVicar B. A., (1991) Low-threshold transient calcium current in rat hippocampal lacunosum-moleculare interneurons: kinetics and modulation by neurotransmitters. J. Neurosci. 11, 2812-2820.
20. Gatley S. J., Pan D., Chen R., Chaturvedi G., and, Ding Y. S., (1996) Affinities of methylphenidate derivatives for dopamine, norepinephrine and serotonin transporters. Life Sci. 58, 231-239. (Pubitemid 126352709)
21. Glowinski J., and, Axelrod J., (1966) Effects of drugs on the disposition of H-3-norepinephrine in the rat brain. Pharmacol. Rev. 18, 775-785.
22. Govindaiah G., Wang T., Gillette M. U., Crandall S. R., and, Cox C. L., (2010) Regulation of inhibitory synapses by presynaptic D dopamine receptors in thalamus. J. Neurophysiol. 104, 2757-2765.
23. Guerriero R. M., Hayes M. M., Dhaliwal S. K., Ren J. Q., and, Kosofsky B. E., (2006) Preadolescent methylphenidate versus cocaine treatment differ in the expression of cocaine-induced locomotor sensitization during adolescence and adulthood. Biol. Psychiatry 60, 1171-1180. (Pubitemid 44693530)
24. Howes S. R., Dalley J. W., Morrison C. H., Robbins T. W., and, Everitt B. J., (2000) Leftward shift in the acquisition of cocaine self-administration in isolation-reared rats: relationship to extracellular levels of dopamine, serotonin and glutamate in the nucleus accumbens and amygdala-striatal FOS expression. Psychopharmacology (Berl) 151, 55-63. (Pubitemid 30639840)
25. Huguenard J. R., and, Prince D. A., (1992) A novel T-type current underlies prolonged Ca(2+)-dependent burst firing in GABAergic neurons of rat thalamic reticular nucleus. J. Neurosci. 12, 3804-3817.
26. Huguenard J. R., and, Prince D. A., (1994) Intrathalamic rhythmicity studied in vitro: nominal T-current modulation causes robust antioscillatory effects. J. Neurosci. 14, 5485-5502. (Pubitemid 24279067)
27. Iwasaki S., Momiyama A., Uchitel O. D., and, Takahashi T., (2000) Developmental changes in calcium channel types mediating central synaptic transmission. J. Neurosci. 20, 59-65. (Pubitemid 30220491)
28. Jahnsen H., and, Llinás R., (1984a) Electrophysiological properties of guinea-pig thalamic neurones: an in vitro study. J. Physiol. (Lond.) 349, 205-226. (Pubitemid 14060329)
29. Jahnsen H., and, Llinás R., (1984b) Ionic basis for the electro-responsiveness and oscillatory properties of guinea pig thalamic neurones in vitro. J. Physiol. (Lond.) 349, 227-247. (Pubitemid 14060330)
30. Jeanmonod D., Schulman J., Ramirez R., et al,. (2003) Neuropsychiatric thalamocortical dysrhythmia: surgical implications. Neurosurg. Clin. N. Am. 14, 251-265.
31. Kovács K., Sík A., Ricketts C., and, Timofeev I., (2010) Subcellular distribution of low-voltage activated T-type Ca2+ channel subunits (Ca(v)3.1 and Ca(v)3.3) in reticular thalamic neurons of the cat. J. Neurosci. Res. 88, 448-460.
32. Kuczenski R., and, Segal D. S., (1992) Differential effects of amphetamine and dopamine uptake blockers (cocaine, nomifensine) on caudate and accumbens dialysate dopamine and 3-methoxytyramine. J. Pharmacol. Exp. Ther. 262, 1085-1094.
33. Kuczenski R., and, Segal D. S., (1997) Effects of methylphenidate on extracellular dopamine, serotonin, and norepinephrine: comparison with amphetamine. J. Neurochem. 68, 2032-2037. (Pubitemid 27176139)
34. Kuczenski R., and, Segal D. S., (2001) Locomotor effects of acute and repeated threshold doses of amphetamine and methylphenidate: relative roles of dopamine and norepinephrine. J. Pharmacol. Exp. Ther. 296, 876-883. (Pubitemid 32187360)
35. Laemmli U. K., (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
36. Landisman C. E., Long M. A., Beierlein M., Deans M. R., Paul D. L., and, Connors B. W., (2002) Electrical synapses in the thalamic reticular nucleus. J. Neurosci. 22, 1002-1009. (Pubitemid 34141779)
37. Liao Y. F., Tsai M. L., Chen C. C., and, Yen C. T., (2011) Involvement of the Cav3.2 T-type calcium channel in thalamic neuron discharge patterns. Mol. Pain 7, 43-53.
38. Llinás R., and, Geijo-Barrientos E., (1988) In vitro studies of mammalian thalamic and reticularis thalami neurons, in Cellular Thalamic Mechanisms, (, Bentivoglio M., and, Spreafico R., eds), pp. 23-33. Elsevier Science B. V, Amsterdam.
39. Llinás R. R., Ribary U., Jeanmonod D., Kronberg E., and, Mitra P. P., (1999) Thalamocortical dysrhythmia: a neurological and neuropsychiatric syndrome characterized by magnetoencephalography. Proc. Natl Acad. Sci. USA 96, 15222-15227. (Pubitemid 30019793)
40. Ma Y., Ma H., Hong J. T., Kim Y. B., Nam S. Y., and, Oh K. W., (2008) Cocaine withdrawal enhances pentobarbital-induced sleep in rats: evidence of GABAergic modulation. Behav. Brain Res. 194, 114-117.
41. McCormick D. A., and, Feeser H. R., (1990) Functional implications of burst firing and single spike activity in lateral geniculate relay neurons. Neuroscience 39, 103-113.
42. Morton W. A., and, Stockton G. G., (2000) Methylphenidate abuse and psychiatric side effects. Prim. Care Companion J. Clin. Psychiatry 2, 159-164.
43. Pan D., Gatley S. J., Dewey S. L., Chen R., Alexoff D. A., Ding Y. S., and, Fowler J. S., (1994) Binding of bromine-substituted analogs of methylphenidate to monoamine transporters. Eur. J. Pharmacol. 264, 177-182. (Pubitemid 24319801)
44. Pedroarena C., and, Llinás R., (1997) Dendritic calcium conductances generate high-frequency oscillation in thalamocortical neurons. Proc. Natl Acad. Sci. USA 94, 724-728. (Pubitemid 27053701)
45. Pinault D., and, Deschênes M., (1992) Voltage-dependent 40-Hz oscillations in rat reticular thalamic neurons in vivo. Neuroscience 51, 245-258.
46. Ritz M. C., Lamb R. J., Goldberg S. R., and, Kuhar M. J., (1987) Cocaine receptors on dopamine transporters are related to self-administration of cocaine. Science 237, 1219-1223. (Pubitemid 17131228)
47. Rodríguez J. J., Noristani H. N., Hoover W. B., Linley S. B., and, Vertes R. P., (2011) Serotonergic projections and serotonin receptor expression in the reticular nucleus of the thalamus in the rat. Synapse 65, 919-928.
48. Ross S. B., and, Renyi A. L., (1969) Inhibition of the uptake of tritiated 5-hydroxytryptamine in brain tissue. Eur. J. Pharmacol. 7, 270-277.
49. Rowe D. L., Robinson P. A., and, Gordon E., (2005) Stimulant drug action in attention deficit hyperactivity disorder (ADHD): inference of neurophysiological mechanisms via quantitative modelling. Clin. Neurophysiol. 116, 324-335. (Pubitemid 40136539)
50. Rutter J. J., Baumann M. H., and, Waterhouse B. D., (1998) Systemically administered cocaine alters stimulus-evoked responses of thalamic somatosensory neurons to perithreshold vibrissae stimulation. Brain Res. 798, 7-17. (Pubitemid 28342015)
51. Segal D. S., and, Kuczenski R., (1999) Escalating dose-binge treatment with methylphenidate: role of serotonin in the emergent behavioral profile. J. Pharmacol. Exp. Ther. 291, 19-30. (Pubitemid 29451568)
52. Shammah-Lagnado S. J., Alheid G. F., and, Heimer L., (1996) Efferent connections of the caudal part of the globus pallidus in the rat. J. Comp. Neurol. 376, 489-507. (Pubitemid 26419121)
53. Shoji S., Simms D., Yamada K., and, Gallagher J. P., (1998) Cocaine administered in vitro to brain slices from rats treated with cocaine chronically in vivo results in a gamma-aminobutyric acid receptor-mediated hyperpolarization recorded from the dorsolateral septum. J. Pharmacol. Exp. Ther. 286, 509-518. (Pubitemid 28318027)
54. Spangler R., Unterwald E. M., and, Kreek M. J., (1993) 'Binge' cocaine administration induces a sustained increase of prodynorphin mRNA in rat caudate-putamen. Brain Res. Mol. Brain Res. 19, 323-327.
55. Spreafico R., Battaglia G., and, Frassoni C., (1991) The reticular thalamic nucleus (RTN) of the rat: cytoarchitectural, Golgi, immunocytochemical, and horseradish peroxidase study. J. Comp. Neurol. 304, 478-490.
56. Steriade M., (2005) Sleep, epilepsy and thalamic reticular inhibitory neurons. Trends Neurosci. 28, 317-324. (Pubitemid 40775777)
57. Steriade M., and, Llinás R. R., (1988) The functional states of the thalamus and the associated neuronal interplay. Physiol. Rev. 68, 649-742.
58. Sun Y. G., Wu C. S., Renger J. J., Uebele V. N., Lu H. C., and, Beierlein M., (2012) GABAergic synaptic transmission triggers action potentials in thalamic reticular nucleus neurons. J. Neurosci. 32, 7782-7790.
59. Talley E. M., Cribbs L. L., Lee J. H., Daud A., Perez-Reyes E., and, Bayliss D. A., (1999) Differential distribution of three members of a gene family encoding low voltage-activated (T-type) calcium channels. J. Neurosci. 19, 1895-1911. (Pubitemid 29133368)
60. Thanos P. K., Bermeo C., Rubinstein M., Suchland K. L., Wang G. J., Grandy D. K., and, Volkow N. D., (2010) Conditioned place preference and locomotor activity in response to methylphenidate, amphetamine and cocaine in mice lacking dopamine D4 receptors. J. Psychopharmacol. 24, 897-904.
61. Tsakiridou E., Bertollini L., de Curtis M., Avanzini G., and, Pape H. C., (1995) Selective increase in T-type calcium conductance of reticular thalamic neurons in a rat model of absence epilepsy. J. Neurosci. 15, 3110-3117.
62. Urbano F. J., Bisagno V., Wikinski S. I., Uchitel O. D., and, Llinás R. R., (2009) Cocaine Acute "Binge" Administration Results in Altered Thalamocortical Interactions in Mice. Biol. Psychiatry 66, 769-776.
63. Volkow N. D., and, Insel T. R., (2003) What are the long-term effects of methylphenidate treatment? Biol. Psychiatry 54, 1307-1309. (Pubitemid 37522152)
64. Volkow N. D., and, Swanson J. M., (2003) Variables that affect the clinical use and abuse of methylphenidate in the treatment of ADHD. Am. J. Psychiatry 160, 1909-1918. (Pubitemid 39619623)
65. Volkow N. D., Ding Y. S., Fowler J. S., et al,. (1995) Is methylphenidate like cocaine? Studies on their pharmacokinetics and distribution in the human brain. Arch. Gen. Psychiatry 52, 456-463.
66. Volkow N. D., Wang G. J., Fowler J. S., Logan J., Gatley S. J., Wong C., Hitzemann R., and, Pappas N. R., (1999a) Reinforcing effects of psychostimulants in humans are associated with increases in brain dopamine and occupancy of D(2) receptors. J. Pharmacol. Exp. Ther. 291, 409-415. (Pubitemid 29451617)
67. Volkow N. D., Wang G. J., Fowler J. S., et al,. (1999b) Methylphenidate and cocaine have similar in vivo potency to block the dopamine transporters in the human brain. Life Sci. 65, 7-12.
68. Volkow N. D., Wang G. J., Tomasi D., et al,. (2012) Methylphenidate- elicited dopamine increases in ventral striatum are associated with long-term symptom improvement in adults with attention deficit hyperactivity disorder. J. Neurosci. 32, 841-849.
69. Wise R. A., and, Bozarth M. A., (1987) A psychomotor stimulant theory of addiction. Psychol. Rev. 94, 469-492.
70. Zhang S. J., Huguenard J. R., and, Prince D. A., (1997) GABAA receptor-mediated Cl- currents in rat thalamic reticular and relay neurons. J. Neurophysiol. 78, 2280-2286. (Pubitemid 27495457)
71. Zhang Z. W., Zak J. D., and, Liu H., (2010) MeCP2 is required for normal development of GABAergic circuits in the thalamus. J. Neurophysiol. 103, 2470-2481.