Nonlinear dose-dependent impact of D1 receptor activation on motor cortex plasticity in humans

Journal of Neuroscience

Volumn 34, Issue 7, 2014, Pages 2744-2753

  Fresnoza, Shane ^a   Paulus, Walter ^a   Nitsche, Michael A ^a   Kuo, Min Fang ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Dopamine; Dopamine receptors; Neuroplasticity; Paired associative stimulation; Transcranial direct current stimulation; Transcranial magnetic stimulation

Indexed keywords

DOPAMINE; DOPAMINE RECEPTORS; NEUROPLASTICITY; PAIRED ASSOCIATIVE STIMULATION; TRANSCRANIAL DIRECT CURRENT STIMULATION; TRANSCRANIAL MAGNETIC STIMULATION;

ADULT; DOPAMINE AGENTS; DOPAMINE ANTAGONISTS; DOUBLE-BLIND METHOD; EVOKED POTENTIALS, MOTOR; FEMALE; HUMANS; LEVODOPA; MALE; MOTOR CORTEX; NEURONAL PLASTICITY; NONLINEAR DYNAMICS; RECEPTORS, DOPAMINE D1; SULPIRIDE; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84893636302     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3655-13.2014     Document Type: Article

References (59)

1. Arnsten AFT (1997) Catecholamine regulation of the prefrontal cortex. J Psychopharmacology 11:151-162. CrossRef
2. Bailey CH, Giustetto M, Huang YY, Hawkins RD, Kandel ER (2000) Is heterosynaptic modulation essential for stabilizing Hebbian plasticity and memory? Nat Rev Neurosci 1:11-20. CrossRef Medline
3. Brozoski TJ, Brown RM, Rosvold HE, Goldman PS (1979) Cognitive deficit caused by regional depletion of dopamine in prefrontal cortex of rhesus monkey. Science 205:929-932. CrossRef Medline
4. Cai JX, Arnsten AF (1997) Dose-dependent effects of the dopamine D1 receptor agonists A77636 or SKF81297 on spatial working memory in aged monkeys. J Pharmacol Exp Ther 283:183-189. Medline
5. Cepeda C, Hurst RS, Altemus KL, Flores-Hernández J, Calvert CR, Jokel ES, Grandy DK, Low MJ, Rubinstein M, Ariano MA, Levine MS (2001) Facilitated glutamatergic transmission in the striatum of D2 dopamine receptor-deficient mice. J Neurophysiol 85:659-670. Medline
6. Chen Z, Ito K, Fujii S, Miura M, Furuse H, Sasaki H, Kaneko K, Kato H, Miyakawa H (1996) Roles of dopamine receptors in long-term depression: enhancement via D1 receptors and inhibition via D2 receptors. Receptors Channels 4:1-8. Medline
7. Cools R (2006) Dopaminergic modulation of cognitive functionimplications for L-DOPA treatment in Parkinson's disease. Neurosci Biobehav Rev 30:1-23. CrossRef Medline
8. Cools R, D'Esposito M (2011) Inverted-U-shaped dopamine actions on human working memory and cognitive control. Biol Psychiatry 69:e113-e125. CrossRef Medline
9. Dubois B, Pillon B (1996) Cognitive deficits in Parkinson's disease. J Neurology 244:2-8. CrossRef
10. Durstewitz D, Seamans JK (2008) The dual-state theory of prefrontal cortex dopamine function with relevance to catechol-O-methyltransferase genotypes and schizophrenia. Biol Psychiatry 64:739-749. CrossRef Medline
11. Flöel A, Breitenstein C, Hummel F, Celnik P, Gingert C, Sawaki L, Knecht S, Cohen LG (2005) Dopaminergic influences on formation of a motor memory. Ann Neurol 58:121-130. CrossRef Medline
12. Floel A, Vomhof P, Lorenzen A, Roesser N, Breitenstein C, Knecht S (2008) Levodopa improves skilled hand functions in the elderly. Eur J Neurosci 27:1301-1307. CrossRef Medline
13. 1 agonist into the rat medial prefrontal cortex. Behav Neurosci 115:934-939. CrossRef Medline
14. Flores-Hernandez J, Hernandez S, Snyder GL, Yan Z, Fienberg AA, Moss SJ, Greengard P, Surmeier DJ (2000) D1 dopamine receptor activation reduces GABA(A) receptor currents in neostriatal neurons through a PKA/DARPP-32/PP1 signaling cascade. J Neurophysiol 83:2996-3004. Medline
15. Goldman-Rakic PS, Castner SA, Svensson TH, Siever LJ, Williams GV (2004) Targeting the dopamine D1 receptor in schizophrenia: insights for cognitive dysfunction. Psychopharmacology 174:3-16. Medline
16. Gotham AM, Brown RG, Marsden CD (1988) 'Frontal' cognitive function in patients with Parkinson's disease 'on' and 'off' levodopa. Brain 111: 299-321. CrossRef Medline
17. Grace AA, Gerfen CR, Aston-Jones G (1998) Catecholamines in the central nervous system. Overview. Adv Pharmacol 42:655-670. CrossRef Medline
18. Granon S, Passetti F, Thomas KL, Dalley JW, Everitt BJ, Robbins TW (2000) Enhanced and impaired attentional performance after infusion of D1 dopaminergic receptor agents into rat prefrontal cortex. J Neurosci 20: 1208-1215. Medline
19. Grundey J, Freznosa S, Klinker F, Lang N, Paulus W, Nitsche MA (2013) Cortical excitability in smoking and not smoking individuals with and without nicotine. Psychopharmacology 229:653-664. CrossRef Medline
20. Gurden H, Takita M, Jay TM (2000) Essential role of D1 but not D2 receptors in the NMDA receptor-dependent long-term potentiation at hippocampal-prefrontal cortex synapses in vivo. J Neurosci 20:RC106. Medline
21. Hasan A, Nitsche MA, Herrmann M, Schneider-Axmann T, Marshall L, Gruber O, Falkai P, Wobrock T (2012) Impaired long-term depression in schizophrenia: a cathodal t DCS pilot study. Brain Stimul 5:475-483. CrossRef Medline
22. Huang YY, Simpson E, Kellendonk C, Kandel ER (2004) Genetic evidence for the bidirectional modulation of synaptic plasticity in the prefrontal cortex by D1 receptors. Proc Natl Acad Sci U S A 101:3236-3241. CrossRef Medline
23. Knecht S, Breitenstein C, Bushuven S, Wailke S, Kamping S, Flöel A, Zwitserlood P, Ringelstein EB (2004) Levodopa: faster and better word learning in normal humans. Ann Neurol 56:20-26. CrossRef Medline
24. Kristin MP-F, Brian M, Daniel A, Babak S, Steven CC (2013) Genetic variation in the human brain dopamine system influences motor learning and its modulation by L-Dopa. PLo S One 8:e61197. CrossRef Medline
25. Kuo MF, Paulus W, Nitsche MA (2008) Boosting focally-induced brain plasticity by dopamine. Cereb Cortex 18:648-651. CrossRef Medline
26. Lisman JE (2001) Three Ca2+ levels affect plasticity differently: the LTP zone, the LTD zone and no man's land. J Physiol 532:285. CrossRef Medline
27. Manahan-Vaughan D, Kulla A (2003) Regulation of depotentiation and long-term potentiation in the dentate gyrus of freely moving rats by dopamine D2-like receptors. Cereb Cortex 13:123-135. CrossRef Medline
28. Misonou H, Mohapatra DP, Park EW, Leung V, Zhen D, Misonou K, Anderson AE, Trimmer JS (2004) Regulation of ion channel localization and phosphorylation by neuronal activity. Nat Neurosci 7:711-718. CrossRef Medline
29. Mockett BG, Guévremont D, Williams JM, Abraham WC (2007) Dopamine D1/D5 receptor activation reverses NMDA receptor-dependent longterm depression in rat hippocampus. J Neurosci 27:2918-2926. CrossRef Medline
30. Momiyama T, Sim JA, Brown DA (1996) Dopamine D1-like receptormediated presynaptic inhibition of excitatory transmission onto rat magnocellular basal forebrain neurones. J Physiol 495:97-106. Medline
31. Monte-Silva K, Kuo MF, Thirugnanasambandam N, Liebetanz D, Paulus W, Nitsche MA (2009) Dose-dependent inverted U-shaped effect of dopamine (D2-like) receptor activation on focal and nonfocal plasticity in humans. J Neurosci 29:6124-6131. CrossRef Medline
32. Monte-Silva K, Liebetanz D, Grundey J, Paulus W, Nitsche MA (2010) Dosage-dependent non-linear effect of L-dopa on human motor cortex plasticity. J Physiol 588:3415-3424. CrossRef Medline
33. Murphy BL, Arnsten AF, Goldman-Rakic PS, Roth RH (1996) Increased dopamine turnover in the prefrontal cortex impairs spatial working memory performance in rats and monkeys. Proc Natl Acad Sci U S A 93:1325-1329. CrossRef Medline
34. Nitsche MA, Paulus W (2001) Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology 57: 1899-1901. CrossRef Medline
35. Nitsche MA, Nitsche MS, Klein CC, Tergau F, Rothwell JC, Paulus W (2003a) Level of action of cathodal DCpolarisation induced inhibition of the human motor cortex. Clin Neurophysiol 114:600-604. CrossRef Medline
36. Nitsche MA, Fricke K, Henschke U, Schlitterlau A, Liebetanz D, Lang N, Henning S, Tergau F, Paulus W (2003b) Pharmacological modulation of cortical excitability shifts induced by transcranial direct current stimulation in humans. J Physiol 553:293-301. CrossRef Medline
37. Nitsche MA, Liebetanz D, Schlitterlau A, Henschke U, Fricke K, Frommann K, Lang N, Henning S, Paulus W, Tergau F (2004) GABAergic modulation of DC stimulation-induced motor cortex excitability shifts in humans. Eur J Neurosci 19:2720-2726. CrossRef Medline
38. Nitsche MA, Lampe C, Antal A, Liebetanz D, Lang N, Tergau F, Paulus W (2006) Dopaminergic modulation of long-lasting direct current-induced cortical excitability changes in the human motor cortex. Eur J Neurosci 23:1651-1657. CrossRef Medline
39. Nitsche MA, Doemkes S, Karaköse T, Antal A, Liebetanz D, Lang N, Tergau F, Paulus W (2007) Shaping the effects of transcranial direct current stimulation of the human motor cortex. J Neurophysiol 97:3109-3117. CrossRef Medline
40. Nitsche MA, Cohen LG, Wassermann EM, Priori A, Lang N, Antal A, Paulus W, Hummel F, Boggio PS, Fregni F, Pascual-Leone A (2008) Transcranial direct current stimulation: state of the art 2008. Brain Stimul 1:206-223. CrossRef Medline
41. Nitsche MA, Kuo MF, Grosch J, Bergner C, Monte-Silva K, Paulus W (2009) D1-receptor impact on neuroplasticity in humans. J Neurosci 29:2648-2653. CrossRef Medline
42. Otani S, Blond O, Desce JM, Crépel F (1998) Dopamine facilitates longterm depression of glutamatergic transmission in rat prefrontal cortex. Neuroscience 85:669-676. CrossRef Medline
43. Pennartz CM, Dolleman-Van der Weel MJ, Kitai ST, Lopes da Silva FH (1992) Presynaptic dopamine D1 receptors attenuate excitatory and inhibitory limbic inputs to the shell region of the rat nucleus accumbens studied in vitro. J Neurophysiol 67:1325-1334. Medline
44. Pina M, Cunningham C (2014) Effects of dopamine receptor antagonists on the acquisition of ethanol-induced conditioned place preference in mice. Psychopharmacology (Berl) 231:459-468. CrossRef Medline
45. Piri M, Rostampour M, Nasehi M, Zarrindast MR (2013) Blockade of the dorsal hippocampal dopamine D1 receptors inhibits the scopolamineinduced state-dependent learning in rats. Neuroscience 252:460-467. CrossRef Medline
46. Rioult-Pedotti MS, Friedman D, Hess G, Donoghue JP (1998) Strengthening of horizontal cortical connections following skill learning. Nat Neurosci 1:230-234. CrossRef Medline
47. Seamans JK, Yang CR (2004) The principal features and mechanisms of dopamine modulation in the prefrontal cortex. Prog Neurobiol 74:1-58. CrossRef Medline
48. Stagg CJ, Nitsche MA (2011) Physiological basis of transcranial direct current stimulation. Neuroscientist 17:37-53. CrossRef Medline
49. Stagg CJ, Best JG, Stephenson MC, O'Shea J, Wylezinska M, Kincses ZT, Morris PG, Matthews PM, Johansen-Berg H (2009) Polarity-sensitive modulation of cortical neurotransmitters by transcranial stimulation. J Neurosci 29:5202-5206. CrossRef Medline
50. Stefan K, Kunesch E, Cohen LG, Benecke R, Classen J (2000) Induction of plasticity in the human motor cortex by paired associative stimulation. Brain 123:572-584. CrossRef Medline
51. Stefan K, Kunesch E, Benecke R, Cohen LG, Classen J (2002) Mechanisms of enhancement of human motor cortex excitability induced by interventional paired associative stimulation. J Physiol 543:699-708. CrossRef Medline
52. Thirugnanasambandam N, Grundey J, Paulus W, Nitsche MA (2011) Dosedependent nonlinear effect of L-dopa on paired associative stimulationinduced neuroplasticity in humans. J Neurosci 31:5294-5299. CrossRef Medline
53. Ueki Y, Mima T, Kotb M, Sawada H, Saiki H, Ikeda A, Begum T, Reza F, Nagamine T, Fukuyama H (2006) Altered plasticity of the human motor cortex in Parkinson's disease. Ann Neurol 59:60-71. CrossRef Medline
54. Vijayraghavan S, Wang M, Birnbaum SG, Williams GV, Arnsten AF (2007) Inverted-U dopamine D1 receptor actions on prefrontal neurons engaged in working memory. Nat Neurosci 10:376-384. CrossRef Medline
55. Williams GV, Castner SA (2006) Under the curve: critical issues for elucidating D1 receptor function in working memory. Neuroscience 139:263-276. CrossRef Medline
56. Witte AV, Flöel A (2012) Effects of COMT polymorphisms on brain function and behavior in health and disease. Brain Res Bull 88:418-428. CrossRef Medline
57. Witte AV, Kürten J, Jansen S, Schirmacher A, Brand E, Sommer J, Flöel A (2012) Interaction of BDNF and COMT polymorphisms on pairedassociative stimulation-induced cortical plasticity. J Neurosci 32:4553-4561. CrossRef Medline
58. Wolters A, Sandbrink F, Schlottmann A, Kunesch E, Stefan K, Cohen LG, Benecke R, Classen J (2003) A temporally asymmetric Hebbian rule governing plasticity in the human motor cortex. J Neurophysiol 89:2339-2345. CrossRef Medline
59. Zahrt J, Taylor JR, Mathew RG, Arnsten AF (1997) Supranormal stimulation of D1 dopamine receptors in the rodent prefrontal cortex impairs spatial working memory performance. J Neurosci 17:8528-8535. Medline