Dopamine modulates persistent synaptic activity and enhances the signal-to-noise ratio in the prefrontal cortex

PLoS ONE

Volumn 4, Issue 8, 2009, Pages

  Kroener, Sven ^a   Chandler, Judson L ^a   Phillips, Paul E M ^b   Seamans, Jeremy K ^c  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE; METIROSINE; RESERPINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; COCULTURE; COGNITION; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DOPAMINERGIC TRANSMISSION; EVOKED RESPONSE; HIPPOCAMPUS; MOUSE; NERVE CELL NETWORK; NEUROMODULATION; NONHUMAN; PREFRONTAL CORTEX; SIGNAL NOISE RATIO; SYNAPTIC TRANSMISSION; VENTRAL TEGMENTUM; ANIMAL; C57BL MOUSE; PATCH CLAMP; PHYSIOLOGY; SYNAPSE;

ANIMALS; COCULTURE TECHNIQUES; DOPAMINE; MICE; MICE, INBRED C57BL; PATCH-CLAMP TECHNIQUES; PREFRONTAL CORTEX; SYNAPSES;

EID: 68349157331     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0006507     Document Type: Article

References (76)

1. Williams GV, Goldman-Rakic PS (1995) Modulation of memory fields by dopamine D1 receptors in prefrontal cortex. Nature 376: 572-575.
2. Murphy BL, Arnsten AFT, Goldman-Rakic PS, Roth RH (1996) Increased dopamine turnover in the prefrontal cortex impairs spatial working memory performance in rats and monkeys. Proc Nat Acad Sci 93: 1325-1329.
3. Sawaguchi T (2001) The effects of dopamine and its antagonists on directional delay-period activity of prefrontal neurons in monkeys during an oculomotor delayed-response task. Neurosci Res 41: 115-28.
4. Winterer G, Weinberger DR (2004) Genes, dopamine and cortical signal-tonoise ratio in schizophrenia. Trends Neurosci 27: 683-90.
5. 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: 376-84.
6. Grace AA (1991) Phasic versus tonic dopamine release and the modulation of dopamine system responsivity: a hypothesis for the etiology of schizophrenia. Neuroscience 41: 1-24.
7. Goto Y, Otani S, Grace AA (2007) The Yin and Yang of dopamine release: a new perspective. Neuropharmacology 53: 583-7.
8. Seamans JK, Yang CR (2004) The principal features and mechanisms of dopamine modulation in the prefrontal cortex. Prog Neurobiol 74: 1-58.
9. Zheng P, Zhang XX, Bunney BS, Shi WX (1999) Opposite modulation by cortical N-methyl-D-aspartate receptor-mediated responses by low and high concentrations of dopamine. Neuroscience 91: 527-535.
10. Trantham-Davidson H, Neely LC, Lavin A, Seamans JK (2004) Mechanisms underlying differential D1 versus D2 dopamine receptor regulation of inhibition in prefrontal cortex. J Neurosci 24: 10652-9.
11. Timofeev I, Grenier F, Steriade M (2001) Disfacilitation and active inhibition in the neocortex during the natural sleep-wake cycle: an intracellular study. Proc Natl Acad Sci 98: 1924-1929.
12. Shu Y, Hasenstaub A, McCormick DA (2003) Turning on and off recurrent balanced cortical activity. Nature 423: 288-93.
13. Haider B, Duque A, Hasenstaub AR, Yu Y, McCormick DA (2007) Enhancement of visual responsiveness by spontaneous local network activity in vivo. J Neurophysiol 97: 4186-202.
14. Matsuda Y, Marzo A, Otani S (2006) The presence of background dopamine signal converts long-term synaptic depression to potentiation in rat prefrontal cortex. J Neurosci 26: 4803-10.
15. Franke H, Schelhorn N, Illes P (2003) Dopaminergic neurons develop axonal projections to their target areas in organotypic co-cultures of the ventral mesencephalon and the striatum/prefrontal cortex. Neurochem Int 42: 431-9.
16. Seamans JK, Nogueira L, Lavin A (2003) Synaptic basis of persistent activity in prefrontal cortex in vivo and in organotypic cultures. Cereb Cortex 13: 242-50.
17. Sawamoto K, Nakao N, Kobayashi K, Matsushita N, Takahashi H, et al. (2001) Visualization, direct isolation, and transplantation of midbrain dopaminergic neurons. Proc Natl Acad Sci 98: 6423-8.
18. Tu Y, Kröner S, Abernathy K, Lapish C, Seamans J, et al. (2007) Ethanol disrupts patterns of persistent activity in prefrontal cortical neurons. J Neurosci 27: 4765-4775.
19. Chen NH, Lai YJ, Pan WH (1997) Effects of different perfusion medium on the extracellular basal concentration of dopamine in striatum and medial prefrontal cortex: a zero-net flux microdialysis study. Neurosci Lett 225: 197-200.
20. Del Arco A, Mora F (2000) Endogenous dopamine potentiates the effects of glutamate on extracellular GABA in the prefrontal cortex of the freely moving rat. Brain Res Bull 53: 339-345.
21. Haider B, Duque A, Hasenstaub AR, McCormick DA (2006) Neocortical network activity in vivo is generated through a dynamic balance of excitation and inhibition. J Neurosci 26: 4535-45.
22. Plenz D, Aertsen A (1996) Neural dynamics in cortex-striatum co-cultures II. Spatiotemporal characteristics of neuronal activity. Neuroscience 70: 893-924.
23. Reynolds JN, Wickens JR (2000) Substantia nigra dopamine regulates synaptic plasticity and membrane potential fluctuations in the rat neostriatum, in vivo. Neuroscience 99: 199-203.
24. West AR, Grace AA (2002) Opposite influences of endogenous dopamine D1 and D2 receptor activation on activity states and electrophysiological properties of striatal neurons: studies combining in vivo intracellular recordings and reverse microdialysis. J Neurosci 22: 294-304.
25. Missale C, Nash SR, Robinson SW, Jaber M, Caron MG (1998) Dopamine receptors: from structure to function. Physiol Rev 78: 189-225.
26. Lee SP, So CH, Rashid AJ, Varghese G, Cheng R, et al. (2004) Dopamine D1 and D2 receptor Co-activation generates a novel phospholipase C-mediated calcium signal. J Biol Chem 279: 35671-8.
27. Neve KA, Seamans JK, Trantham-Davidson H (2004) Dopamine receptor signaling. J Recept Signal Transduct Res 24: 165-205.
28. Yang CR, Seamans JK (1996) Dopamine D1 receptor actions in layer V-VI rat prefrontal cortex neurons in vitro: modulation of dendritic-somatic signal integration. J Neurosci 16: 1922-1935.
29. Gulledge AT, Jaffe DB (1998) Dopamine decreases the excitability of layer V pyramidal cells in the rat prefrontal cortex. J Neurosci 18: 9139-51.
30. Henze DA, Gonzalez-Burgos GR, Urban NN, Lewis DA, Barrionuevo G (2000) Dopamine increases excitability of pyramidal neurons in primate prefrontal cortex. J Neurophysiol 84: 2799-809.
31. Kröner S, Krimer LS, Lewis DA, Barrionuevo G (2007) Dopamine increases inhibition in the monkey dorsolateral prefrontal cortex through cell type-specific modulation of interneurons. Cereb Cortex 17: 1020-32.
32. Seamans JK, Durstewitz D, Christie B, Stevens CF, Sejnowski TJ (2001a) Dopamine D1/D5 receptor modulation of excitatory synaptic inputs to layer V prefrontal cortex neurons. Proc Natl Acad Sci 98: 301-306.
33. Seamans JK, Gorelova N, Durstewitz D, Yang CR (2001b) Bidirectional dopamine modulation of GABAergic inhibition in prefrontal cortical pyramidal neurons. J Neurosci 21: 3628-3638.
34. Tseng KY, Snyder-Keller A, O'Donnell P (2007) Dopaminergic modulation of striatal plateau depolarizations in corticostriatal organotypic cocultures. Psychopharmacology (Berl) 191: 627-40.
35. Timofeev I, Grenier F, Bazhenov M, Sejnowski TJ, Steriade M (2000) Origin of slow cortical oscillations in deafferented cortical slabs. Cereb Cortex 10: 1185-1199.
36. Nestler E, Hyman SE, Malenka RC, eds (2001) Molecular Neuropharmacology: A Foundation for Clinical Neuroscience. New York: McGraw-Hill.
37. Rolls ET, Thorpe SJ, Boytim M, Szabo I, Perrett DI (1984) Responses of striatal neurons in the behaving monkey. 3. Effects of iontophoretically applied dopamine on normal responsiveness. Neuroscience 12: 1201-12.
38. Servan-Schreiber D, Printz H, Cohen JD (1990) A network model of catecholamine effects: gain, signal-to-noise ratio, and behavior. Science 249: 892-5.
39. 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: 739-49.
40. Durstewitz D, Seamans JK, Sejnowski TJ (2000) Dopamine-mediated stabilization of delay-period activity in a network model of prefrontal cortex. J Neurophysiol 83: 1733-50.
41. Durstewitz D, Seamans JK (2002) The computational role of dopamine D1 receptors in working memory. Neural Netwok 15: 561-72.
42. González-Burgos G, Kröner S, Seamans JK, Lewis DA, Barrionuevo G (2005) Dopaminergic modulation of synaptic depression in fast spiking interneurons of the monkey dorsolateral prefrontal cortex. J Neurophysiol 94: 4168-77.
43. Arnsten AF (1997) Catecholamine regulation of the prefrontal cortex. J Psychopharmacol 11: 151-162.
44. Trantham H, Szumlinski KK, McFarland K, Kalivas PW, Lavin A (2002) Repeated cocaine administration alters the electrophysiological properties of prefrontal cortical neurons. Neuroscience 113: 749-53.
45. Trantham-Davidson H, Lavin A (2004) Acute cocaine administration depresses cortical activity. Neuropsychopharmacology 29: 2046-51.
46. Tseng KY, O'Donnell P (2007) Dopamine modulation of prefrontal cortical interneurons changes during adolescence. Cereb Cortex 17: 1235-40.
47. Nicola SM, Surmeier J, Malenka RC (2000) Dopaminergic modulation of neuronal excitability in the striatum and nucleus accumbens. Annu Rev Neurosci 23: 185-215.
48. Hernandez-Lopez S, Bargas J, Surmeier DJ, Reyes A, Galarraga E (1997) D1 receptor activation enhances evoked discharge in neostriatal medium spiny neurons by modulating an L-type Ca2+ conductance. J Neurosci 17: 3334-42.
49. Lavin A, Grace AA (2001) Stimulation of D1-type dopamine receptors enhances excitability in prefrontal cortical pyramidal neurons in a state-dependent manner. Neuroscience 104: 335-46.
50. Singer W (1999) Neuronal synchrony: a versatile code for the definition of relations? Neuron 24: 49-65, 111-25.
51. Lau PM, Bi GQ (2005) Synaptic mechanisms of persistent reverberatory activity in neuronal networks. Proc Natl Acad Sci 102: 10333-8.
52. Sanchez-Vives MV, McCormick DA (2000) Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci 3: 1027-34.
53. Hasenstaub A, Shu Y, Haider B, Kraushaar U, Duque A, et al. (2005) Inhibitory postsynaptic potentials carry synchronized frequency information in active cortical networks. Neuron 47: 423-35.
54. Arieli A, Sterkin A, Grinvald A, Aertsen A (1996) Dynamics of ongoing activity: explanation of the large variability in evoked cortical responses. Science 273: 1868-71.
55. Azouz R, Gray CM (1999) Cellular mechanisms contributing to response variability of cortical neurons in vivo. J Neurosci 19: 2209-23.
56. Tsodyks M, Kenet T, Grinvald A, Arieli A (1999) Linking spontaneous activity of single cortical neurons and the underlying functional architecture. Science 286: 1943-6.
57. Shu Y, Hasenstaub A, Badoual M, Bal T, McCormick DA (2003) Barrages of synaptic activity control the gain and sensitivity of cortical neurons. J Neurosci 23: 10388-401.
58. Leger JF, Stern EA, Aertsen A, Heck D (2005) Synaptic integration in rat frontal cortex shaped by network activity. J Neurophysiol 93: 281-93.
59. Steriade M (2001) Impact of network activities on neuronal properties in corticothalamic systems. J Neurophysiol 86: 1-39.
60. Peters Y, Barnhardt NE, O'Donnell P (2004) Prefrontal cortical up states are synchronized with ventral tegmental area activity. Synapse 52: 143-52.
61. Lewis BL, O'Donnell P (2000) Ventral tegmental area afferents to the prefrontal cortex maintain membrane potential 'up' states in pyramidal neurons via D(1) dopamine receptors. Cereb Cortex 10: 1168-75.
62. Tseng KY, O'Donnell P (2005) Post-pubertal emergence of prefrontal cortical up states induced by D1-NMDA co-activation. Cereb Cortex 15: 49-57.
63. Stewart CV, Plenz D (2006) Inverted-U profile of dopamine-NMDA-mediated spontaneous avalanche recurrence in superficial layers of rat prefrontal cortex. J Neurosci 26: 8148-59.
64. Durstewitz D, Gabriel T (2007) Dynamical basis of irregular spiking in NMDAdriven prefrontal cortex neurons. Cereb Cortex 17: 894-908.
65. Hasenstaub A, Sachdev RN, McCormick DA (2007) State changes rapidly modulate cortical neuronal responsiveness. J Neurosci 27: 9607-22.
66. Timofeev I, Contreras D, Steriade M (1996) Synaptic responsiveness of cortical and thalamic neurones during various phases of slow sleep oscillation in cat. J Physiol 494: 265-78.
67. Winterer G, Ziller M, Dorn H, Frick K, Mulert C, et al. (1999) Cortical activation, signal-to-noise ratio and stochastic resonance during information processing in man. Clin Neurophysiol 110: 1193-203.
68. Muller UU, Ward LM (2000) Stochastic resonance in a statistical model of a time-integrating detector. Physical Review 61: 4286-4294.
69. Moss F, Ward LM, Sannita WG (2004) Stochastic resonance and sensory information processing: a tutorial and review of application. Clin Neurophysiol 115: 267-81.
70. Ward LM, Doesburg SM, Kitajo K, MacLean SE, Roggeveen AB (2006) Neural synchrony in stochastic resonance, attention, and consciousness. Can J Exp Psychol 60: 319-26.
71. Floresco SB, West AR, Ash B, Moore H, Grace AA (2003) Afferent modulation of dopamine neuron firing differentially regulates tonic and phasic dopamine transmission. Nat Neurosci 6: 968-73.
72. Venton BJ, Seipel AT, Phillips PE, Wetsel WC, Gitler D, et al. (2006) Cocaine increases dopamine release by mobilization of a synapsin-dependent reserve pool. J Neurosci 26: 3206-9.
73. Goldman-Rakic PS, Muly EC, Williams GV (2000) D(1) receptors in prefrontal cells and circuits. Brain Res Brain Res Rev 31: 295-301.
74. Brunel N, Wang XJ (2001) Effects of neuromodulation in a cortical network model of object working memory dominated by recurrent inhibition. J Comput Neurosci 11: 63-85.
75. Compte A, Brunel N, Goldman-Rakic PS, Wang XJ (2000) Synaptic mechanisms and network dynamics underlying spatial working memory in a cortical network model. Cereb Cortex 10: 910-23.
76. Durstewitz D, Kelc M, Güntürkün O (1999) A neurocomputational theory of the dopaminergic modulation of working memory functions. J Neurosci 19: 2807-22.