Transcranial direct current stimulation during sleep improves declarative memory

Journal of Neuroscience

Volumn 24, Issue 44, 2004, Pages 9985-9992

  Marshall, Lisa ^a   Mölle, Matthias ^a   Hallschmid, Manfred ^a   Born, Jan ^a  

^a UNIVERSITY OF LÜBECK   (Germany)

Author keywords

Declarative memory; Direct current (DC) potential; Electroencephalography (EEG); Nonrapid eye movement (NonREM) sleep; Slow oscillation; Transcranial direct current stimulation (tDCS)

Indexed keywords

ADULT; ALPHA RHYTHM; ARTICLE; BETA RHYTHM; DEPOLARIZATION; DIRECT CURRENT; ELECTROENCEPHALOGRAPHY; FRONTAL CORTEX; HUMAN; HUMAN EXPERIMENT; LEARNING; MALE; MEMORY; MEMORY CONSOLIDATION; MOOD; MOTOR PERFORMANCE; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL PLASTICITY; NORMAL HUMAN; OSCILLATORY POTENTIAL; PRIORITY JOURNAL; SLEEP PATTERN; SLEEP STAGE; SLOW WAVE SLEEP; THETA RHYTHM; TRANSCRANIAL MAGNETIC STIMULATION; VERBAL MEMORY; WAKEFULNESS;

ADULT; BRAIN; CEREBRAL CORTEX; CROSS-OVER STUDIES; DOUBLE-BLIND METHOD; ELECTRIC STIMULATION; ELECTROENCEPHALOGRAPHY; HUMANS; MALE; MEMORY; MENTAL RECALL; PAIRED-ASSOCIATE LEARNING; POLYSOMNOGRAPHY; SLEEP; SLEEP STAGES; WAKEFULNESS;

EID: 7744226189     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2725-04.2004     Document Type: Article

References (70)

1. Achermann P, Borbely AA (1997) Low-frequency (< 1 Hz) oscillations in the human sleep electroencephalogram. Neuroscience 81:213-222.
2. Amzica F, Steriade M (2000) Neuronal and glial membrane potentials during sleep and paroxysmal oscillations in the neocortex. J Neurosci 20:6648-6665.
3. Amzica F, Massimini M, Manfridi A (2002) Spatial buffering during slow and paroxysmal sleep oscillations in cortical networks of glial cells in vivo. J Neurosci 22:1042-1053.
4. Bazhenov M, Timofeev I, Steriade M, Sejnowski TJ (2002) Model of thalamocortical slow-wave sleep oscillations and transitions to activated states. J Neurosci 22:8691-8704.
5. Bikson M, Inoue M, Akiyama H, Deans JK, Fox JE, Miyakawa H, Jefferys JG (2004) Effects of uniform extracellular DC electric fields on excitability in rat hippocampal slices in vitro. J Physiol (Lond) 557:175-190.
6. Bindman LJ, Lippold OC, Redfearn JW (1962) Long-lasting changes in the level of the electrical activity of the cerebral cortex produced by polarizing currents. Nature 196:584-585.
7. Bindman LJ, Lippold OC, Redfearn JW (1964) The action of brief polarizing currents on the cerebral cortex of the rat (i) during current flowand (ii) in the production of long-lasting after-effects. J Physiol (Lond) 172:369-382.
8. Blaney PH (1986) Affect and memory: a review. Psychol Bull 99:229-246.
9. Born J, Gais S (2003) Roles of early and late nocturnal sleep for the consolidation of human memories. In: Sleep and brain plasticity (Maquet P, Smith C, Stickgold R, eds), pp 65-85. New York: Oxford UP.
10. Bradshaw KD, Emptage NJ, Bliss TV (2003) A role for dendritic protein synthesis in hippocampal late LTP. Eur J Neurosci 18:3150-3152.
11. Brickenkamp R, Zillmer E (2002) d2 test of attention. Göttingen, Germany: Hogrefe and Huber.
12. Buzsáki G (1989) Two-stage model of memory trace formation: a role for "noisy" brain states. Neuroscience 31:551-570.
13. Buzsáki G, Bickford RG, Ponomareff G, Thal LJ, Mandel R, Gage FH (1988) Nucleus basalis and thalamic control of neocortical activity in the freely moving rat. J Neurosci 8:4007-4026.
14. Cauller LJ, Connors BW (1994) Synaptic physiology of horizontal afferents to layer I in slices of rat SI neocortex. J Neurosci 14:751-762.
15. Creutzfeldt OD, Fromm GH, Kapp H (1962) Influence of transcortical dc currents on cortical neuronal activity. Exp Neurol 5:436-452.
16. Ekstrand BR, Barrett TR, West JN, Maier WG (1977) The effect of sleep on human long-term memory. In: Neurobiology of sleep and memory (Drucker-Colin RR, McGaugh JL, eds), pp 419-438. New York: Academic.
17. Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1:1-47.
18. Gais S, Born J (2004) Low acetylcholine during slow-wave sleep is critical for declarative memory consolidation. Proc Natl Acad Sci USA 101:2140-2144.
19. Gais S, Plihal W, Wagner U, Born J (2000) Early sleep triggers memory for early visual discrimination skills. Nat Neurosci 3:1335-1339.
20. Gais S, Mölle M, Helms K, Born J (2002) Learning-dependent increases in sleep spindle density. J Neurosci 22:6830-6834.
21. Gartside IB (1968) Mechanisms of sustained increases of firing rate of neurons in the rat cerebral cortex after polarization: reverberating circuits or modification of synaptic conductance? Nature 220:382-383.
22. Hasselmo ME (1999) Neuromodulation: acetylcholine and memory consolidation. Trends Cogn Sci 3:351-359.
23. Huber R, Ghilardi MF, Massimini M, Tononi G (2004) Local sleep and learning. Nature 430:78-81.
24. Islam N, Moriwaki A, Hattori Y, Hori Y (1994) Anodal polarization induces protein kinase C gamma (PKC gamma)-like immunoreactivity in the rat cerebral cortex. Neurosci Res 21:169-172.
25. Islam N, Moriwaki A, Hori Y (1995) Co-localization of c-fos protein and protein kinase C gamma in the rat brain following anodal polarization. Indian J Physiol Pharmacol 39:209-215.
26. Janke W, Debus G (1978) Die Eigenschaftswörterliste EWL. Eine mehrdimensionale Methode zur Beschreibung von Aspekten des Befindens. Göttingen, Germany: Hogrefe.
27. Jasper HH (1958) The ten-twenty electrode system of the International Federation. Electroencephalogr Clin Neurophysiol 10:371-375.
28. Jefferys JG (1995) Nonsynaptic modulation of neuronal activity in the brain: electric currents and extracellular ions. Physiol Rev 75:689-723.
29. Kim HG, Connors BW (1993) Apical dendrites of the neocortex: correlation between sodium- and calcium-dependent spiking and pyramidal cell morphology. J Neurosci 13:5301-5311.
30. Kudrimoti HS, Barnes CA, McNaughton BL (1999) Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics. J Neurosci 19:4090-4101.
31. Liebetanz D, Nitsche MA, Tergau F, Paulus W (2002) Pharmacological approach to the mechanisms of transcranial DC-stimulation-induced after-effects of human motor cortex excitability. Brain 125:2238-2247.
32. Lolas F (1977) Brain polarization: behavioral and therapeutic effects. Biol Psychiatry 12:37-47.
33. Lutzenberger W, Elbert T (1987) Assessment of effects of weak electric currents on brain and behavior. In: Safety assessment of NMR clinical equipment. (Schmidt KH, ed), pp 36-45. Stuttgart, Germany: Thieme.
34. Maquet P (2001) The role of sleep in learning and memory. Science 294:1052.
35. Marshall L, Mölle M, Fehm HL, Born J (1998) Scalp recorded direct current brain potentials during human sleep. Eur J Neurosci 10:1167-1178.
36. Marshall L, Mölle M, Born J (2003) Spindle and slow wave rhythms at slow wave sleep transitions are linked to strong shifts in the cortical direct current potential. Neuroscience 121:1047-1053.
37. Massimini M, Amzica F (2001) Extracellular calcium fluctuations and intracellular potentials in the cortex during the slow sleep oscillation. J Neurophysiol 85:1346-1350.
38. McCormick DA, Shu Y, Hasenstaub A, Sanchez-Vives M, Badoual M, Bal T (2003) Persistent cortical activity: mechanisms of generation and effects on neuronal excitability. Cereb Cortex 13:1219-1231.
39. McNaughton BL, Barnes CA, Battaglia FP, Bower MR, Cowen SL, Ekstrom AD, Gerrard JL, Hoffman FP, Houston FP, Karten Y, Lipa P, Pennartz CMA, Sutherland GR (2003) Off-line reprocessing of recent memory and its role in memory consolidation: a progress report. In: Sleep and brain plasticity (Maquet P, Smith C, Stickgold R, eds), pp 225-246. New York: Oxford UP.
40. Mednick S, Nakayama K, Stickgold R (2003) Sleep-dependent learning: a nap is as good as a night. Nat Neurosci 6:697-698.
41. Nadasdy Z, Hirase H, Czurko A, Csicsvari J, Buzsáki G (1999) Replay and time compression of recurring spike sequences in the hippocampus. J Neurosci 19:9497-9507.
42. Nitsche MA, Paulus W (2001) Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology 57:1899-1901.
43. Nitsche MA, Liebetanz D, Antal A, Lang N, Tergau F, Paulus W (2003a) Modulation of cortical excitability by weak direct current stimulation- technical, safety and functional aspects. Suppl Clin Neurophysiol 56:255-276.
44. 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 DC stimulation in humans. J Physiol (Lond) 553:293-301.
45. Pandya DN, Yeterian EH (1985) Architecture and connections of cortical association areas. In: Cerebral cortex, Vol 4 (Peters A, Jones EG, eds), pp 3-61. New York: Plenum.
46. Pennartz CM, Uylings HB, Barnes CA, McNaughton BL (2002) Memory reactivation and consolidation during sleep: from cellular mechanisms to human performance. Prog Brain Res 138:143-166.
47. Plihal W, Born J (1997) Effects of early and late nocturnal sleep on declarative and procedural memory. J Cogn Neurosci 9:534-547.
48. Plihal W, Born J (1999) Effects of early and late nocturnal sleep on priming and spatial memory. Psychophysiology 36:571-582.
49. Priori A (2003) Brain polarization in humans: a reappraisal of an old tool for prolonged non-invasive modulation of brain excitability. Clin Neurophysiol 114:589-595.
50. Purpura DP, McMurtry JG (1965) Intracellular activities and evoked potential changes during polarization of motor cortex. J Neurophysiol 28:166-185.
51. Rechtschaffen A, Kales A (1968) A manual of standardized terminology, techniques and scoring system for sleep stages of human subjects. National Institutes of Health Publication 204. Washington, DC: United States Government Printing Office.
52. Rockland KS, Pandya DN (1979) Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey. Brain Res 179:3-20.
53. Roland PE (2002) Dynamic depolarization fields in the cerebral cortex. Trends Neurosci 25:183-190.
54. Schiller J, Schiller Y, Stuart G, Sakmann B (1997) Calcium action potentials restricted to distal apical dendrites of rat neocortical pyramidal neurons. J Physiol 505:605-616.
55. Sejnowski TJ, Destexhe A (2000) Why do we sleep? Brain Res 886:208-223.
56. Shepherd GM, Brayton RK, Miller JP, Segev I, Rinzel J, Rall W (1985) Signal enhancement in distal cortical dendrites by means of interactions between active dendritic spines. Proc Natl Acad Sci USA 82:2192-2195.
57. Shu Y, Hasenstaub A, McCormick DA (2003) Turning on and off recurrent balanced cortical activity. Nature 423:288-293.
58. Siapas AG, Wilson MA (1998) Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron 21:1123-1128.
59. Singer JA, Salovey P (1988) Mood and memory: evaluating the network theory of affect. Clin Psychol Rev 8:211-251.
60. Sirota A, Csicsvari J, Buhl D, Buzsáki G (2003) Communication between neocortex and hippocampus during sleep in rodents. Proc Natl Acad Sci USA 100:2065-2069.
61. Smith C (2001) Sleep states and memory processes in humans: procedural versus declarative memory systems. Sleep Med Rev 5:491-506.
62. Sourdet V, Debanne D (1999) The role of dendritic filtering in associative long-term synaptic plasticity. Learn Mem 6:422-447.
63. Steriade M, Timofeev I (2003) Neuronal plasticity in thalamocortical networks during sleep and waking oscillations. Neuron 37:563-576.
64. Steriade M, Dossi RC, Nuñez A (1991) Network modulation of a slow intrinsic oscillation of cat thalamocortical neurons implicated in sleep delta waves: cortically induced synchronization and brainstem cholinergic suppression. J Neurosci 11:3200-3217.
65. Steriade M, Timofeev I, Grenier F (2001) Natural waking and sleep states: a view from inside neocortical neurons. J Neurophysiol 85:1969-1985.
66. 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 USA 98:1924-1929.
67. Walker MP (2004) A refined model of sleep and the time course of memory. Behav Brain Sci, in press.
68. Watson D, Clark LA, Tellegen A (1998) Development and validation of brief measures of positive and negative affect: the PANAS scales. J Pers Soc Psychol 54:1063-1070.
69. Wong-Riley M (1978) Reciprocal connections between striate and prestriate cortex in squirrel monkey as demonstrated by combined peroxidase histochemistry and autoradiography. Brain Res 147:159-164.
70. Zeki S, Shipp S (1988) The functional logic of cortical connections. Nature 335:311-317.