The effect of transcranial direct current stimulation: A role for cortical excitation/inhibition balance?

Frontiers in Human Neuroscience

Volumn , Issue SEP, 2013, Pages

  Krause, Beatrix ^a   Márquez Ruiz, Javier ^b   Cohen Kadosh, Roi ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSIDAD PABLO DE OLAVIDE   (Spain)

Author keywords

Cognition; Excitation; GABA; Glutamate; Inhibition; Transcranial direct current stimulation (tDCS)

Indexed keywords

4 AMINOBUTYRIC ACID; NEUROTRANSMITTER;

ATTENTION DEFICIT DISORDER; BRAIN CORTEX; BRAIN DEPTH STIMULATION; BRAIN REGION; COGNITIVE DEFECT; GABAERGIC SYSTEM; HUMAN; LONG TERM POTENTIATION; MENTAL PERFORMANCE; NERVE CELL INHIBITION; NERVE CELL NETWORK; NEUROCHEMISTRY; NEUROMODULATION; NONHUMAN; REVIEW; SYNAPTIC TRANSMISSION; TRANSCRANIAL DIRECT CURRENT STIMULATION;

EID: 84884697656     PISSN: 16625161     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnhum.2013.00602     Document Type: Review

References (53)

1. Arcos-Burgos, M., Londono, A. C., Pineda, D. A., Lopera, F., Palacio, J. D., Arbelaez, A., et al. (2012). Analysis of brain metabolism by proton magnetic resonance spec-troscopy (1H-MRS) in attention-deficit/hyperactivity disorder suggests a generalized differential onto-genic pattern from controls. Atten. Defic. Hyperact. Disord. 4, 205-212. doi: 10.1007/s12402-012-0088-0
2. Atallah, B. V., and Scanziani, M. (2009). Instantaneous modulation of gamma oscillation frequency by balancing excitation with inhibition. Neuron 62, 566-577. doi: 10.1016/j. neuron.2009.04.027
3. Belousov, A. B. (2012). Novel model for the mechanisms of glutamate-dependent excitotoxicity: role of neuronal gap junctions. Brain Res. 1487, 123-130. doi: 10.1016/j.brainres.2012.05.063
4. Bikson, M., Inoue, M., Akiyama, H., Deans, J. K., Fox, J. E., Miyakawa, H., et al. (2004). Effects of uniform extracellular DC electric fields on excitability in rat hippocampal slices in vitro. J. Physiol. 557, 175-190. doi: 10.1113/jphysiol.2003. 055772
5. Bindman, L. J., Lippold, O. C., and Redfearn, J. W. (1964). The action of brief polarizing currents on the cerebral cortex of the rat (1) during current flow and (2) in the production of long-lasting after-effects. J. Physiol. 172, 369-382.
6. Carrey, N. J., Macmaster, F. P., Gaudet, L., and Schmidt, M. H. (2007). Striatal creatine and glutamate/glutamine in attention-deficit/hyperactivity disorder. J. Child Adolesc. Psychopharmacol. 17, 11-17. doi: 10.1089/cap.2006.0008
7. Clark, V. P., Coffman, B. A., Trumbo, M. C., and Gasparovic, C. (2011). Transcranial direct current stimulation (tDCS) produces localized and specific alterations in neurochem-istry: a (1)H magnetic resonance spectroscopy study. Neurosci. Lett. 500, 67-71. doi: 10.1016/j.neulet. 2011.05.244
8. Cohen Kadosh, R. (2013). Using transcranial electrical stimulation to enhance cognitive functions in the typical and atypical brain. Transl. Neurosci. 4, 20-33. doi: 10. 2478/s13380-013-0104-7
9. David, C. N., Rapoport, J. L., and Gogtay, N. (2013). Treatments in context: transcranial direct current brain stimulation as a potential treatment in pediatric psychosis. Expert Rev. Neurother. 13, 447-458. doi: 10.1586/ern.13.29
10. Edden, R. A., Crocetti, D., Zhu, H., Gilbert, D. L., and Mostofsky, S. H. (2012). Reduced GABA concentration in attention-deficit/ hyperactivity disorder. Arch. Gen. Psychiatry 69, 750-753. doi: 10. 1001/archgenpsychiatry.2011.2280
11. Eichler, S. A., and Meier, J. C. (2008). E-I balance and human diseases - from molecules to networking. Front. Mol. Neurosci. 1:2. doi: 10. 3389/neuro.02.002.2008
12. Faden, A. I., Demediuk, P., Panter, S. S., and Vink, R. (1989). The role of excitatory amino acids and NMDA receptors in traumatic brain injury. Science 244, 798-800. doi:10.1126/science.2567056
13. Floyer-Lea, A., Wylezinska, M., Kinc-ses, T., and Matthews, P. M. (2006). Rapid modulation of GABA concentration in human sensorimotor cortex during motor learning. J. Neu-rophysiol. 95, 1639-1644. doi: 10. 1152/jn.00346.2005
14. Fregni, F., Boggio, P. S., Santos, M. C., Lima, M., Vieira, A. L., Rigonatti, S. P., et al. (2006). Noninvasive cortical stimulation with transcranial direct current stimulation in Parkinson's disease. Mov. Disord. 21, 1693-1702. doi: 10.1002/mds.21012
15. Fritsch, B., Reis, J., Martinowich, K., Schambra, H. M., Ji, Y., Cohen, L. G., et al. (2010). Direct current stimulation promotes BDNF-dependent synaptic plasticity: potential implications for motor learning. Neuron 66, 198-204. doi: 10.1016/j.neuron. 2010.03.035
16. Frohlich, F., and McCormick, D. A. (2010). Endogenous electric fields may guide neocortical network activity. Neuron 67, 129-143. doi: 10.1016/j.neuron.2010.06.005
17. Goto, N., Yoshimura, R., Moriya, J., Kakeda, S., Ueda, N., Ikenouchi-Sugita, A., et al. (2009). Reduction of brain gamma-aminobutyric acid (GABA) concentrations in early-stage schizophrenia patients: 3T Proton MRS study. Schizophr. Res. 112, 192-193. doi: 10.1016/j.schres. 2009.04.026
18. Haider, B., Duque, A., Hasenstaub, A. R., and McCormick, D. A. (2006). Neocortical network activity in vivo is generated through a dynamic balance of excitation and inhibition. J. Neurosci. 26, 4535-4545. doi: 10. 1523/jneurosci.5297-05.2006
19. Harris, R. E., and Clauw, D. J. (2012). Imaging central neurochemical alterations in chronic pain with proton magnetic resonance spectroscopy. Neurosci. Lett. 520, 192-196. doi: 10.1016/j.neulet.2012. 03.042
20. Hess, G., and Donoghue, J. P. (1994). Long-term potentiation of horizontal connections provides a mechanism to reorganize cortical motor maps. J. Neurophysiol. 71, 2543-2547.
21. Jacobs, K. M., and Donoghue, J. P. (1991). Reshaping the cortical motor map by unmasking latent intracortical connections. Science 251, 944-947. doi: 10.2307/2874910
22. Jacobson, L., Koslowsky, M., and Lavi-dor, M. (2012). tDCS polarity effects in motor and cognitive domains: a meta-analytical review. Exp. Brain Res. 216, 1-10. doi: 10.1007/s00221-011-2891-9
23. Jocham, G., Hunt, L. T., Near, J., and Behrens, T. E. (2012). A mechanism for value-guided choice based on the excitation-inhibition balance in prefrontal cortex. Nat. Neurosci. 15, 960-961. doi: 10.1038/nn.3140
24. Kabakov, A. Y., Muller, P. A., Pascual-Leone, A., Jensen, F. E., and Rotenberg, A. (2012). Contribution of axonal orientation to pathway-dependent modulation of excitatory transmission by direct current stimulation in isolated rat hippocampus. J. Neurophysiol. 107, 1881-1889. doi: 10.1152/jn.00715.2011
25. Khedr, E. M., Shawky, O. A., El-Hammady, D. H., Rothwell, J. C., Darwish, E. S., Mostafa, O. M., et al. (2013). Effect of anodal versus cathodal transcranial direct current stimulation on stroke rehabilitation: a pilot randomized controlled trial. Neurorehabil. Neural Repair 27, 592-601. doi: 10. 1177/1545968313484808
26. Krause, B., and Cohen Kadosh, R. (2013). Can transcranial electrical stimulation improve learning difficulties in atypical brain development? A future possibility for cognitive training. Dev. Cogn. Neu-rosci. doi: 10.1016/j.dcn.2013.04. 001. [Epub ahead of print].
27. Kubas, B., Kulak, W., Sobaniec, W., Tarasow, E., Lebkowska, U., and Walecki, J. (2012). Metabolite alterations in autistic children: a 1H MR spectroscopy study. Adv. Med. Sci. 57, 152-156. doi: 10.2478/v10039-012-0014-x
28. Kuo, M.-F., and Nitsche, M. A. (2012). Effects of transcranial electrical stimulation on cognition. Clin. EEG Neurosci. 43, 192-199. doi:10.1177/1550059412444975
29. Long, Z., Medlock, C., Dzemidzic, M., Shin, Y. W., Goddard, A. W., and Dydak, U. (2013). Decreased GABA levels in anterior cingu-late cortex/medial prefrontal cortex in panic disorder. Prog. Neu-ropsychopharmacol. Biol. Psychiatry 44, 131-135. doi: 10.1016/j.pnpbp. 2013.01.020
30. Marquez-Ruiz, J., Leal-Campanario, R., Sanchez-Campusano, R., Molaee-Ardekani, B., Wendling, F., Miranda, P. C., et al. (2012). Transcranial direct-current stimulation modulates synaptic mechanisms involved in associative learning in behaving rabbits. Proc. Natl. Acad. Sci. U S A 109, 6710-6715. doi: 10.1073/pnas.1121147109
31. McCormick, D. A. (1992). Neuro-transmitter actions in the thala-mus and cerebral cortex and their role in neuromodulation of thala-mocortical activity. Prog. Neurobiol. 39, 337-388. doi: 10.1016/0301-0082(92)90012-4
32. Molaee-Ardekani, B., Marquez-Ruiz, J., Merlet, I., Leal-Campanario, R., Gruart, A., Sanchez-Campusano, R., et al. (2013). Effects of transcranial Direct Current Stimulation (tDCS) on cortical activity: a computational modeling study. Brain Stimul. 6, 25-39. doi: 10.1016/j.brs.2011. 12.006
33. Moreno-Duarte, I., Morse, L., Alam, M., Bikson, M., Zafonte, R., and Fregni, F. (2013). Targeted therapies using electrical and magnetic neural stimulation for the treatment of chronic pain in spinal cord injury. Neuroimage doi:10.1016/j. neuroimage.2013.05.097. [Epub ahead of print].
34. Morgan, P. T., Pace-Schott, E. F., Mason, G. F., Forselius, E., Fasula, M., Valentine, G. W., et al. (2012). Cortical GABA levels in primary insomnia. Sleep 35, 807-814. doi: 10.5665/sleep.1880
35. Nicoll, R. A., Malenka, R. C., and Kauer, J. A. (1990). Functional comparison of neurotransmitter receptor subtypes in mammalian central nervous system. Physiol. Rev. 70, 513-565.
36. Nitsche, M. A., and Paulus, W. (2001). Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology 57, 1899-1901. doi: 10. 1212/wnl.57.10.1899
37. Nitsche, M. A., Nitsche, M. S., Klein, C. C., Tergau, F., Rothwell, J. C., and Paulus, W. (2003). Level of action of cathodal DC polarisation induced inhibition of the human motor cortex. Clin. Neurophysiol. 114, 600-604. doi: 10.1016/s1388-2457(02)00412-1
38. Polania, R., Paulus, W., and Nitsche, M. A. (2012). Modulating cortico-striatal and thalamo-cortical functional connectivity with transcranial direct current stimulation. Hum. Brain Mapp. 33, 2499-2508. doi:10.1002/hbm.21380
39. Radman, T., Ramos, R. L., Brumberg, J. C., and Bikson, M. (2009). Role of cortical cell type and morphology in subthreshold and suprathresh-old uniform electric field stimulation in vitro. Journal Brain Stimul. 2, 215-228, 228.e1-3. doi: 10.1016/j.brs. 2009.03.007
40. Reato, D., Rahman, A., Bikson, M., and Parra, L. C. (2010). Low-Intensity electrical stimulation affects network dynamics by modulating population rate and spike timing. J. Neurosci. 30, 15067-15079. doi:10.1523/jneurosci.2059-10.2010
41. Rojas, D. C., Singel, D., Steinmetz, S., Hepburn, S., and Brown, M. S. (2013). Decreased left perisylvian GABA concentration in children with autism and unaffected siblings. Neuroimage doi: 10.1016/j. neuroimage.2013.01.045. [Epub ahead of print].
42. Rowland, L. M., Kontson, K., West, J., Edden, R. A., Zhu, H., Wijtenburg, S. A., et al. (2013). In vivo measurements of Glutamate, GABA, and NAAG in Schizophrenia. Schizophr. Bull. 39, 1096-1104. doi: 10.1093/schbul/sbs092
43. Rubenstein, J. L., and Merzenich, M. M. (2003). Model of autism: increased ratio of excitation/inhibition in key neural systems. Genes Brain Behav. 2, 255-267.
44. Ruffini, G., Wendling, F., Merlet, I., Molaee-Ardekani, B., Mekonnen, A., Salvador, R., et al. (2013). Transcranial current brain stimulation (tCS): models and technologies. IEEE Trans. Neural Syst. Rehabil. Eng. 21, 333-345. doi:10.1109/tnsre.2012.2200046
45. Shu, Y., Hasenstaub, A., and McCormick, D. A. (2003). Turning on and off recurrent balanced cortical activity. Nature 423, 288-293. doi: 10.1038/nature01616
46. Song, J. J., Vanneste, S., Van De Heyn-ing, P., and De Ridder, D. (2012). Transcranial direct current stimulation in tinnitus patients: a systemic review and meta-analysis. Scientific-WorldJournal 2012:427941. doi: 10. 1100/2012/427941
47. Stagg, C. J., Bachtiar, V., and Johansen-Berg, H. (2011). The role of GABA in human motor learning. Curr. Biol. 21, 480-484. doi:10.1016/j.cub.2011.01.069
48. Stagg, C. J., Best, J. G., Stephenson, M. C., O'shea, J., Wylezinska, M., Kincses, Z. T., et al. (2009). Polarity-sensitive modulation of cortical neurotransmitters by transcranial stimulation. J. Neurosci. 29, 5202-5206. doi: 10.1523/JNEUROSCI. 4432-08.2009
49. Turrigiano, G. G., and Nelson, S. B. (2000). Hebb and homeostasis in neuronal plasticity. Curr. Opin. Neurobiol. 10, 358-364. doi:10.1016/s0959-4388(00)00091-x
50. Vicario, C. M., and Nitsche, M. A. (2013). Transcranial direct current stimulation: a remediation tool for the treatment of childhood congenital dyslexia? Front. Hum. Neu-rosci. 7:139. doi:10.3389/fnhum. 2013.00139
51. Weiss, M., and Lavidor, M. (2012). When less is more: evidence for a facilitative cathodal tDCS effect in attentional abilities. J. Cogn. Neurosci. 24, 1826-1833. doi: 10. 1162/jocn_a_00248
52. Yizhar, O., Fenno, L. E., Prigge, M., Schneider, F., Davidson, T. J., O'shea, D. J., et al. (2011). Neocorti-cal excitation/inhibition balance in information processing and social dysfunction. Nature 477, 171-178. doi: 10.1038/nature10360
53. Yoon, J. H., Maddock, R. J., Rokem, A., Silver, M. A., Minzenberg, M. J., Ragland, J. D., et al. (2010). GABA concentration is reduced in visual cortex in schizophrenia and correlates with orientation-specific surround suppression. J. Neurosci. 30, 3777-3781. doi:10.1523/jneurosci. 6158-09.2010