Does Prefrontal Cortex Transcranial Direct Current Stimulation Influence the Oxygen Uptake at Rest and Post-exercise?

R. Montenegro; A. H. Okano; F. A. Cunha; E. B. Fontes; P. Farinatti

doi:10.1055/s-0033-1333769

International Journal of Sports Medicine, Table of Contents

Int J Sports Med 2014; 35(06): 459-464
DOI: 10.1055/s-0033-1333769

Physiology & Biochemistry

Does Prefrontal Cortex Transcranial Direct Current Stimulation Influence the Oxygen Uptake at Rest and Post-exercise?

R. Montenegro

¹Physical Activity and Health Promotion Laboratory (LABSAU), Institute of Physical Education and Sports, Rio de Janeiro State University, Rio de Janeiro, Brazil

,

A. H. Okano

²Departament of Sport Science, University of Campinas, Londrina, Brazil

,

F. A. Cunha

³Physical Activity Sciences Graduate Program, Salgado de Oliveira University, Rio de Janeiro, Brazil

,

E. B. Fontes

⁴SPORTS SCIENCE, University of CAMPINAS – UNICAMP, CAMPINAS, Brazil

,

P. Farinatti

⁵School of Physical Education, Rio de Janeiro State University, Rio de Janeiro, Brazil

› Author Affiliations

Abstract

The study evaluated the effect of transcranial direct current stimulation (tDCS) applied over prefrontal cortex on the oxygen uptake (V˙ O₂) at rest and during post-exercise recovery. The V˙ O₂ was assessed in eleven healthy subjects before, during tDCS (sham or anodal tDCS, 2 mA, 20 min), and 30-min following isocaloric aerobic exercise (~200 kcal). During tDCS, no changes were observed on V˙ O₂ compared to baseline (P=0.95) and sham condition (P=0.85). The association between isocaloric exercise and anodal tDCS increased the V˙ O₂ throughout 30-min recovery compared to sham condition (P<0.001). Therefore, the energy expenditure within the excess post-exercise oxygen consumption (EPOC) period, after anodal tDCS was approximately 19% higher compared to the sham condition (P<0.05). In conclusion, anodal tDCS applied on the prefrontal cortex combined with submaximal aerobic exercise increased the EPOC, enhancing the V˙ O₂ and energy expenditure at least for 30-min of recovery.

Key words

energy expenditure - metabolism - isocaloric exercise - EPOC - central nervous system - health

Full Text

References

References
1 Alonzo A, Brassil J, Taylor JL, Martin D, Loo CK. Daily transcranial direct current stimulation (tDCS) leads to greater increases in cortical excitability than second daily transcranial direct current stimulation. Brain Stimul. 2012 5. 208-213
2 Bikson M, Datta A, Rahman A, Scaturro J. Electrode montages for tDCS and weak transcranial electrical stimulation: role of “return” electrode’s position and size. Clin Neurophysiol 2010; 121: 1976-1978
3 Binkofski F, Loebig M, Jauch-Chara K, Bergmann S, Melchert UH, Scholand-Engler HG, Schweiger U, Pellerin L, Oltmanns KM. Brain energy consumption induced by electrical stimulation promotes systemic glucose uptake. Biol Psychiat 2011; 70: 690-695
4 Boggio PS, Bermpohl F, Vergara AO, Muniz AL, Nahas FH, Leme PB, Rigonatti SP, Fregni F. Go-no-go task performance improvement after anodal transcranial DC stimulation of the left dorsolateral prefrontal cortex in major depression. J Affect Disord 2007; 101: 91-98
5 Boggio PS, Sultani N, Fecteau S, Merabet L, Mecca T, Pascual-Leone A, Basaglia A, Fregni F. Prefrontal cortex modulation using transcranial DC stimulation reduces alcohol craving: a double-blind, sham-controlled study. Drug Alcohol Depend 2008; 92: 55-60
6 Boggio PS, Khoury LP, Martins DC, Martins OE, de Macedo EC, Fregni F. Temporal cortex direct current stimulation enhances performance on a visual recognition memory task in Alzheimer disease. J Neurol Neurosurg Psychiat 2009; 80: 444-447
7 Buchfuhrer MJ, Hansen JE, Robinson TE, Sue DY, Wasserman K, Whipp BJ. Optimizing the exercise protocol for cardiopulmonary assessment. J Appl Physiol 1983; 55: 1558-1564
8 Cogiamanian F, Marceglia S, Ardolino G, Barbieri S, Priori A. Improved isometric force endurance after transcranial direct current stimulation over the human motor cortical areas. Eur J Neurosci 2007; 26: 242-249
9 Dundas JE, Thickbroom GW, Mastaglia FL. Perception of comfort during transcranial DC stimulation: effect of NaCl solution concentration applied to sponge electrodes. Clin Neurophysiol 2007; 118: 1166-1170
10 Ekkekakis P. Illuminating the black box: investigating prefrontal cortical hemodynamics during exercise with near-infrared spectroscopy. J Sport Exerc Psychol 2009; 31: 505-553
11 Fink GR, Adams L, Watson JD, Innes JA, Wuyam B, Kobayashi I, Corfield DR, Murphy K, Jones T, Frackowiak RS. Hyperpnoea during and immediately after exercise in man: evidence of motor cortical involvement. J Physiol 1995; 489 Pt 3 663-675
12 Gandiga PC, Hummel FC, Cohen LG. Transcranial DC stimulation (tDCS): a tool for double-blind sham-controlled clinical studies in brain stimulation. Clin Neurophysiol 2006; 117: 845-850
13 Garber CE, Blissmer B, Deschenes MR, Franklin BA, Lamonte MJ, Lee IM, Nieman DC, Swain DP. American College of Sports Medicine position stand. Quantity and quality of exercise for developing and maintaining cardiorespiratory, musculoskeletal, and neuromotor fitness in apparently healthy adults: guidance for prescribing exercise. Med Sci Sports Exerc 2011; 43: 1334-1359
14 Harriss DJ, Atkinson G. Update – ethical standards in sport and exercise science research. Int J Sports Med 2011; 32: 819-821
15 Howley ET, Bassett Jr DR, Welch HG. Criteria for maximal oxygen uptake: review and commentary. Med Sci Sports Exerc 1995; 27: 1292-1301
16 Ide K, Horn A, Secher NH. Cerebral metabolic response to submaximal exercise. J Appl Physiol 1999; 87: 1604-1608
17 Klem GH, Luders HO, Jasper HH, Elger C. The ten-twenty electrode system of the International Federation. The International Federation of Clinical Neurophysiology. Electroencephalogr Clin Neurophysiol Suppl 1999; 52: 3-6
18 LaForgia J, Withers RT, Gore CJ. Effects of exercise intensity and duration on the excess post-exercise oxygen consumption. J Sports Sci 2006; 24: 1247-1264
19 Lang N, Siebner HR, Ward NS, Lee L, Nitsche MA, Paulus W, Rothwell JC, Lemon RN, Frackowiak RS. How does transcranial DC stimulation of the primary motor cortex alter regional neuronal activity in the human brain?. Eur J Neurosci 2005; 22: 495-504
20 Lippold OC, Redfearn JW. Mental Changes Resulting from the Passage of Small Direct Currents through the Human Brain. Br J Psychiat 1964; 110: 768-772
21 Merzagora AC, Foffani G, Panyavin I, Mordillo-Mateos L, Aguilar J, Onaral B, Oliviero A. Prefrontal hemodynamic changes produced by anodal direct current stimulation. Neuroimage 2010; 49: 2304-2310
22 Miller EK, Freedman DJ, Wallis JD. The prefrontal cortex: categories, concepts and cognition. Philos Trans R Soc Lond B Biol Sci 2002; 357: 1123-1136
23 Montenegro RA, Farinatti Pde T, Fontes EB, Soares PP, Cunha FA, Gurgel JL, Porto F, Cyrino ES, Okano AH. Transcranial direct current stimulation influences the cardiac autonomic nervous control. Neurosci Lett 2011; 497: 32-36
24 Montenegro RA, Okano AH, Cunha FA, Gurgel JL, Fontes EB, Farinatti PT. Prefrontal cortex transcranial direct current stimulation associated with aerobic exercise change aspects of appetite sensation in overweight adults. Appetite 2012; 58: 333-338
25 Nitsche MA, Paulus W. Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol 2000; 527 (Pt 3) 633-639
26 Nitsche MA, Nitsche MS, Klein CC, Tergau F, Rothwell JC, Paulus W. Level of action of cathodal DC polarisation induced inhibition of the human motor cortex. Clin Neurophysiol 2003; 114: 600-604
27 Nitsche MA, Niehaus L, Hoffmann KT, Hengst S, Liebetanz D, Paulus W, Meyer BU. MRI study of human brain exposed to weak direct current stimulation of the frontal cortex. Clin Neurophysiol 2004; 115: 2419-2423
28 Pelchat ML, Johnson A, Chan R, Valdez J, Ragland JD. Images of desire: food-craving activation during fMRI. Neuroimage 2004; 23: 1486-1493
29 Raimundo RJ, Uribe CE, Brasil-Neto JP. Lack of clinically detectable acute changes on autonomic or thermoregulatory functions in healthy subjects after transcranial direct current stimulation (tDCS). Brain Stimul 2012; 5: 196-200
30 Redfearn JW, Lippold OC, Costain R. A Preliminary Account of the Clinical Effects of Polarizing the Brain in Certain Psychiatric Disorders. Br J Psychiat 1964; 110: 773-785
31 Rigonatti SP, Boggio PS, Myczkowski ML, Otta E, Fiquer JT, Ribeiro RB, Nitsche MA, Pascual-Leone A, Fregni F. Transcranial direct stimulation and fluoxetine for the treatment of depression. Eur Psychiat 2008; 23: 74-76
32 Robbins TW, Arnsten AF. The neuropsychopharmacology of fronto-executive function: monoaminergic modulation. Annu Rev Neurosci 2009; 32: 267-287
33 Rupp T, Perrey S. Prefrontal cortex oxygenation and neuromuscular responses to exhaustive exercise. Eur J Appl Physiol 2008; 102: 153-163
34 Suzuki M, Miyai I, Ono T, Oda I, Konishi I, Kochiyama T, Kubota K. Prefrontal and premotor cortices are involved in adapting walking and running speed on the treadmill: an optical imaging study. Neuroimage 2004; 23: 1020-1026
35 Swain DP. Energy cost calculations for exercise prescription: an update. Sports Med 2000; 30: 17-22
36 Tanaka S, Hanakawa T, Honda M, Watanabe K. Enhancement of pinch force in the lower leg by anodal transcranial direct current stimulation. Exp Brain Res 2009; 196: 459-465
37 Tanaka S, Takeda K, Otaka Y, Kita K, Osu R, Honda M, Sadato N, Hanakawa T, Watanabe K. Single session of transcranial direct current stimulation transiently increases knee extensor force in patients with hemiparetic stroke. Neurorehabil Neural Repair 2011; 25: 565-569
38 Timinkul A, Kato M, Omori T, Deocaris CC, Ito A, Kizuka T, Sakairi Y, Nishijima T, Asada T, Soya H. Enhancing effect of cerebral blood volume by mild exercise in healthy young men: a near-infrared spectroscopy study. Neurosci Res 2008; 61: 242-248
39 Uher R, Murphy T, Brammer MJ, Dalgleish T, Phillips ML, Ng VW, Andrew CM, Williams SC, Campbell IC, Treasure J. Medial prefrontal cortex activity associated with symptom provocation in eating disorders. Am J Psychiat 2004; 161: 1238-1246
40 Uher R, Yoganathan D, Mogg A, Eranti SV, Treasure J, Campbell IC, McLoughlin DM, Schmidt U. Effect of left prefrontal repetitive transcranial magnetic stimulation on food craving. Biol Psychiat 2005; 58: 840-842
41 Vandermeeren Y, Jamart J, Ossemann M. Effect of tDCS with an extracephalic reference electrode on cardio-respiratory and autonomic functions. BMC Neurosci 2010; 11: 38
42 Vernieri F, Assenza G, Maggio P, Tibuzzi F, Zappasodi F, Altamura C, Corbetto M, Trotta L, Palazzo P, Ercolani M, Tecchio F, Rossini PM. Cortical neuromodulation modifies cerebral vasomotor reactivity. Stroke 2010; 41: 2087-2090
43 Zheng X, Alsop DC, Schlaug G. Effects of transcranial direct current stimulation (tDCS) on human regional cerebral blood flow. Neuroimage 2011; 58: 26-33