The effects of noninvasive brain stimulation on heart rate and heart rate variability: a systematic review and meta-analysis
Open accessAbstract
Noninvasive brain stimulation (NIBS) techniques such as transcranial magnetic stimulation and transcranial direct current stimulation are widely used to test the involvement of specific cortical regions in various domains such as cognition and emotion. Despite the capability of stimulation techniques to test causal directions, this approach has been only sparsely used to examine the cortical regulation of autonomic nervous system (ANS) functions such as heart rate (HR) and heart rate variability (HRV) and to test current models in this regard. In this preregistered (PROSPERO) systematic review and meta-analysis, we aimed to investigate, based on meta-regression, whether NIBS represents an effective method for modulating HR and HRV measures, and to evaluate whether the ANS is modulated by cortical mechanisms affected by NIBS. Here we have adhered to the PRISMA guidelines. In a series of four meta-analyses, a total of 131 effect sizes from 35 sham-controlled trials were analyzed using robust variance estimation random-effects meta-regression technique. NIBS was found to effectively modulate HR and HRV with small to medium effect sizes. Moderator analyses yielded significant differences in effects between stimulation of distinct cortical areas. Our results show that NIBS is a promising tool to investigate the cortical regulation of ANS, which may add to the existing brain imaging and animal study literature. Future research is needed to identify further factors modulating the size of effects. As many of the studies reviewed were found to be at high risk of bias, we recommend that methods to reduce potential risk of bias be used in the design and conduct of future studies.
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Stimulating the vagus nerve non-invasively represents a valid target for health-related issues.
“By considering the importance of the parasympathetic nervous system for health-related issues, stimulating non-invasively the vagus nerve represents a valid target (Gerritsen & Band, 2018; Schmaußer, Hoffmann, Raab, & Laborde, 2022; Sevoz-Couche & Laborde, 2022; Vanderhasselt & Ottaviani, 2022)”
From Effects of voluntary slow breathing on heart rate and heart rate variability: A systematic review and a meta-analysis (2022) · cites this paper as Schmaußer, Hoffmann, Raab, & Laborde, 2022
Section 1.1 links vagal activity and heart-rate variability to cardiovascular health, and the Discussion and Conclusions report that noninvasive brain stimulation can modulate heart rate and heart-rate variability. But the interventions reviewed are TMS and tDCS targeting brain regions, not noninvasive stimulation of the vagus nerve itself. The paper therefore does not establish that vagus-nerve stimulation is a valid target for health-related issues. (LLM, conf=0.84)
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Cites
RoB 2: a revised tool for assessing risk of bias in randomised trials
Sterne, J. A. C., Savović, J., Page, M. J., Elbers, R. G., Blencowe, N. S., Boutron, I., Cates, C. J., Cheng, H.-Y., Corbett, M. S., Eldridge, S. M., et al. (2019) · BMJ · doi:10.1136/bmj.l4898 · Cited by 33,583 · see citing works
Lakens, D. (2013) · Frontiers in Psychology · doi:10.3389/fpsyg.2013.00863 · Cited by 10,303 · see citing works
An overview of heart rate variability metrics and norms
Shaffer, F., & Ginsberg, J. P. (2017) · Frontiers in Public Health · doi:10.3389/fpubh.2017.00258 · Cited by 7,185 · see citing works
Heart rate variability: origins, methods, and interpretive caveats
BERNTSON, G. G., THOMAS BIGGER, J., ECKBERG, D. L., GROSSMAN, P., KAUFMANN, P. G., MALIK, M., NAGARAJA, H. N., PORGES, S. W., SAUL, J. P., STONE, P. H., et al. (1997) · Psychophysiology · doi:10.1111/j.1469-8986.1997.tb02140.x · Cited by 3,962 · see citing works
Porges, S. W. (2007) · Biological Psychology · doi:10.1016/j.biopsycho.2006.06.009 · Cited by 3,415 · see citing works
A model of neurovisceral integration in emotion regulation and dysregulation
Thayer, J. F., & Lane, R. D. (2000) · Journal of Affective Disorders · doi:10.1016/s0165-0327(00)00338-4 · Cited by 3,092 · see citing works
Transcranial direct current stimulation: State of the art 2008
Nitsche, M. A., Cohen, L. G., Wassermann, E. M., Priori, A., Lang, N., Antal, A., Paulus, W., Hummel, F., Boggio, P. S., Fregni, F., et al. (2008) · Brain Stimulation · doi:10.1016/j.brs.2008.06.004 · Cited by 3,057 · see citing works
Outlier and influence diagnostics for meta-analysis
Viechtbauer, W., & Cheung, M. W.-L. (2010) · Research Synthesis Methods · doi:10.1002/jrsm.11 · Cited by 2,949 · see citing works
Laborde, S., Mosley, E., & Thayer, J. F. (2017) · Frontiers in Psychology · doi:10.3389/fpsyg.2017.00213 · Cited by 2,336 · see citing works
Self-citationThayer, J. F., Hansen, A. L., Saus-Rose, E., & Johnsen, B. H. (2009) · Annals of Behavioral Medicine · doi:10.1007/s12160-009-9101-z · Cited by 1,872 · see citing works
Methods to estimate the between‐study variance and its uncertainty in meta‐analysis
Veroniki, A. A., Jackson, D., Viechtbauer, W., Bender, R., Bowden, J., Knapp, G., Kuss, O., Higgins, J. P., Langan, D., & Salanti, G. (2016) · Research Synthesis Methods · doi:10.1002/jrsm.1164 · Cited by 1,685 · see citing works
The Central Autonomic Network: Functional Organization, Dysfunction, and Perspective
BENARROCH, E. E. (1993) · Mayo Clinic Proceedings · doi:10.1016/s0025-6196(12)62272-1 · Cited by 1,534 · see citing works
Heart rate variability: measurement and clinical utility.
Kleiger, R. E., Stein, P. K., & Bigger, J. T. (2005) · Annals of Noninvasive Electrocardiology · doi:10.1111/j.1542-474x.2005.10101.x · Cited by 1,290 · see citing works
Cardiovascular effects of human insular cortex stimulation
Oppenheimer, S. M., Gelb, A., Girvin, J. P., & Hachinski, V. C. (1992) · Neurology · doi:10.1212/wnl.42.9.1727 · Cited by 1,272 · see citing works
Human cingulate cortex and autonomic control: converging neuroimaging and clinical evidence
Critchley, H. D., Mathias, C. J., Josephs, O., O’Doherty, J., Zanini, S., Dewar, B., Cipolotti, L., Shallice, T., & Dolan, R. J. (2003) · Brain · doi:10.1093/brain/awg216 · Cited by 1,201 · see citing works
The role of vagal function in the risk for cardiovascular disease and mortality
Thayer, J. F., & Lane, R. D. (2007) · Biological Psychology · doi:10.1016/j.biopsycho.2005.11.013 · Cited by 1,033 · see citing works
Koenigs, M., & Grafman, J. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.03.004 · Cited by 956 · see citing works
Regression Methods to Detect Publication and Other Bias in Meta‐Analysis
Sterne, J. A. C., & Egger, M. (2005) · Publication Bias in Meta‐Analysis · doi:10.1002/0470870168.ch6 · Cited by 826 · see citing works
Meta-analysis with robust variance estimation: Expanding the range of working models
Pustejovsky, J. E., & Tipton, E. (2022) · Prevention Science · doi:10.1007/s11121-021-01246-3 · Cited by 737 · see citing works
A direct brainstem–amygdala–cortical ‘alarm’system for subliminal signals of fear.
Liddell, B. J., Brown, K. J., Kemp, A. H., Barton, M. J., Das, P., Peduto, A., Gordon, E., & Williams, L. M. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2004.08.016 · Cited by 670 · see citing works
Tanner-Smith, E. E., & Tipton, E. (2014) · Research Synthesis Methods · doi:10.1002/jrsm.1091 · Cited by 588 · see citing works
The hierarchical basis of neurovisceral integration
Smith, R., Thayer, J. F., Khalsa, S. S., & Lane, R. D. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.02.003 · Cited by 523 · see citing works
Rodgers, M. A., & Pustejovsky, J. E. (2021) · Psychological Methods · doi:10.1037/met0000300 · Cited by 492 · see citing works
How to formulate research recommendations
Brown, P., Brunnhuber, K., Chalkidou, K., Chalmers, I., Clarke, M., Fenton, M., Forbes, C., Glanville, J., Hicks, N. J., Moody, J., et al. (2006) · BMJ · doi:10.1136/bmj.38987.492014.94 · Cited by 381 · see citing works
Testing for funnel plot asymmetry of standardized mean differences
Pustejovsky, J. E., & Rodgers, M. A. (2019) · Research Synthesis Methods · doi:10.1002/jrsm.1332 · Cited by 354 · see citing works
Page, M. J., Higgins, J. P. T., Clayton, G., Sterne, J. A. C., Hróbjartsson, A., & Savović, J. (2016) · PLOS ONE · doi:10.1371/journal.pone.0159267 · Cited by 284 · see citing works
Iseger, T. A., van Bueren, N. E. R., Kenemans, J. L., Gevirtz, R., & Arns, M. (2020) · Brain Stimulation · doi:10.1016/j.brs.2019.10.006 · Cited by 142 · see citing works
Vagal Mediation of Low-Frequency Heart Rate Variability During Slow Yogic Breathing
Kromenacker, B. W., Sanova, A. A., Marcus, F. I., Allen, J. J. B., & Lane, R. D. (2018) · Psychosomatic Medicine · doi:10.1097/psy.0000000000000603 · Cited by 114 · see citing works
Boes, A. D., Uitermarkt, B. D., Albazron, F. M., Lan, M. J., Liston, C., Pascual-Leone, A., Dubin, M. J., & Fox, M. D. (2018) · Brain Stimulation · doi:10.1016/j.brs.2018.01.029 · Cited by 94 · see citing works
Beda, A., Simpson, D. M., Carvalho, N. C., & Carvalho, A. R. S. (2014) · Psychophysiology · doi:10.1111/psyp.12163 · Cited by 43 · see citing works
Flagged first, then by citations
Research works printed but not linked: 163
- S Agboada, D., Mosayebi Samani, M., Jamil, A., Kuo, M.-F., & Nitsche, M. A. (2019). Expanding the parameter space of anodal transcranial direct current stimulation of the primary motor cortex. Scientific Reports, 9(1), 18185. https://doi.org/10.1038/s4159 8-019-54621 -0 · DOI
- Angius, L., Marcora, S. M., Hopker, J. G., & Mauger, A. R. (2018). The effect of anodal transcranial direct current stimulation over left and right temporal cortex on the cardiovascular response: A comparative study. Frontiers in Physiology, 9, e01822. https://doi. org/10.3389/fphys.2018.01822 · DOI
- Angius, L., Pageaux, B., Hopker, J., Marcora, S. M., & Mauger, A. R. (2016). Transcranial direct current stimulation improves isometric time to exhaustion of the knee extensors. Neuroscience, 339, 363-375. https://doi.org/10.1016/j.neuro scien ce.2016.10.028 · DOI
- Angius, L., Santarnecchi, E., Pascual-Leone, A., & Marcora, S. M. (2019). Transcranial direct current stimulation over the left dorsolateral prefrontal cortex improves inhibitory control and endurance per- formance in healthy individuals. Neuroscience, 419, 34-45. https:// doi.org/10.1016/j.neuro scien ce.2019.08.052 · DOI
- Ansakorpi, H., Korpelainen, J. T., Tanskanen, P., Huikuri, H. V., Koivula, A., Tolonen, U., Pyhtinen, J., Myllylä, V. V., & Isojärvi, J. I. (2004). Cardiovascular regulation and hippocampal sclerosis. Epilepsia, 45(8), 933-939. https://doi.org/10.1111/j.0013-9580.2004.65003.x · DOI
- Baeken, C., van Beek, V., Vanderhasselt, M. A., Duprat, R., & Klooster, D. (2021). Cortical thickness in the right anterior cingulate cortex re- lates to clinical response to left prefrontal accelerated intermittent theta burst stimulation: An exploratory study. Neuromodulation, 24(5), 938-949. https://doi.org/10.1111/ner.13380 · DOI
- Baldari, C., Buzzachera, C. F., Vitor-Costa, M., Gabardo, J. M., Bernardes, A. G., Altimari, L. R., & Guidetti, L. (2018). Effects of transcranial direct current stimulation on psychophysiological responses to maximal incremental exercise test in recreational endurance run- ners. Frontiers in Psychology, 9, 1867. https://doi.org/10.3389/ fpsyg.2018.01867 · DOI
- Bär, K. J., Herbsleb, M., Schumann, A., de la Cruz, F., Gabriel, H. W., & Wagner, G. (2016). Hippocampal-brainstem connectivity associ- ated with vagal modulation after an intense exercise intervention in healthy men. Frontiers in Neuroscience, 10, 145. https://doi. org/10.3389/fnins.2016.00145 · DOI
- Barwood, M. J., Butterworth, J., Goodall, S., House, J. R., Laws, R., Nowicky, A., & Corbett, J. (2016). The effects of direct current stim- ulation on exercise performance, pacing and perception in temper- ate and hot environments. Brain Stimulation, 9(6), 842-849. https:// doi.org/10.1016/j.brs.2016.07.006 · DOI
- Begemann, M. J., Brand, B. A., Ćurčić-Blake, B., Aleman, A., & Sommer, I. E. (2020). Efficacy of non-invasive brain stimulation on cogni- tive functioning in brain disorders: A meta-analysis. Psychological Medicine, 50(15), 2465-2486. https://doi.org/10.1017/S0033 29172 0003670 · DOI · Paper page
- Beissner, F., Meissner, K., Bär, K. J., & Napadow, V. (2013). The autonomic brain: An activation likelihood estimation meta-analysis for central processing of autonomic function. Journal of Neuroscience, 33(25), 10503-10511. https://doi.org/10.1523/JNEUR OSCI.1103-13.2013 · DOI · Paper page
- Berger, C., Domes, G., Balschat, J., Thome, J., & Höppner, J. (2017). Effects of prefrontal rTMS on autonomic reactions to affective pictures. Journal of Neural Transmission, 124(Suppl. 1), 139-152. https://doi.org/10.1007/s0070 2-015-1491-4 · DOI
- Bergmann, T. O., Karabanov, A., Hartwigsen, G., Thielscher, A., & Siebner, H. R. (2016). Combining non-invasive transcranial brain stimulation with neuroimaging and electrophysiology: Current ap- proaches and future perspectives. Neuroimage, 140, 4-19. https:// doi.org/10.1016/j.neuro image.2016.02.012 · DOI
- Bestmann, S., Baudewig, J., Siebner, H. R., Rothwell, J. C., & Frahm, J. (2004). Functional MRI of the immediate impact of transcranial magnetic stimulation on cortical and subcortical motor circuits. European Journal of Neuroscience, 19(7), 1950-1962. https://doi. org/10.1111/j.1460-9568.2004.03277.x · DOI
- Beynel, L., Powers, J. P., & Appelbaum, L. G. (2020). Effects of repet- itive transcranial magnetic stimulation on resting-state connec- tivity: A systematic review. Neuroimage, 211, 116596. https://doi. org/10.1016/j.neuro image.2020.116596 · DOI
- Borenstein, M. (2009). Introduction to meta-analysis. Wiley. https://doi. org/10.1002/97804 70743386 · DOI · Paper page
- Brosschot, J. F., Verkuil, B., & Thayer, J. F. (2017). Exposed to events that never happen: Generalized unsafety, the default stress response, and prolonged autonomic activity. Neuroscience and Biobehavioral Reviews, 74(Pt B), 287-296. https://doi.org/10.1016/j.neubi orev.2016.07.019 · DOI · Paper page
- Brunoni, A. R., Kemp, A. H., Dantas, E. M., Goulart, A. C., Nunes, M. A., Boggio, P. S., Mill, J. G., Lotufo, P. A., Fregni, F., & Benseñor, I. M. (2013). Heart rate variability is a trait marker of major depressive disorder: Evidence from the sertraline vs electric current therapy to treat depression clinical study. International Journal of Neuropsychopharmacology, 16(9), 1937-1949. https://doi.org/10.1017/S1461 14571 3000497 · DOI
- Brunoni, A. R., Nitsche, M. A., Bolognini, N., Bikson, M., Wagner, T., Merabet, L., Edwards, D. J., Valero-Cabre, A., Rotenberg, A., Pascual-Leone, A., Ferrucci, R., Priori, A., Boggio, P., & Fregni, F. (2011). Clinical research with transcranial direct current stimulation (tDCS): Challenges and future directions. Brain Stimulation, 5(3), 175-195. https://doi.org/10.1016/j.brs.2011.03.002 · DOI · Paper page
- Brunoni, A. R., & Vanderhasselt, M. A. (2014). Working memory improvement with non-invasive brain stimulation of the dor- solateral prefrontal cortex: A systematic review and meta- analysis. Brain and Cognition, 86, 1-9. https://doi.org/10.1016/j. bandc.2014.01.008 · DOI · Paper page
- Brunoni, A. R., Vanderhasselt, M.-A., Boggio, P. S., Fregni, F., Dantas, E. M., Mill, J. G., Lotufo, P. A., & Benseñor, I. M. (2013). Polarity- and valence-dependent effects of prefrontal transcranial direct current stimulation on heart rate variability and salivary cortisol. Psychoneuroendocrinology, 38(1), 58-66. https://doi.org/10.1016/j. psyne uen.2012.04.020 · DOI
- Buchheit, M. (2014). Monitoring training status with HR measures: Do all roads lead to Rome? Frontiers in Physiology, 5, 73. https://doi. org/10.3389/fphys.201 · DOI
- Bulubas, L., Padberg, F., Bueno, P. V., Duran, F., Busatto, G., Amaro, E., Jr., Benseñor, I. M., Lotufo, P. A., Goerigk, S., Gattaz, W., Keeser, D., & Brunoni, A. R. (2019). Antidepressant effects of tDCS are as- sociated with prefrontal gray matter volumes at baseline: Evidence from the ELECT-TDCS trial. Brain Stimulation, 12(5), 1197-1204. https://doi.org/10.1016/j.brs.2019.05.006 · DOI
- Burnham, K. P., & Anderson, D. R. (2004). Model selection and inference. A practical information-theoretical approach (2nd ed.). Springer-Verlag.
- Cárdenas-Morales, L., Nowak, D. A., Kammer, T., Wolf, R. C., & Schönfeldt-Lecuona, C. (2010). Mechanisms and applications of theta-burst rTMS on the human motor cortex. Brain Topography, 22(4), 294-306. https://doi.org/10.1007/s1054 8-009-0084-7 · DOI · Paper page
- Carnevale, L., Maffei, A., Landolfi, A., Grillea, G., Carnevale, D., & Lembo, G. (2020). Brain functional magnetic resonance imaging high- lights altered connections and functional networks in patients with hypertension. Hypertension, 76(5), 1480-1490. https://doi. org/10.1161/HYPER TENSI ONAHA.120.15296 · DOI
- Carnevali, L., Pattini, E., Sgoifo, A., & Ottaviani, C. (2019). Effects of prefrontal transcranial direct current stimulation on auto- nomic and neuroendocrine responses to psychosocial stress in healthy humans. Stress. Advance Online Publication. https://doi. org/10.1080/10253 890.2019.1625884 · DOI
- Chang, C., Metzger, C. D., Glover, G. H., Duyn, J. H., Heinze, H. J., & Walter, M. (2013). Association between heart rate vari- ability and fluctuations in resting-state functional connectiv- ity. Neuroimage, 68, 93-104. https://doi.org/10.1016/j.neuro image.2012.11.038 · DOI
- Chew, T., Ho, K. A., & Loo, C. K. (2015). Inter-and intra-individual vari- ability in response to transcranial direct current stimulation (tDCS) at varying current intensities. Brain Stimulation, 8(6), 1130-1137. https://doi.org/10.1016/j.brs.2015.07.031 · DOI
- Chouchou, F., Mauguière, F., Vallayer, O., Catenoix, H., Isnard, J., Montavont, A., Jung, J., Pichot, V., Rheims, S., & Mazzola, L. (2019). How the insula speaks to the heart: Cardiac responses to insular stimulation in humans. Human Brain Mapping, 40(9), 2611-2622. https://doi.org/10.1002/hbm.24548 · DOI · Paper page
- Ciccone, A. B., Deckert, J. A., Schlabs, C. R., Tilden, M. J., Herda, T. J., Gallagher, P. M., & Weir, J. P. (2019). Transcranial direct current stimulation of the temporal lobe does not affect high-intensity work capacity. Journal of Strength and Conditioning Research, 33(8), 2074-2086. https://doi.org/10.1519/JSC.00000 00000 002561 · DOI
- Clancy, J. A., Johnson, R., Raw, R., Deuchars, S. A., & Deuchars, J. (2014). Anodal transcranial direct current stimulation (tDCS) over the motor cortex increases sympathetic nerve activity. Brain Stimulation, 7(1), 97-104. https://doi.org/10.1016/j.brs.2013.08.005 · DOI
- Conde, V., Vollmann, H., Sehm, B., Taubert, M., Villringer, A., & Ragert, P. (2012). Cortical thickness in primary sensorimotor cortex in- fluences the effectiveness of paired associative stimulation. Neuroimage, 60(2), 864-870. https://doi.org/10.1016/j.neuro image.2012.01.052 · DOI
- Corp, D. T., Bereznicki, H., Clark, G. M., Youssef, G. J., Fried, P. J., Jannati, A., Davies, C. B., Gomes-Osman, J., Stamm, J., Chung, S. W., Bowe, S. J., Rogasch, N. C., Fitzgerald, P. B., Koch, G., Di Lazzaro, V., Pascual- Leone, A., Enticott, P. G., & Big TMS Data Collaboration. (2020). Large-scale analysis of interindividual variability in theta-burst stimulation data: Results from the 'Big TMS Data Collaboration'. Brain Stimulation, 13(5), 1476-1488. https://doi.org/10.1016/j. brs.2020.07.018 · DOI
- Critchley, H. D., Eccles, J., & Garfinkel, S. N. (2013). Interaction between cognition, emotion, and the autonomic nervous system. Handbook of Clinical Neurology, 117, 59-77. https://doi.org/10.1016/B978-0- 444-53491 -0.00006 -7 · DOI · Paper page
- da Silva, F. T., Browne, R. A., Pinto, C. B., Saleh Velez, F. G., do Egito, E. S., do Rêgo, J. T., da Silva, M. R., Dantas, P. M., & Fregni, F. (2017). Transcranial direct current stimulation in individuals with spinal cord injury: Assessment of autonomic nervous system activity. Restorative Neurology and Neuroscience, 35(2), 159-169. https://doi. org/10.3233/RNN-160685 · DOI
- Datta, A., Bansal, V., Diaz, J., Patel, J., Reato, D., & Bikson, M. (2009). Gyri-precise head model of transcranial direct current stimulation: Improved spatial focality using a ring electrode versus conventional rectangular pad. Brain Stimulation, 2(4), 201-207.e1. https://doi. org/10.1016/j.brs.2009.03.005 · DOI
- Dayan, E., Censor, N., Buch, E. R., Sandrini, M., & Cohen, L. G. (2013). Noninvasive brain stimulation: From physiology to network dy- namics and back. Nature Neuroscience, 16(7), 3422. https://doi. org/10.1038/nn.3422 · DOI
- de Morree, H. M., Rutten, G. J., Szabó, B. M., Sitskoorn, M. M., & Kop, W. J. (2016). Effects of insula resection on autonomic nervous system activity. Journal of Neurosurgical Anesthesiology, 28(2), 153-158. https://doi.org/10.1097/ANA.00000 00000 000207 · DOI
- De Pisapia, N., Barchiesi, G., Jovicich, J., & Cattaneo, L. (2019). The role of medial prefrontal cortex in processing emotional self-referential in- formation: A combined TMS/fMRI study. Brain Imaging and Behavior, 13, 603-614. https://doi.org/10.1007/s1168 2-018-9867-3 · DOI
- De Putter, L. M. S., Vanderhasselt, M.-A., Baeken, C., de Raedt, R., & Koster, E. H. W. (2015). Combining tDCS and working memory training to down regulate state rumination: A single-session double blind sham-controlled trial. Cognitive Therapy and Research, 39(6), 754-765. https://doi.org/10.1007/s1060 8-015-9710-8 · DOI
- del Paso, G. A., Langewitz, W., Mulder, L. J., van Roon, A., & Duschek, S. (2013). The utility of low frequency heart rate variability as an index of sympathetic cardiac tone: A review with emphasis on a reanal- ysis of previous studies. Psychophysiology, 50(5), 477-487. https:// doi.org/10.1111/psyp.12027 · DOI · Paper page
- Deng, Z. D., Lisanby, S. H., & Peterchev, A. V. (2013). Electric field depth- focality tradeoff in transcranial magnetic stimulation: Simulation comparison of 50 coil designs. Brain Stimulation, 6(1), 1-13. https:// doi.org/10.1016/j.brs.2012.02.005 · DOI
- Dericioglu, N., Demirci, M., Cataltepe, O., Akalan, N., & Saygi, S. (2013). Heart rate variability remains reduced and sympathetic tone ele- vated after temporal lobe epilepsy surgery. Seizure, 22(9), 713-718. https://doi.org/10.1016/j.seizu re.2013.05.007 · DOI
- Di Lazzaro, V., Dileone, M., Pilato, F., Capone, F., Musumeci, G., Ranieri, F., Ricci, V., Bria, P., Di Iorio, R., de Waure, C., Pasqualetti, P., & Profice, P. (2011). Modulation of motor cortex neuronal networks by rTMS: Comparison of local and remote effects of six different protocols of stimulation. Journal of Neurophysiology, 105(5), 2150- 2156. https://doi.org/10.1152/jn.00781.2010 · DOI · Paper page
- Dissanayaka, T. D., Zoghi, M., Farrell, M., Egan, G. F., & Jaberzadeh, S. (2018). Sham transcranial electrical stimulation and its effects on corticospinal excitability: A systematic review and meta- analysis. Reviews in the Neurosciences, 29(2), 223-232. https://doi. org/10.1515/revne uro-2017-0026 · DOI
- Edwards, D., Cortes, M., Datta, A., Minhas, P., Wassermann, E. M., & Bikson, M. (2013). Physiological and modeling evidence for focal transcranial electrical brain stimulation in humans: A basis for high-definition tDCS. Neuroimage, 74, 266-275. https://doi. org/10.1016/j.neuro image.2013.01.042 · DOI
- Era, V., Carnevali, L., Thayer, J. F., Candidi, M., & Ottaviani, C. (2021). Dissociating cognitive, behavioral and physiological stress-related responses through dorsolateral prefrontal cortex inhibition. Psychoneuroendocrinology, 124, 105070. https://doi.org/10.1016/j. psyne uen.2020.105070 · DOI
- Erdogan, E. T., Saydam, S. S., Kurt, A., & Karamursel, S. (2018). Anodal transcranial direct current stimulation of the motor cortex in healthy volunteers. Neurophysiology, 50(2), 124-130. https://doi. org/10.1007/s1106 2-018-9726-2 · DOI
- Esser, S. K., Huber, R., Massimini, M., Peterson, M. J., Ferrarelli, F., & Tononi, G. (2006). A direct demonstration of cortical LTP in hu- mans: A combined TMS/EEG study. Brain Research Bulletin, 69(1), 3. https://doi.org/10.1016/j.brain resbu ll.2005.11.003 · DOI
- Filmer, H. L., Ehrhardt, S. E., Shaw, T. B., Mattingley, J. B., & Dux, P. E. (2019). The efficacy of transcranial direct current stimulation to prefrontal areas is related to underlying cortical morphol- ogy. NeuroImage, 196, 41-48. https://doi.org/10.1016/j.neuro image.2019.04.026 · DOI
- Foerster, Á. S., Rezaee, Z., Paulus, W., Nitsche, M. A., & Dutta, A. (2018). Effects of cathode location and the size of anode on an- odal transcranial direct current stimulation over the leg motor area in healthy humans. Frontiers in Neuroscience, 12, 443. https://doi. org/10.3389/fnins.2018.00443 · DOI
- Forte, G., Favieri, F., & Casagrande, M. (2019). Heart rate variability and cognitive function: A systematic review. Frontiers in Neuroscience, 13, e00710. https://doi.org/10.3389/fnins.2019.00710 · DOI · Paper page
- Germano-Soares, A. H., Montenegro, R. A., Cavalcante, B. R., Domingues, W. J. R., de Lima, P. F. M., Meneses, A. L., Almeida, T. R. M., Okano, A. H., & Ritti-Dias, R. M. (2017). Hemodynamic and autonomic re- sponses after a single session of resistance exercise following an- odal motor cortex tDCS. Isokinetics and Exercise Science, 25(2), 113- 120. https://doi.org/10.3233/IES-160653 · DOI
- Ghasemian-Shirvan, E., Farnad, L., Mosayebi-Samani, M., Verstraelen, S., Meesen, R. L. J., Kuo, M.-F., & Nitsche, M. A. (2020). Age-related differences of motor cortex plasticity in adults: A transcranial di- rect current stimulation study. Brain Stimulation, 13(6), 1588-1599. https://doi.org/10.1016/j.brs.2020.09.004 · DOI
- Gillie, B. L., & Thayer, J. F. (2014). Individual differences in resting heart rate variability and cognitive control in posttraumatic stress dis- order. Frontiers in Psychology, 5, 758. https://doi.org/10.3389/ fpsyg.2014.00758 · DOI
- Goldstein, D. S., Bentho, O., Park, M. Y., & Sharabi, Y. (2011). Low- frequency power of heart rate variability is not a measure of cardiac sympathetic tone but may be a measure of modulation of cardiac au- tonomic outflows by baroreflexes. Experimental Physiology, 96(12), 1255-1261. https://doi.org/10.1113/expph ysiol.2010.056259 · DOI · Paper page
- Goodwin, G. M., McCloskey, D. I., & Mitchell, J. H. (1972). Cardiovascular and respiratory responses to changes in central command during isometric exercise at constant muscle tension. Journal of Physiology, 226(1), 173-190. https://doi.org/10.1113/jphys iol.1972. · DOI
- sp009979 · DOI
- Grossman, P., & Taylor, E. W. (2007). Toward understanding respiratory sinus arrhythmia: Relations to cardiac vagal tone, evolution and biobehavioral functions. Biological Psychology, 74(2), 263-285. https://doi.org/10.1016/j.biops ycho.2005.11.014 · DOI · Paper page
- Hallam, G. P., Whitney, C., Hymers, M., Gouws, A. D., & Jefferies, E. (2016). Charting the effects of TMS with fMRI: Modulation of cortical recruitment within the distributed network supporting semantic control. Neuropsychologia, 93(Pt A), 40-52. https://doi. org/10.1016/j.neuro psych ologia.2016.09.012 · DOI
- Hamner, J. W., Villamar, M. F., Fregni, F., & Taylor, J. A. (2015). Transcranial direct current stimulation (tDCS) and the cardiovascular responses to acute pain in humans. Clinical Neurophysiology, 126(5), 1039- 1046. https://doi.org/10.1016/j.clinph.2014.08.019 · DOI
- Hassanzahraee, M., Nitsche, M. A., Zoghi, M., & Jaberzadeh, S. (2020). Determination of anodal tDCS duration threshold for reversal of corticospinal excitability: An investigation for induction of counter- regulatory mechanisms. Brain Stimulation, 13(3), 832-839. https:// doi.org/10.1016/j.brs.2020.02.027 · DOI
- Hedges, L. V., & Olkin, I. (2014). Statistical method for meta-analysis. Elsevier Science. http://gbv.eblib.com/patro n/FullR ecord.aspx?p=1901162
- Hedges, L. V., Tipton, E., & Johnson, M. C. (2010). Robust variance esti- mation in meta-regression with dependent effect size estimates. Research Synthesis Methods, 1(1), 39-65. https://doi.org/10.1002/ jrsm. · DOI · Paper page
- Heinz, G., de Angelis, K., Dal Corso, S., de Sousa, M. H. G., Viana, A., Dos Santos, F., Correa, J. C. F., & Correa, F. I. (2020). Effects of tran- scranial direct current stimulation (tDCS) and exercises treadmill on autonomic modulation of hemiparetic patients due to stroke-clinic test, controlled, randomized, double-blind. Frontiers in Neurology, 10, e01402. https://doi.org/10.3389/fneur.2019.01402 · DOI
- Herwig, U., Satrapi, P., & Schönfeldt-Lecuona, C. (2003). Using the in- ternational 10-20 EEG system for positioning of transcranial magnetic stimulation. Brain Topography, 16(2), 95-99. https://doi. org/10.1023/b:brat.00000 06333.93597. · DOI
- Hillebrand, S., Gast, K. B., de Mutsert, R., Swenne, C. A., Jukema, J. W., Middeldorp, S., Rosendaal, F. R., & Dekkers, O. M. (2013). Heart rate variability and first cardiovascular event in populations without known cardiovascular disease: Meta-analysis and dose- response meta-regression. Europace, 15(5), 742-749. https://doi. org/10.1093/europ ace/eus341 · DOI
- Hilz, M. J., Devinsky, O., Szczepanska, H., Borod, J. C., Marthol, H., & Tutaj, M. (2006). Right ventromedial prefrontal lesions result in paradoxical cardiovascular activation with emotional stimuli. Brain, 129(Pt 12), 3343-3355. https://doi.org/10.1093/brain/ awl299 · DOI
- Holgado, D., Zandonai, T., Ciria, L. F., Zabala, M., Hopker, J., & Sanabria, D. (2019). Transcranial direct current stimulation (tDCS) over the left prefrontal cortex does not affect time-trial self-paced cycling performance: Evidence from oscillatory brain activity and power output. PLoS ONE, 14(2), e0210873. https://doi.org/10.1371/journ al.pone.0210873 · DOI
- Holmes, N. P., & Tamè, L. (2019). Locating primary somatosensory cortex in human brain stimulation studies: Systematic review and meta- analytic evidence. Journal of Neurophysiology, 121(1), 152-162. https://doi.org/10.1152/jn.00614.2018 · DOI
- Hoogendam, J. M., Ramakers, G. M. J., & Di Lazzaro, V. (2010). Physiology of repetitive transcranial magnetic stimulation of the human brain. Brain Stimulation, 3(2), 95-118. https://doi.org/10.1016/j. brs.2009.10.005 · DOI · Paper page
- Huber, T. J., Schneider, U., & Rollnik, J. (2003). Gender differences in the effect of repetitive transcranial magnetic stimulation in schizophre- nia. Psychiatry Research, 120(1), 103-105. https://doi.org/10.1016/ S0165 -1781(03)00170 -7 · DOI
- Hugdahl, K. (1996). Cognitive influences on human autonomic nervous system function. Current Opinion in Neurobiology, 6(2), 252-258. https://doi.org/10.1016/s0959 -4388(96)80080 -8 · DOI
- Iezzi, E., Suppa, A., Conte, A., Li Voti, P., Bologna, M., & Berardelli, A. (2011). Short-term and long-term plasticity interaction in human primary motor cortex. European Journal of Neuroscience, 33(10), 1908-1915. https://doi.org/10.1111/j.1460-9568.2011.07674.x · DOI
- Iseger, T. A., Arns, M., Downar, J., Blumberger, D. M., Daskalakis, Z. J., & Vila-Rodriguez, F. (2020). Cardiovascular differences be- tween sham and active iTBS related to treatment response in MDD. Brain Stimulation, 13(1), 167-174. https://doi.org/10.1016/j. brs.2019.09.016 · DOI
- Jackson, D., Riley, R., & White, I. R. (2011). Multivariate meta-analysis: Potential and promise. Statistics in Medicine, 30(20), 2481-2498. https://doi.org/10.1002/sim.4172 · DOI · Paper page
- Jandackova, V. K., Scholes, S., Britton, A., & Steptoe, A. (2016). Are changes in heart rate variability in middle-aged and older people normative or caused by pathological conditions? Findings from a large population-based longitudinal cohort study. Journal of the American Heart Association, 5(2), e002365. https://doi.org/10.1161/ JAHA.115.002365 · DOI
- Jänig, W. (2006). The integrative action of the autonomic nervous system: Neurobiology of homeostasis. Cambridge University Press.
- Kao, Y.-C., Tzeng, N.-S., Chao, C.-Y., Chang, C.-C., & Chang, H.-A. (2020). Modulation of self-appraisal of illness, medication adherence, life quality and autonomic functioning by transcranial direct current stimulation in schizophrenia patients. Clinical Neurophysiology, 131(8), 1997-2007. https://doi.org/10.1016/j.clinph.2020.02.029 · DOI
- Kemp, A. H., & Quintana, D. S. (2013). The relationship between mental and physical health: Insights from the study of heart rate variability. International Journal of Psychophysiology, 89(3), 288-296. https:// doi.org/10.1016/j.ijpsy cho.2013.06.018 · DOI · Paper page
- Klomjai, W., Katz, R., & Lackmy-Vallée, A. (2015). Basic principles of transcranial magnetic stimulation (TMS) and repetitive TMS (rTMS). Annals of Physical and Rehabilitation Medicine, 58(4), 208-213. https://doi.org/10.1016/j.rehab.2015.05.005 · DOI
- Koenig, J., Abler, B., Agartz, I., Åkerstedt, T., Andreassen, O. A., Anthony, M., Bär, K. J., Bertsch, K., Brown, R. C., Brunner, R., Carnevali, L., Critchley, H. D., Cullen, K. R., de Geus, E., de la Cruz, F., Dziobek, I., Ferger, M. D., Fischer, H., Flor, H., … Quintana, D. S. (2021). Cortical thickness and resting-state cardiac function across the lifespan: A cross-sectional pooled mega-analysis. Psychophysiology, 58(7), e13688. https://doi.org/10.1111/psyp.13688 · DOI
- Koenig, J., & Thayer, J. F. (2016). Sex differences in healthy human heart rate variability: A meta-analysis. Neuroscience and Biobehavioral Reviews, 64, 288-310. https://doi.org/10.1016/j.neubi orev.2016.03.007 · DOI · Paper page
- Kreuzer, P. M., Schecklmann, M., Lehner, A., Wetter, T. C., Poeppl, T. B., Rupprecht, R., de Ridder, D., Landgrebe, M., & Langguth, B. (2015). The ACDC pilot trial: Targeting the anterior cingulate by double cone coil rTMS for the treatment of depression. Brain Stimulation, 8(2), 240-246. https://doi.org/10.1016/j.brs.2014.11.014 · DOI
- Kuo, H. I., Bikson, M., Datta, A., Minhas, P., Paulus, W., Kuo, M. F., & Nitsche, M. A. (2013). Comparing cortical plasticity induced by con- ventional and high-definition 4 × 1 ring tDCS: A neurophysiological study. Brain Stimulation, 6(4), 644-648. https://doi.org/10.1016/j. brs.2012.09.010 · DOI
- Laborde, S., Mosley, E., & Mertgen, A. (2018). Vagal tank theory: The three rs of cardiac vagal control functioning-Resting, reactiv- ity, and recovery. Frontiers in Neuroscience, 12, 458. https://doi. org/10.3389/fnins.2018.00458 · DOI
- Lee, Y.-S., Bae, S.-H., & Kim, K.-Y. (2019). Effects of repetitive transcra- nial magnetic stimulation on psychological aspects of patients with chronic lower back pain. Journal of Magnetics, 24(3), 543-548. https://doi.org/10.4283/JMAG.2019.24.3.543 · DOI
- Levasseur-Moreau, J., Brunelin, J., & Fecteau, S. (2013). Non-invasive brain stimulation can induce paradoxical facilitation. Are these neu- roenhancements transferable and meaningful to security services? Frontiers in Human Neuroscience, 7, 449. https://doi.org/10.3389/ fnhum.2013.00449 · DOI
- Levinthal, D. J., & Strick, P. L. (2012). The motor cortex communicates with the kidney. Journal of Neuroscience, 32(19), 6726-6731. https://doi.org/10.1523/JNEUR OSCI.0406-12.2012 · DOI · Paper page
- Li, L. M., Uehara, K., & Hanakawa, T. (2015). The contribution of interin- dividual factors to variability of response in transcranial direct cur- rent stimulation studies. Frontiers in Cellular Neuroscience, 9, 181. https://doi.org/10.3389/fncel.2015.00181 · DOI · Paper page
- López-Alonso, V., Fernández-Del-Olmo, M., Costantini, A., Gonzalez- Henriquez, J. J., & Cheeran, B. (2015). Intra-individual variabil- ity in the response to anodal transcranial direct current stimula- tion. Clinical Neurophysiology, 126(12), 2342-2347. https://doi. org/10.1016/j.clinph.2015.03.022 · DOI
- Lu, M., & Ueno, S. (2017). Comparison of the induced fields using dif- ferent coil configurations during deep transcranial magnetic stim- ulation. PLoS ONE, 12(6), e0178422. https://doi.org/10.1371/journ al.pone.0178422 · DOI
- Maeda, F., Keenan, J. P., Tormos, J. M., Topka, H., & Pascual-Leone, A. (2000a). Modulation of corticospinal excitability by repetitive tran- scranial magnetic stimulation. Clinical Neurophysiology, 111(5), 800- 805. https://doi.org/10.1016/s1388 -2457(99)00323 -5 · DOI
- Maeda, F., Keenan, J. P., Tormos, J. M., Topka, H., & Pascual-Leone, A. (2000b). Interindividual variability of the modulatory effects of repetitive transcranial magnetic stimulation on cortical excitabil- ity. Experimental Brain Research, 133(4), 425-430. https://doi. org/10.1007/s0022 10000432 · DOI · Paper page
- Makovac, E., Thayer, J. F., & Ottaviani, C. (2017). A meta-analysis of non- invasive brain stimulation and autonomic functioning: Implications for brain-heart pathways to cardiovascular disease. Neuroscience and Biobehavioral Reviews, 74(Pt B). https://doi.org/10.1016/j.neubi orev.2016.05.001 · DOI · Paper page
- Malik, M., Bigger, J. T., Camm, A. J., Kleiger, R. E., Malliani, A., Moss, A. J., & Schwartz, P. J. (1996). Heart rate variability: Standards of measurement, physiological interpretation, and clinical use. European Heart Journal, 17(3), 354-381. https://doi.org/10.1093/ oxfor djour nals.eurhe artj.a014868 · DOI · Paper page
- Marins, F. R., Limborço-Filho, M., Xavier, C. H., Biancardi, V. C., Vaz, G. C., Stern, J. E., Oppenheimer, S. M., & Fontes, M. A. (2016). Functional topography of cardiovascular regulation along the rostrocaudal axis of the rat posterior insular cortex. Clinical and Experimental Pharmacology & Physiology, 43(4), 484-493. https:// doi.org/10.1111/1440-1681.12542 · DOI
- Masuki, S., & Nose, H. (2009). Increased cerebral activity suppresses baroreflex control of heart rate in freely moving mice. Journal of Physiology, 587(Pt 23), 5783-5794. https://doi.org/10.1113/jphys iol.2009.176164 · DOI
- Mather, M., Joo Yoo, H., Clewett, D. V., Lee, T. H., Greening, S. G., Ponzio, A., Min, J., & Thayer, J. F. (2017). Higher locus coeruleus MRI contrast is associated with lower parasympathetic influence over heart rate variability. Neuroimage, 150, 329-335. https://doi. org/10.1016/j.neuro image.2017.02.025 · DOI
- Matsumoto, H., & Ugawa, Y. (2016). Adverse events of tDCS and tACS: A review. Clinical neurophysiology practice, 2, 19-25. https://doi. org/10.1016/j.cnp.2016.12.003 · DOI
- Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & PRISMA Group. (2010). Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. International Journal of Surgery, 8(5), 336-341. https://doi.org/10.1016/j. ijsu.2010.02.007 · DOI · Paper page
- Morrissey, M. B. (2016). Rejoinder: Further considerations for meta- analysis of transformed quantities such as absolute values. Journal of Evolutionary Biology, 29, 1922-1931. https://doi.org/10.1111/ jeb.12951 · DOI
- Mulcahy, J. S., Larsson, D., Garfinkel, S. N., & Critchley, H. D. (2019). Heart rate variability as a biomarker in health and affective dis- orders: A perspective on neuroimaging studies. Neuroimage, 202, 116072. https://doi.org/10.1016/j.neuro image.2019.116072 · DOI
- Nagai, M., Hoshide, S., & Kario, K. (2010). The insular cortex and car- diovascular system: A new insight into the brain-heart axis. Journal of the American Society of Hypertension, 4(4), 174-182. https://doi. org/10.1016/j.jash.2010.05.001 · DOI · Paper page
- Napadow, V., Dhond, R., Conti, G., Makris, N., Brown, E. N., & Barbieri, R. (2008). Brain correlates of autonomic modulation: Combining heart rate variability with fMRI. Neuroimage, 42(1), 169-177. https://doi. org/10.1016/j.neuro image.2008.04.238 · DOI
- Naumczyk, P., Sabisz, A., Witkowska, M., Graff, B., Jodzio, K., Gąsecki, D., Szurowska, E., & Narkiewicz, K. (2017). Compensatory functional reorganization may precede hypertension-related brain damage and cognitive decline: A functional magnetic resonance imag- ing study. Journal of Hypertension, 35(6), 1252-1262. https://doi. org/10.1097/HJH.00000 00000 001293 · DOI
- Nguyen, V. T., Breakspear, M., Hu, X., & Guo, C. C. (2016). The integra- tion of the internal and external milieu in the insula during dynamic emotional experiences. Neuroimage, 124(Pt A), 455-463. https:// doi.org/10.1016/j.neuro image.2015.08.078 · DOI
- Nikolin, S., Boonstra, T. W., Loo, C. K., & Martin, D. (2017). Combined effect of prefrontal transcranial direct current stimulation and a working memory task on heart rate variability. PLoS ONE, 12(8), e0181833. https://doi.org/10.1371/journ al.pone.0181833 · DOI
- Nonnekes, J., Arrogi, A., Munneke, M. A., van Asseldonk, E. H., Oude Nijhuis, L. B., Geurts, A. C., & Weerdesteyn, V. (2014). Subcortical structures in humans can be facilitated by transcranial direct cur- rent stimulation. PLoS ONE, 9(9), e107731. https://doi.org/10.1371/ journ al.pone.0107731 · DOI
- Notzon, S., Deppermann, S., Fallgatter, A., Diemer, J., Kroczek, A., Domschke, K., Zwanzger, P., & Ehlis, A.-C. (2015). Psychophysiological effects of an iTBS modulated virtual reality challenge including participants with spider phobia. Biological Psychology, 112, 66-76. https://doi.org/10.1016/j.biops ycho.2015.10.003 · DOI
- Ottaviani, C., Mancini, F., Provenzano, S., Collazzoni, A., & D'Olimpio, F. (2018). Deontological morality can be experimentally enhanced by increasing disgust: A transcranial direct current stimulation study. Neuropsychologia, 119, 474-481. https://doi.org/10.1016/j.neuro psych ologia.2018.09.009 · DOI
- Ozdemir, R. A., Tadayon, E., Boucher, P., Momi, D., Karakhanyan, K. A., Fox, M. D., Halko, M. A., Pascual-Leone, A., Shafi, M. M., & Santarnecchi, E. (2020). Individualized perturbation of the human connectome reveals reproducible biomarkers of network dynam- ics relevant to cognition. Proceedings of the National Academy of Sciences of the United States of America, 117(14), 8115-8125. https://doi.org/10.1073/pnas.19112 40117 · DOI
- Park, S.-B., Sung, D. J., Kim, B., Kim, S., & Han, J.-K. (2019). Transcranial direct current stimulation of motor cortex enhances running per- formance. PLoS ONE, 14(2), e0211902. https://doi.org/10.1371/ journ al.pone.0211902 · DOI
- Pascual-Leone, A., Walsh, V., & Rothwell, J. (2000). Transcranial magnetic stimulation in cognitive neuroscience-Virtual lesion, chronometry, and functional connectivity. Current Opinion in Neurobiology, 10(2), 232-237. https://doi.org/10.1016/s0959 -4388(00)00081 -7 · DOI · Paper page
- Penttilä, J., Helminen, A., Jartti, T., Kuusela, T., Huikuri, H. V., Tulppo, M. P., Coffeng, R., & Scheinin, H. (2001). Time domain, geometri- cal and frequency domain analysis of cardiac vagal outflow: Effects of various respiratory patterns. Clinical Physiology, 21(3), 365-376. https://doi.org/10.1046/j.1365-2281.2001.00337.x · DOI · Paper page
- Perna, G., Riva, A., Defillo, A., Sangiorgio, E., Nobile, M., & Caldirola, D. (2020). Heart rate variability: Can it serve as a marker of mental health resilience? Special Section on "Translational and Neuroscience Studies in Affective Disorders" Section Editor, Maria Nobile MD, PhD. Journal of Affective Disorders, 263, 754-761. https://doi.org/10.1016/j.jad.2019.10.017 · DOI
- Petrocchi, N., Piccirillo, G., Di Fiorucci, C., Moscucci, F., Di Iorio, C., Mastropietri, F., Parrotta, I., Pascucci, M., Magrì, D., & Ottaviani, C. (2017). Transcranial direct current stimulation enhances sooth- ing positive affect and vagal tone. Neuropsychologia, 96, 256-261. https://doi.org/10.1016/j.neuro psych ologia.2017.01.028 · DOI
- Piccirillo, G., Ottaviani, C., Fiorucci, C., Petrocchi, N., Moscucci, F., Di Iorio, C., Mastropietri, F., Parrotta, I., Pascucci, M., & Magrì, D. (2016). Transcranial direct current stimulation improves the QT variability index and autonomic cardiac control in healthy subjects older than 60 years. Clinical Interventions in Aging, 11, 1687-1695. https://doi.org/10.2147/CIA.S116194 · DOI
- Pigott, T. D., & Polanin, J. R. (2020). Methodological guidance paper: High-quality meta-analysis in a systematic review. Review of Educational Research, 90(1), 24-46. https://doi.org/10.3102/00346 54319 877153 · DOI · Paper page
- Poppa, T., de Witte, S., Vanderhasselt, M.-A., Bechara, A., & Baeken, C. (2020). Theta-burst stimulation and frontotemporal regulation of cardiovascular autonomic outputs: The role of state anxiety. International Journal of Psychophysiology, 149, 25-34. https://doi. org/10.1016/j.ijpsy cho.2019.12.011 · DOI
- Priori, A., Hallett, M., & Rothwell, J. C. (2009). Repetitive transcra- nial magnetic stimulation or transcranial direct current stimula- tion? Brain Stimulation, 2(4), 241-245. https://doi.org/10.1016/j. brs.2009.02.004 · DOI · Paper page
- Pulopulos, M. M., Schmausser, M., de Smet, S., Vanderhasselt, M.-A., Baliyan, S., Venero, C., Baeken, C., & de Raedt, R. (2020). The effect of HF-rTMS over the left DLPFC on stress regulation as measured by cortisol and heart rate variability. Hormones and Behavior, 124, 104803. https://doi.org/10.1016/j.yhbeh.2020.104803 · DOI
- Raimondo, R. J. S., Uribe, C. E., & Brasil-Neto, J. P. (2012). Lack of clin- ically detectable acute changes on autonomic or thermoregula- tory functions in healthy subjects after transcranial direct current stimulation (tDCS). Brain Stimulation, 5(3), 196-200. https://doi. org/10.1016/j.brs.2011.03.009 · DOI
- Raven, P. B., Fadel, P. J., & Smith, S. A. (2002). The influence of central command on baroreflex resetting during exercise. Exercise and Sport Sciences Reviews, 30(1), 39-44. https://doi.org/10.1097/00003 677-20020 1000-00008 · DOI
- Reisert, M., Weiller, C., & Hosp, J. A. (2021). Displaying the auto- nomic processing network in humans-A global tractography ap- proach. Neuroimage, 231, 117852. https://doi.org/10.1016/j.neuro image.2021.117852 · DOI
- Remue, J., Vanderhasselt, M.-A., Baeken, C., Rossi, V., Tullo, J., & de Raedt, R. (2016). The effect of a single HF-rTMS session over the left DLPFC on the physiological stress response as measured by heart rate variability. Neuropsychology, 30(6), 756-766. https://doi. org/10.1037/neu00 00255 · DOI
- Rich, T. L., & Gillick, B. T. (2019). Electrode placement in transcranial di- rect current stimulation-how reliable is the determination of C3/ C4? Brain Sciences, 9(3), 69. https://doi.org/10.3390/brain sci90 30069 · DOI
- Riley, R. D. (2009). Multivariate meta-analysis: The effect of ignoring within-study correlation. Journal of the Royal Statistical Society: Series A (Statistics in Society), 172(4), 789-811. https://doi. org/10.1111/j.1467-985X.2008.00593.x · DOI
- Riley, R. D., Jackson, D., Salanti, G., Burke, D. L., Price, M., Kirkham, J., & White, I. R. (2017). Multivariate and network meta-analysis of multiple outcomes and multiple treatments: Rationale, concepts, and examples. BMJ, 358, j3932. https://doi.org/10.1136/bmj.j3932 · DOI
- Ruit, K. G., & Neafsey, E. J. (1988). Cardiovascular and respiratory re- sponses to electrical and chemical stimulation of the hippocampus in anesthetized and awake rats. Brain Research, 457(2), 310-321. https://doi.org/10.1016/0006-8993(88)90701 -9 · DOI
- Sanchez-Larsen, A., Principe, A., Ley, M., Navarro-Cuartero, J., & Rocamora, R. (2021). Characterization of the insular role in car- diac function through intracranial electrical stimulation of the human insula. Annals of Neurology, 89(6), 1172-1180. https://doi. org/10.1002/ana.26074 · DOI
- Sauvaget, A., Bulteau, S., Guilleux, A., Leboucher, J., Pichot, A., Valrivière, P., Vanelle, J.-M., Sébille-Rivain, V., & Grall-Bronnec, M. (2018). Both active and sham low-frequency rTMS single sessions over the right DLPFC decrease cue-induced cravings among pathological gamblers seeking treatment: A randomized, double-blind, sham- controlled crossover trial. Journal of Behavioral Addictions, 7(1), 126-136. https://doi.org/10.1556/2006.7.2018. · DOI
- Schecklmann, M., Schmaußer, M., Klinger, F., Kreuzer, P. M., Krenkel, L., & Langguth, B. (2020). Resting motor threshold and magnetic field output of the figure-of-8 and the double-cone coil. Scientific re- ports, 10(1), 1644. https://doi.org/10.1038/s4159 8-020-58034 -2 · DOI
- Schestatsky, P., Simis, M., Freeman, R., Pascual-Leone, A., & Fregni, F. (2013). Non-invasive brain stimulation and the autonomic nervous system. Clinical Neurophysiology, 124(9), 1716-1728. https://doi. org/10.1016/j.clinph.2013.03.020 · DOI
- Schilberg, L., Schuhmann, T., & Sack, A. T. (2017). Interindividual vari- ability and intraindividual reliability of intermittent theta burst stimulation-induced neuroplasticity mechanisms in the healthy brain. Journal of Cognitive Neuroscience, 29(6), 1022-1032. https:// doi.org/10.1162/jocn_a_01100 · DOI
- Sclocco, R., Beissner, F., Desbordes, G., Polimeni, J. R., Wald, L. L., Kettner, N. W., Kim, J., Garcia, R. G., Renvall, V., Bianchi, A. M., Cerutti, S., Napadow, V., & Barbieri, R. (2016). Neuroimaging brainstem cir- cuitry supporting cardiovagal response to pain: A combined heart rate variability/ultrahigh-field (7T) functional magnetic resonance imaging study. Philosophical Transactions: Series A, Mathematical, Physical, and Engineering Sciences, 374(2067), 20150189. https:// doi.org/10.1098/rsta.2015.0189 · DOI
- Sclocco, R., Kim, J., Garcia, R. G., Sheehan, J. D., Beissner, F., Bianchi, A. M., Cerutti, S., Kuo, B., Barbieri, R., & Napadow, V. (2016). Brain circuitry supporting multi-organ autonomic outflow in response to nausea. Cerebral Cortex, 26(2), 485-497. https://doi.org/10.1093/ cerco r/bhu172 · DOI
- Seibt, O., Brunoni, A. R., Huang, Y., & Bikson, M. (2015). The pursuit of DLPFC: Non-neuronavigated methods to target the left dorsolat- eral pre-frontal cortex with symmetric bicephalic transcranial di- rect current stimulation (tDCS). Brain Stimulation, 8(3), 590-602. https://doi.org/10.1016/j.brs.2015.01.401 · DOI
- Siebner, H. R., Hartwigsen, G., Kassuba, T., & Rothwell, J. C. (2009). How does transcranial magnetic stimulation modify neuronal activity in the brain? Implications for studies of cognition. Cortex, 45(9), 1035- 1042. https://doi.org/10.1016/j.cortex.2009.02.007 · DOI
- Silber, D. H., Sinoway, L. I., Leuenberger, U. A., & Amassian, V. E. (2000). Magnetic stimulation of the human motor cortex evokes skin sym- pathetic nerve activity. Journal of Applied Physiology, 88(1), 126- 134. https://doi.org/10.1152/jappl.2000.88.1.126 · DOI
- Silva, D. S., Coan, A. C., & Avelar, W. M. (2019). Neuropsychological and neuroimaging evidences of cerebral dysfunction in stroke-free pa- tients with atrial fibrillation: A review. Journal of the Neurological Sciences, 399, 172-181. https://doi.org/10.1016/j.jns.2019.02.027 · DOI
- Silva, L. M., Silva, K., Lira-Bandeira, W. G., Costa-Ribeiro, A. C., & Araújo- Neto, S. A. (2021). Localizing the primary motor cortex of the hand by the 10-5 and 10-20 systems for neurostimulation: An MRI study. Clinical EEG and Neuroscience, 52(6), 427-435. https://doi. org/10.1177/15500 59420 934590 · DOI
- Silvani, A., Calandra-Buonaura, G., Dampney, R. A., & Cortelli, P. (2016). Brain-heart interactions: Physiology and clinical implica- tions. Philosophical Transactions: Series A, Mathematical, Physical, and Engineering Sciences, 374(2067), 20150181. https://doi. org/10.1098/rsta.2015.0181 · DOI
- Sklerov, M., Dayan, E., & Browner, N. (2019). Functional neuroimaging of the central autonomic network: Recent developments and clinical implications. Clinical Autonomic Research, 29(6), 555-566. https:// doi.org/10.1007/s1028 6-018-0577-0 · DOI
- Smith, S. A., Mitchell, J. H., & Garry, M. G. (2006). The mammalian exer- cise pressor reflex in health and disease. Experimental Physiology, 91(1), 89-102. https://doi.org/10.1113/expph ysiol.2005.032367 · DOI
- Steinfurth, E., Wendt, J., Geisler, F., Hamm, A. O., Thayer, J. F., & Koenig, J. (2018). Resting state vagally-mediated heart rate variability is associated with neural activity during explicit emotion regula- tion. Frontiers in Neuroscience, 12, 794. https://doi.org/10.3389/ fnins.2018.00794 · DOI
- ch6 · DOI · Paper page
- Thair, H., Holloway, A. L., Newport, R., & Smith, A. D. (2017). Transcranial direct current stimulation (tDCS): A beginner's guide for design and implementation. Frontiers in Neuroscience, 11, 641. https://doi. org/10.3389/fnins.2017.00641 · DOI
- Thayer, J. F., Ahs, F., Fredrikson, M., Sollers, J. J. 3rd, & Wager, T. D. (2012). A meta-analysis of heart rate variability and neuroimaging studies: implications for heart rate variability as a marker of stress and health. Neuroscience and biobehavioral reviews, 36(2), 747-756. https://doi.org/10.1016/j.neubi orev.2011.11.009 · DOI · Paper page
- Thayer, J. F., & Lane, R. D. (2009). Claude Bernard and the heart-brain connection: Further elaboration of a model of neurovisceral in- tegration. Neuroscience and Biobehavioral Reviews, 33(2), 81-88. https://doi.org/10.1016/j.neubi orev.2008.08.004 · DOI · Paper page
- Thayer, J. F., Sollers, J. J., 3rd, Labiner, D. M., Weinand, M., Herring, A. M., Lane, R. D., & Ahern, G. L. (2009). Age-related differences in pre- frontal control of heart rate in humans: A pharmacological block- ade study. International Journal of Psychophysiology, 72(1), 81-88. https://doi.org/10.1016/j.ijpsy cho.2008.04.007 · DOI
- Thomas, F., Pixa, N. H., Berger, A., Cheng, M. Y., Doppelmayr, M., & Steinberg, F. (2020). Neither cathodal nor anodal transcranial direct current stimulation on the left dorsolateral prefrontal cortex alone or applied during moderate aerobic exercise modulates executive function. Neuroscience, 443, 71-83. https://doi.org/10.1016/j. neuro scien ce.2020.07.017 · DOI
- Trapp, N. T., Bruss, J., King Johnson, M., Uitermarkt, B. D., Garrett, L., Heinzerling, A., Wu, C., Koscik, T. R., Ten Eyck, P., & Boes, A. D. (2020). Reliability of targeting methods in TMS for depression: Beam F3 vs. 5.5 cm. Brain Stimulation, 13(3), 578-581. https://doi. org/10.1016/j.brs.2020.01.010 · DOI
- Valenza, G., Sclocco, R., Duggento, A., Passamonti, L., Napadow, V., Barbieri, R., & Toschi, N. (2019). The central autonomic network at rest: Uncovering functional MRI correlates of time-varying autonomic outflow. Neuroimage, 197, 383-390. https://doi. org/10.1016/j.neuro image.2019.04.075 · DOI
- Valenzuela, P. L., Amo, C., Sanchez-Martinez, G., Torrontegi, E., Vazquez-Carrion, J., Montalvo, Z., Lucia, A., & de La Villa, P. (2019). Enhancement of mood but not performance in elite athletes with transcranial direct-current stimulation. International Journal of Sports Physiology and Performance, 14(3), 310-316. https://doi. org/10.1123/ijspp.2018-0473 · DOI
- van den Eynde, F., Claudino, A. M., Campbell, I., Horrell, L., Andiappan, M., Stahl, D., & Schmidt, U. (2011). Cardiac safety of repeti- tive transcranial magnetic stimulation in bulimic eating disor- ders. Brain Stimulation, 4(2), 112-114. https://doi.org/10.1016/j. brs.2010.06.003 · DOI
- Viechtbauer, W. (2010). Conducting meta-analyses in R with the meta- for package. Journal of Statistical Software, 36(3), 1-48. https://doi. org/10.18637/ jss.v036.i03 · DOI · Paper page
- Walsh, V. (1998). Brain mapping: Faradization of the mind. Current Biology, 8(1), R8-R11. https://doi.org/10.1016/S0960 -9822(98)70098 -3 · DOI
- Weller, S., Nitsche, M. A., & Plewnia, C. (2020). Enhancing cognitive control training with transcranial direct current stimulation: A systematic parameter study. Brain Stimulation, 13(5), 1358-1369. https://doi.org/10.1016/j.brs.2020.07.006 · DOI
- Williamson, J. W., Fadel, P. J., & Mitchell, J. H. (2006). New insights into central cardiovascular control during exercise in humans: A central command update. Experimental Physiology, 91(1), 51-58. https://doi. org/10.1113/expph ysiol.2005.032037 · DOI
- Woods, A. J., Antal, A., Bikson, M., Boggio, P. S., Brunoni, A. R., Celnik, P., Cohen, L. G., Fregni, F., Herrmann, C. S., Kappenman, E. S., Knotkova, H., Liebetanz, D., Miniussi, C., Miranda, P. C., Paulus, W., Priori, A., Reato, D., Stagg, C., Wenderoth, N., & Nitsche, M. A. (2016). A technical guide to tDCS, and related non-invasive brain stimulation tools. Clinical Neurophysiology, 127(2), 1031-1048. https://doi.org/10.1016/j.clinph.2015.11.012 · DOI
- Yasui, Y., Breder, C. D., Saper, C. B., & Cechetto, D. F. (1991). Autonomic responses and efferent pathways from the insular cortex in the rat. Journal of Comparative Neurology, 303(3), 355-374. https://doi. org/10.1002/cne.90303 0303 · DOI
Cited by
Sorted by citations
Laborde, S., Allen, M. S., Borges, U., Dosseville, F., Hosang, T. J., Iskra, M., Mosley, E., Salvotti, C., Spolverato, L., Zammit, N., et al. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104711 · Cited by 272 · see citing works
Self-citationLee, H., Lee, J. H., Hwang, M.-H., & Kang, N. (2023) · Journal of Affective Disorders · doi:10.1016/j.jad.2023.07.039 · Cited by 25 · see citing works
- Authors
- Schmaußer, M., Hoffmann, S., Raab, M., & Laborde, S.
- Affiliations
- German Sport University Cologne (DE)
- FernUniversität in Hagen (DE)
- Corresponding author
- Schmaußer, Maximilian
- Venue
- Journal of Neuroscience Research
- Publisher
- Wiley
- Published
- 2022-05-17
- Volume
- 100
- Issue
- 9
- Pages
- 1664-1694
- ISSN
- 0360-4012 (ISSN-L)
- 1097-4547
- OpenAlex
- W4280625488
- Cited by
- 59
- References
- 30
- Citations by year
- 2026: 11 · 2025: 15 · 2024: 14 · 2023: 14 · 2022: 5
- FWCI
- 2.44
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience Research (publishedVersion, other-oa)
- PubMed (publishedVersion)
- Research Open (London South Bank University) (acceptedVersion, cc-by)
- OSF Preprints (OSF Preprints) (submittedVersion)
- Topics
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Heart Rate Variability and Autonomic Control
- Life Sciences › Neuroscience › Neurology › Transcranial Magnetic Stimulation Studies
- Life Sciences › Neuroscience › Neurology › Vagus Nerve Stimulation Research
- Keywords
- non-invasive brain stimulation, transcranial magnetic stimulation, transcranial direct current stimulation, heart rate, heart rate variability, autonomic nervous system, risk of bias
- MeSH terms
- Animals, Brain, Cognition, Heart Rate, Transcranial Magnetic Stimulation, Transcranial Direct Current Stimulation
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