High frequency heart rate variability evoked by repetitive transcranial magnetic stimulation over the medial prefrontal cortex: A preliminary investigation on brain processing of acute stressor-evoked cardiovascular reactivity

Abstract

Introduction: Transcranial Magnetic Stimulation (TMS) is a non-invasive technique for brain stimulation. Repetitive TMS (rTMS) over the medial Prefrontal Cortex (mPFC), Broadman Area 10 (BA10) may stimulate transynaptically perigenual Anterior Cingulate Cortex (pACC, BA 33), insula, amigdala, hypothalamus and connected branches of the Autonomic Nervous System (ANS) involved in stressorevoked cardiovascular reactivity. Stressors are associated with an increase in sympathetic cardiac control, a decrease in parasympathetic control, or both, and, consequently, an increase in systolic/stroke volume, total vascular impedance/resistance and heart rate, a decrease of baroreflex sensitivity, i.e., an increase in blood pressure/arterial tension. Objectives and Aims: The present work aims, using TMS and accordingly to Gianaros modeling, based on functional neuroimaging studies and previous neuroanatomical data from animal models, to probe the connectivity of brain systems involved in stressor-evoked cardiovascular reactivity and to explore TMS potential as a tool for detection and stratification of individual differences concerning this reactivity and hemorreological risk factors correlated with the development of Coronary Heart Disease (CHD). Methods: Both subjects, a 52 years old male and a 40 years old female with previous increased Low Frequency (LF)/High Frequency (HF) Heart Rate Variability (HRV) ratios (respectively, 4.209/3.028) without decompensated cardiorespiratory symptoms, gave informed consent, and ethico-legal issues have been observed. Electroencephalographic (EEG) monitoring has been performed for safety purposes. Immediately after administration, over the mPFC, of 15 pulses of rTMS, during 60 second, with an inductive electrical current, at the stimulating coil, of 85.9 Ampère per μsecond and 66 Ampère per μsecond, respectively, for male and female subjects (a “figure-of-eight” coil and magnetic stimulator MagLite, Dantec/Medtronic, have been used), HRV spectrum analysis (cStress software) has been performed (during 5 minutes, in supine position). Results: In both subjects, LF power, HF power and LF/HF ratio results, before and after rTMS administration, pointed towards sympathetic attenuation and parasympathetic augmentation (respectively, in male/female subject: decreased LF power—65.1 nu/69.3 nu, before rTMS; 56.1 nu/41.6 nu, after rTMS; increased HF power—15.5 nu/22.9 nu, before rTMS; 30.9 nu/45.5 nu, after rTMS). Conclusions: In this preliminary investigation, the existence of a link between “mind” and heart’s function has been put in evidence, through a reversible “virtual” lesion, of brain systems involved in cardiovascular control, caused by TMS. Repetitive TMS over mPFC decreased brain function involved in stressorevoked cardiovascular reactivity, suggesting the importance of TMS in the management of stress-related cardiovascular disorders.

Share and Cite:

Gonçalves, E. and Jesus, S. (2013) High frequency heart rate variability evoked by repetitive transcranial magnetic stimulation over the medial prefrontal cortex: A preliminary investigation on brain processing of acute stressor-evoked cardiovascular reactivity. Open Journal of Psychiatry, 3, 335-344. doi: 10.4236/ojpsych.2013.34035.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] Barbas, H., Saha, S., Rempel-Clower, N. and Ghashghaei, T. (2003) Serial pathways from primate prefrontal cortex to autonomic areas may influence emotional expression. BMC Neuroscience, 4, 25. http://dx.doi.org/10.1186/1471-2202-4-25
[2] Critchley, H.D. (2005) Neural mechanisms of autonomic, affective, and cognitive integration. Journal of Comparative Neurology, 493, 154-166. http://dx.doi.org/10.1002/cne.20749
[3] Vogt, B.A. and Laureys, S. (2005) Posterior cingulate, precuneal and retrosplenial cortices: Cytology and components of the neural network correlates of consciousness. Progress in Brain Research, 150, 205-217. http://dx.doi.org/10.1016/S0079-6123(05)50015-3
[4] Vogt, B.A. and Pandya, D.N. (1987) Cingulate cortex of the rhesus monkey: II cortical afferents. Journal of Comparative Neurology, 262, 271-289. http://dx.doi.org/10.1002/cne.902620208
[5] Lane, R.D., Reiman, E.M., Axelrod, B., Yun, L.S., Holmes, A. and Schwartz, G.E. (1998) Neural correlates of levels of emotional awareness. Evidence of an interaction between emotion and attention in the anterior cingulate cortex. Journal of Cognitive Neuroscience, 10, 525-535. http://dx.doi.org/10.1162/089892998562924
[6] Ochsner, K.N. and Cross, J.J. (2005) The cognitive controI of emotion. Trends in Cognitive Sciences, 9, 242-249. http://dx.doi.org/10.1016/j.tics.2005.03.010
[7] Critchley, H.D., Melmed, R.N., Featherstone, E., Mathias, C.J. and Dolan, R.J. (2002) Volitional control of autonomic arousal: A functetional magnetic resonance study. NeuroImage, 16, 909-919. http://dx.doi.org/10.1006/nimg.2002.1147
[8] Gianaros, P.J., Derbyshire, S.W., May, J.C., Siegle, G.J., Gamalo, M.A. and Jennings, J.R. (2005) Anterior cingulate activity correlates with blood pressure during stress. Psychophysiology, 42, 627-635. http://dx.doi.org/10.1111/j.1469-8986.2005.00366.x
[9] Augustine, J.R. (1996) Circuitry and functional aspects of the insular lobe in primates including humans. Brain Research Reviews, 22, 229-244. http://dx.doi.org/10.1016/S0165-0173(96)00011-2
[10] Verberne, A.J. and Owens, N.C. (1998) Cortical modulation of the cardiovascular system. Progress in Neurobiology, 54, 149-168. http://dx.doi.org/10.1016/S0301-0082(97)00056-7
[11] Craig, A.D. (2003) Interoception: The sense of the physiological condition of the body. Current Opinion in Neurobiology, 13, 500-505. http://dx.doi.org/10.1016/S0959-4388(03)00090-4
[12] Critchley, H.D., Corfield, D.R., Chandler, M.P., Mathias, C.J. and Dolan, R.J. (2000) Cerebral correlates of autonomic cardiovascular arousal: A functional neuroimaging investigation in humans. Journal of Physiology, 523, 259-270. http://dx.doi.org/10.1111/j.1469-7793.2000.t01-1-00259.x
[13] Gianaros, P.J. (2008) Brain-bodv pathways to cardiovascular disease risk. Herbert Weiner Early Career Award Lecture, 66th Annual Meeting of the American Psychosomatic Society, Baltimore.
[14] Gianaros, P.J., Horenstein, J.A., Cohen, S., Matthews, K.A., Brown, S.M., Flory, J.D., et al. (2007) Perigenual anterior cingulate morphology covaries with perceived social standing. Social Cognitive and Affective Neuroscience, 2, 161-173. http://dx.doi.org/10.1093/scan/nsm013
[15] Gianaros, P.J., Horenstein, J.A., Hariri, A.K., Sheu, L.K., Manuck, S.B., Matthews, K.A., et al. (2008) Potential neural embedding of parental social standing. Social Cognitive and Affective Neuroscience, 3, 91-96. http://dx.doi.org/10.1093/scan/nsn003
[16] Gianaros, P.J., Jennings, J.K., Sheu, L.K., Derbyshire, S.W. and Matthews, K.A. (2007) Heightened functional neural activation to psychological stress covaries with exaggerated blood pressure reactivity. Hypertension, 49, 134-140. http://dx.doi.org/10.1161/01.HYP.0000250984.14992.64
[17] Gianaros, P.J., Jennings, J.K., Sheu, L.K., Greer, P.J., Kuller, L.H. and Matthews, K.A. (2007) Prospective reports of chronic life stress predict decreased grey matter volume in the hippocampus. NeuroImage, 35, 795-803. http://dx.doi.org/10.1016/j.neuroimage.2006.10.045
[18] Gianaros, P.J., Sheu, L.K., Matthews, K.A., Jennings, J.K., Manuck, S.B. and Hariri, A.R. (2008) Individual differences in stressor-evoked blood pressure reactivity vary with activation, volume, and functional connectivity of the amygdala. Journal of Neuroscience, 28, 990-999. http://dx. doi.org/10.1523/JNEUROSCI.3606-07.2008
[19] Gianaros, P.J., Van der Veen, F.M. and Jennings, J.K. (2004) Regional cerebral blood flow correlates with heart period and highfrequency heart period variability during working-memory tasks: Implications for the cortical and subcortical regulation of cardiac autonomic activity. Psychophysiology, 41, 521-530. http://dx.doi.org/10.1111/1469-8986. 2004.00179.x
[20] Davis, M. and Whalen, P.J. (2001) The amygdala: Vigilance and emotion. Molecular Psychiatry, 6, 13-34. http://dx.doi.org/10.1038/sj.mp.4000812
[21] LeDoux, J. (2003) The emotional brain, fear, and the amygdala. Cellular and Molecular Neurobiology, 23, 727-738. http://dx.doi.org/10.1023/A:1025048802629
[22] Sah, P., Faber, E.S., Lopez De Armentia, M. and Power, J. (2003) The amygdaloid complex: Anatomy and physiology. Physiological Reviews, 83, 803-834.
[23] Zald, D.H. (2003) The human amygdala and the emotional evaluation of sensory stimuli. Brain research. Brain Research Reviews, 41, 88-123. http://dx.doi.org/10.1016/S0165-0173(02)00248-5
[24] Amaral, D.G. and Price, J.L. (1984) Amygdalo-cortícal projections in the monkey (Macaca fascicularis). Journal of Comparative Neurology, 230, 465-496. http://dx.doi.org/10.1002/cne.902300402
[25] McDonald, A.J. (1998) CorticaI pathways to the mammahan amygdala. Progress in Neurobiology, 55, 257-332. http://dx.doi.org/10.1016/S0301-0082(98)00003-3
[26] Price, J.L. (2003) Comparative aspects of amygdala connectivity. Annals of the New York Academy of Sciences, 985, 50-58. http://dx.doi.org/10.1111/j.1749-6632.2003.tb07070.x
[27] Berntson, G.G., Sarter, M. and Cacioppo, J.T. (1998) Anxiety and cardiovascular reactivity: The basal forebrain cholinergic link. Behavioural Brain Research, 94, 225-248. http://dx.doi.org/10.1016/S0166-4328(98)00041-2
[28] Dampney, R.A. (1994) Functional organization of central pathways regulating the cardiovascular system. Physiological Reviews, 74, 323-364.
[29] Saha, S. (2005) Role of the central nucleus of the amygdala in the control of blood pressure: Descending pathways to medullary cardiovascular nuclei. Clinical and Experimental Pharmacology and Physiology, 32, 450-456. http://dx.doi.org/10.1111/j.1440-1681.2005.04210.x
[30] Saper, C.B. (2002) The central autonomic nervous system: Conscious visceral perception and autonomic pattern generation. Annual Review of Neuroscience, 25, 433-469. http://dx. doi.org/10.1146/annurev.neuro.25.032502.111311
[31] O’Connor, M.F., GündeI, H., McRae, K. and Lane, R.O. (2007) Baseline vagal tone predicts BOLD response during elicitation of grief. Neuropsychopharmacology, 32, 2184-2189. http://dx. doi.org/10.1038/sj.npp.1301342
[32] Lane, R.D., Reiman, E.M., Ahern, G.L. and Thayer, J.F. (2001) Activity in the medial prefrontal cortex correlates with vagal component of heart rate variability. Brain and Cognition, 47, 97-100.
[33] Barker, A.T., Jalinous, R. and Freeston, I.L. (1985) Noninvasive magnetic stimulation of human motor cortex. Lancet, 1, 1106-1107. http://dx.doi.org/10.1016/S0140-6736(85)92413-4
[34] Wilson, S.A., Thickbroom, G.W. and Mastaglia, F.L. (1993) Transcranial magnetic stimulation mapping of the motor cortex in normal subjects. Journal of the Neurological Sciences, 118, 134-144. http://dx.doi.org/10.1016/0022-510X(93)90102-5
[35] Wassermann, E.M., McShane, L.M., Hallett, M. and Cohen, L.G. (1992) Noninvasive mapping of muscle representations in human motor cortex. Electroencephalography and Clinical Neurophysiology, 85, 1-8. http://dx.doi.org/10.1016/0168-5597(92)90094-R
[36] Rossini, P.M. and Rossi, S. (1998) Clinical applications of motor evoked potentials. Electroencephalography and Clinical Neurophysiology, 106, 180-194. http:// dx. doi.org/10. 1016/S0013-4694(97)00097-7
[37] Classen, J., Liepert, J., Wise, S.P., Hallett, M. and Cohen, L.G. (1998) Rapid plasticity of human cortical movement representation induced by practice. Journal of Neurophysiology, 79, 1117-1123.
[38] Pascual-Leone, A., Walsh, V. and Rothwell, J.C. (2000) Transcranial magnetic stimulation in cognitive neuroscience-virtual lesion, chronometry, and functional connectivity. Current Opinion in Neurobiology, 10, 232-237. http://dx.doi.org/10.1016/S0959-4388(00)00081-7
[39] Siebner, H.R. and Rothwell, J.C. (2002) Transcranial magnetic stimulation: New insights into representational cortical plasticity. Experimental Brain Research, 148, 1-16. http://dx.doi. org/10.1007/s00221-002-1234-2
[40] Wassermann, E.M. (1998) Risk and safety of repetitive transcranial magnetic stimulation: Report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation. Electroencephalography and Clinical Neurophysiology, 108, 1-16. http://dx.doi.org/10.1016/S0168-5597(97)00096-8
[41] Lemon, R. (2002) Basic physiology of transcranial magnetic stimulaiton. In: Pascual-Leone, A., Davey, N.J., Rothwell, J., Wasserman, E.M. and Puri, B.K., Eds., Handbook of Transcranial Magnetic Stimulation. Arnold, London, 61-77.
[42] Feinsod, M., Kreinin, B., Chistyakov, A. and Klein, E. (1998) Preliminary evidence for a beneficial effect of low-frequency, repetitive transcranial magnetic stimulation in patients with major depression and schizophrenia. Depression and Anxiety, 7, 65-68. http://dx.doi.org/10.1002/(SICI)1520-6394(1998)7:2<65::AID-DA2>3.0.CO;2-4
[43] Di Lazzaro, V., Oliviero, A., Mazzone, P., et al. (2002) Short-term reduction of intracortical inhibition in the human motor cortex induced by repetitive transcranial magnetic stimulation. Experimental Brain Research, 147, 108-113. http://dx.doi.org/10.1007/s00221-002-1223-5
[44] Rossini, P.M., Barker, A.T., Berardelli, A., et al. (1994) Noninvasive electrical and magnetic stimulation of the brain, spinal cord and roots: Basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalography and Clinical Neurophysiology, 91, 79-92. http://dx.doi.org/10.1016/0013-4694(94)90029-9
[45] Wassermann, E.M. (2002) Variation in the response to transcranial magnetic brain stimulation in the general population. Clinical Neurophysiology, 113, 1165-1171. http://dx.doi.org/10.1016/S1388-2457(02)00144-X
[46] Muellbacher, W., Ziemann, U., Boroojerdi, B. and Hallett, M. (2000) Effects of low-frequency transcranial magnetic stimulation on motor cortex excitability and basic motor behavior. Clinical Neurophysiology, 111, 1002-1007. http://dx.doi.org/10.1016/S1388-2457(00)00284-4
[47] Chen, R., Classen, J., Gerloff, C., et al. (1997) Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology, 48, 1398-1403. http://dx. doi. org/10.1212/WNL.48.5.1398
[48] Berardelli, A., Inghilleri, M., Rothwell, J.C., et al. (1998) Facilitation of muscle evoked responses after repetitive cortical stimulation in man. Experimental Brain Research, 122, 79-84. http://dx.doi.org/10.1007/s002210050493
[49] Pascual-Leone, A., Valls-Sole, J., Wassermann, E.M. and Hallet, M. (1998) Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain, 117, 847-858. http://dx.doi.org/10.1093/brain/117.4.847
[50] Peinemann, A., Reimer, B., Loer, C., et al. (2004) Long-lasting increase in corticospinal excitability after 1800 pulses of subthreshold 5 Hz repetitive TMS to the primary motor cortex. Clinical Neurophysiology, 115, 1519-1526.http://dx.doi.org/10.1016/j.clinph.2004.02.005
[51] Karp, B.I., Wassermann, E.M., Porter, S. and Hallett, M. (1997) Transcranial magnetic stimulation acutely decreases motor tics. Neurology, 48, A397.
[52] Siebner, H.R., Auer, C., Ceballos Baumann, A.O., Conrad, B. and Pascual-Leone, A. (1997) Low-frequency repetitive magnetic stimulation of the motor cortex reduces increased writing pressure in writer’s cramp. Electroencephalography and Clinical Neurophysiology, 103, 10.
[53] Pascual-Leone, A., Valls-Sole, J., Brasil-Neto, J.P., Cammarota, A., Grafman, J. and Hallet, M. (1994) Akinesia in Parkinson’s disease. II. Effects of subthreshold repetitive transcranial motor cortex stimulation. Neurology, 44, 892-898. http://dx.doi.org/10.1212/WNL.44.5.892
[54] Lefaucheur, J.P., Drouot, X., Von Raison, F., MenardLefaucheur, I., Cesaro, P. and Nguyen, J.P. (2004) Improvement of motor performance and modulation of cortical excitability by repetitive transcranial magnetic stimulation of the motor cortex in Parkinson’s disease. Clinical Neurophysiology, 115, 2530-2541. http://dx.doi.org/10.1016/j.clinph.2004.05.025
[55] Siebner, H.R., Mentschel, C., Auer, C. and Conrad, B. (1999) Repetitive transcranial magnetic stimulation has a beneficial effect on bradykinesia in Parkinson’s disease. Neuroreport, 10, 589-594. http://dx.doi.org/10.1097/00001756-199902250-00027
[56] Siebner, H.R., Rossmeier, C., Mentschel, C., Peinemann, A. and Conrad, B. (2000) Short-term motor improvement after sub-threshold 5-Hz repetitive transcranial magnetic stimulation of the primary motor hand area in Parkinson’s disease. Journal of the Neurological Sciences, 178, 91-94. http://dx.doi.org/10.1016/S0022-510X(00)00370-1
[57] Khedr, E.M., Ahmed, M.A., Fathy, N. and Rothwell, J.C. (2005) Therapeutic trial of repetitive transcranial magnetic stimulation after acute ischemic stroke. Neurology, 65, 466-468. http://dx.doi.org/10.1212/01.wnl.0000173067.84247.36
[58] George, M.S., Wassermann, E.M., Williams, W.A., et al. (1995) Daily repetitive transcranial magnetic stimulation (rTMS) improves mood in depression. Neuroreport, 6, 1853-1856. http://dx. doi.org/10.1097/00001756-199510020-00008
[59] Burt, T., Lisanby, S.H. and Sackeim, H.A. (2002) Neuropsychiatric applications of transcranial magnetic stimulation: A meta analysis. The International Journal of Neuropsychopharmacology, 5, 73-103. http://dx.doi.org/10.1017/S1461145702002791
[60] Wassermann, E.M. (2002) Safety and side-effects of transcranial magnetic stimulation and repetitive transcranial magnetic stimulation. In: Pascual-Leone, A., Davey, N.J., Rothwell, J., Wasserman, E.M. and Puri, B.K., Eds., Handbook of Transcranial Magnetic Stimulation. Arnold, New York, 39-49.
[61] Petrovsky, B.V. (1979) Atlas of thoracic surgery. Mosby Company, Toronto.

Copyright © 2024 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.