Abstract:Cerebral cortex can modulate cardiovascular activities, which is mediated by autonomic nervous system (ANS). The investigation of the underlying mechanism plays an important role in the diagnosis, treatment, prevention and control of diseases such as arrhythmia, hypertension and heart failure. ECG, BP, chest impedance signals and near infrared spectroscopy (NIRS) signals in the medial prefrontal cortex (MPFC) were collected synchronously in 27 healthy subjects in supine condition and during 70° head-up tilt test (HUT). Heart rate variability (HRV) and Granger causality (GC) methods were applied to investigate cardiovascular responses in HUT and demonstrate the interactions between cerebral blood volume (CBV) in the MPFC and sympathetic/parasympathetic outflows (indicated by nLF and HF, respectively) as well as between CBV in the MPFC and RRI. Results showed that 1) CO decreased by 24% (P<0.001), HR and DBP increased by 35% (P<0.001) and 7% (P<0.001) respectively, while SBP almost showed no change compared with baseline even though it declined at the beginning of HUT; 2) nLF increased while HF decreased gradually, and then kept a relatively stable state with the former more activated (38.75±9.25 vs 58.62±8.58,P<0.001) while the latter less activated (1.11±0.76 vs 0.80±0.48,P<0.05) than the supine condition; 3) CBV in the MPFC was significantly correlated with both sympathetic and parasympathetic outflows and the correlation coefficients were 0.58 and 0.66 respectively; 4) GC showed frequency specificity with preference of “brain→heart” (P<0.05) in the frequency band of 0.04-0.15 Hz while “heart→brain” (P<0.001) in the frequency band of 0.15-0.4 Hz. Our results indicated that significant cardiovascular responses, mainly modulated by sympathetic and parasympathetic outflows, were elicited during HUT and that the MPFC was involved in the ANS-mediated cardiovascular control with ~0.1 Hz oscillations mediating the process. This study provided new evidence for the brain-heart coupling (the characteristic brain-heart interactions in healthy subjects during HUT) and we found that ~0.1 Hz oscillations play an important role in mediating cerebral autonomic control.
[1] Valenza G, Toschi N, Barbieri R. Uncovering brain-heart information through advanced signal and image processing [J]. Philosophical Transactions, 2016, 374(2067):20160020(1-6).
[2] Peter T, Boyett MR, Logantha SJRJ, et al. Anger, emotion, and arrhythmias: from brain to heart [J]. Frontiers in Physiology, 2011, 2:67(1-11).
[3] Loggia ML, Edwards RR, Kim J, et al. Disentangling linear and nonlinear brain responses to evoked deep tissue pain [J]. Pain, 2012, 153(10):2140-2151.
[4] Samuels MA. The brain-heart connection [J]. Circulation, 2007, 116(1):77-84.
[5] Macey PM, Ogren JA, Kumar R, et al. Functional imaging of autonomic regulation: methods and key findings [J]. Frontiers in Neuroscience, 2016, 9(415):513(1-23).
[6] Tang Yiyuan, Ma Yinghua, Fan Yaxin, et al. Central and autonomic nervous system interaction is altered by short-term meditation [J]. Proceedings of the National Academy of Sciences of the United States of America, 2009, 106(22):8865-8870.
[7] Pfurtscheller G, Schwerdtfeger AR, Seither-Preisler A, et al. Brain-heart communication: evidence for “central pacemaker” oscillations with a dominant frequency at 0.1 Hz in the cingulum [J]. Clinical Neurophysiology, 2016, 128(1):183-193.
[8] Nieuwenhuys R. The insular cortex: a review [J]. Progress in Brain Research, 2012, 195(6):123-163.
[9] Gray MA, Taggart P, Sutton PM, et al. A cortical potential reflecting cardiac function [J]. Proceedings of the National Academy of Sciences of the United States of America, 2007, 104(16):6818-6823.
[10] Thayer JF, Lane RD. Claude Bernard and the heart-brain connection: further elaboration of a model of neurovisceral integration [J]. Neuroscience & Biobehavioral Reviews, 2009, 33(2):81-88.
[11] Golestani AM, Chang C, Kwinta JB, et al. Mapping the end-tidal CO2 response function in the resting-state BOLD fMRI signal: spatial specificity, test-retest reliability and effect of fMRI sampling rate [J]. Neuroimage, 2015, 104:266-277.
[12] Beissner F, Meissner K, Bär KJ, et al. The autonomic brain: an activation likelihood estimation meta-analysis for central processing of autonomic function [J]. Journal of Neuroscience, 2013, 33(25):10503-10511.
[13] Kenny RA, Ingram A, Bayliss J, et al. Head-up tilt: a useful test for investigating unexplained syncope [J]. Lancet, 1986, 1(8494):1352-1355.
[14] Macedo PG, Leite LR, Santosneto L, et al. Tilt test — from the necessary to the indispensable [J]. Arq bras cardiol, 2011, 96(3):246-254.
[15] Li Cuiwei, Zheng Chongxun, Tai Changfeng. Detection of ECG characteristic points using wavelet transforms [J]. IEEE Transactions on Biomedical Engineering, 2002, 42(1):21-28.
[16] Schiecke K, Wacker M, Piper D, et al. Time-variant, frequency-selective, linear and nonlinear analysis of heart rate variability in children with temporal lobe epilepsy [J]. IEEE Transactions on Biomedical Engineering, 2014, 61(6):1798-1808.
[17] Sramek BB. Cardiac output by electrical impedance [J]. Medical Electronics, 1982, 13(2):93-97.
[18] Brovelli A, Ding Mingzhou, Ledberg A, et al. Beta oscillations in a large-scale sensorimotor cortical network: directional influences revealed by granger causality [J]. Proc Natl AcadSci USA, 2004, 101(26):9849-9854.
[19] Keil A, Sabatinelli D, Ding Mingzhou, et al. Re-entrant projections modulate visual cortex in affective perception: evidence from granger causality analysis [J]. Human Brain Mapping, 2009, 30(2):532-540.
[20] Sato JR, Junior EA, Takahashi DY, et al. A method to produce evolving functional connectivity maps during the course of an fMRI experiment using wavelet-based time-varying granger causality [J]. Neuroimage, 2006, 31(1):187-196.
[21] Papoulis A, Pillai SU. Random variables and stochastic processes [M]. New York: McGraw-Hill, 2002.
[22] Pfurtscheller G, Daly I, Bauernfeind G, et al. Coupling between intrinsic prefrontal HbO2 and central EEG beta power oscillations in the resting brain [J].PLoS ONE, 2012, 7(8):e43640(1-9).
[23] Nikulin VV, Fedele T, Mehnert J, et al. Monochromatic ultra-slow (~0.1 Hz) oscillations in the human electroencephalogram and their relation to hemodynamics [J]. Neuroimage, 2014, 97:71-80.
[24] Golanov EV, Yamamoto S, Reis DJ. Spontaneous waves of cerebral blood flow associated with a pattern of electrocortical activity [J]. American Journal of Physiology, 1994, 266(2):204-214.
[25] Wong SW, Massé N, Kimmerly DS, et al. Ventral medial prefrontal cortex and cardiovagal control in conscious humans [J]. Neuroimage, 2007, 35(2):698-708.
[26] Resstel LB, Fernandes KB, Corrêa FM. Medial prefrontal cortex modulation of the baroreflex parasympathetic component in the rat [J]. Brain Research, 2004, 1015(1):136-144.
[27] Resstel LB, Corrêa FM. Medial prefrontal cortex NMDA receptors and nitric oxide modulate the parasympathetic component of the baroreflex [J]. European Journal of Neuroscience, 2006, 23(2):481-488.
[28] Hyman JM, Hasselmo ME, Seamans JK. What is the functional relevance of prefrontal cortex entrainment to hippocampal theta rhythms? [J]. Frontiers in Neuroscience, 2011, 5(6):24(1-13).
[29] Goswami R, Frances MF, Shoemaker JK. Representation of somatosensory inputs within the cortical autonomic network [J]. Neuroimage, 2011, 54(2):1211-1220.
[30] Pfurtscheller G, Klobassa DS, Bauernfeind G, et al. Cardiovascular responses after brisk finger movement and their dependency on the “eigenfrequency” of the baroreflex loop [J]. Neuroscience Letters, 2011, 490(1):31-35.
[31] Pfurtscheller G, Schwerdtfeger A, Seither-Preisler A, et al. Synchronization of intrinsic 0.1-Hz blood-oxygen-level-dependent oscillations in amygdala and prefrontal cortex in subjects with increased state anxiety [J]. European Journal of Neuroscience, 2018, 47: 417-426.
[32] Huang C, Gevirtz RN, Onton J, et al. Investigation of vagal afferent functioning using the heartbeat event related potential [J]. International Journal of Psychophysiology, 2013, 39(3):308-319.
[33] Mather M, Thayer JF. How heart rate variability affects emotion regulation brain networks [J]. Current Opinion in Behavioral Sciences, 2018, 19:98-104.
[34] Faes L, Greco A, Lanata A, et al. Causal brain-heart information transfer during visual emotional elicitation in healthy subjects: preliminary evaluations and future perspectives [C]// Annual Conference of IEEE EMBS. Seogwipo: IEEE, 2017:1559-1562.