Skip to main content
SpringerLink
Log in

Role of the prefrontal lobe in young normotensives with a family history of hypertension and hypertensives

  • Integrative physiology
  • Published:
Pflügers Archiv - European Journal of Physiology Aims and scope Submit manuscript

Abstract

Accumulating evidence has demonstrated a significant relationship between prefrontal lobe and hypertension. Elevated blood pressure is usually associated with a prefrontal hemodynamic abnormality. However, the detailed process is still unclear. In this study, we designed a startle protocol and tested the response of the cerebral cortex and cardiovascular system in young normotensive subjects with a family history of hypertension (FH+). Additionally, the cold forehead test (CFT) was performed in hypertensive subjects. In total, 40 young normotensive subjects (21 with FH+ and 19 without a family history of hypertension (FH-)) and 49 middle-aged subjects (21 normotensives (NT) and 28 hypertensives (HT)) were recruited. Our results showed that the magnitude of startle-evoked alpha oscillation at the parasympathetic-related prefrontal cortex (FP1 and FP2) in the FH+ group was significantly smaller than in the FH- group. Acute bradycardia (RRI increase) was observed in FH- subjects but disappeared in the FH+ group. The coupling between instant cardiac acute response (increased RRI) and prefrontal arousal (magnitude of evoked oscillation) was significantly weakened in the FH+ group compared with the FH- group. Furthermore, the decrease in HR induced by parasympathetic outflow during CFT was absent in HT subjects. Hence, we concluded that the impairment of parasympathetic outflow derived from the prefrontal lobe occurs in both healthy young offspring of hypertensive and hypertensive patients.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  1. Andrew S (2008) Psychophysiological stress reactivity and hypertension. Hypertension 52:220–221

    Article  Google Scholar 

  2. Chen KH, Aksan N, Anderson SW, Grafft A, Chapleau MW (2014) Habituation of parasympathetic-mediated heart rate responses to recurring acoustic startle. Front Psychol 5:1288

    PubMed  PubMed Central  Google Scholar 

  3. De Wardener HE (2001) The hypothalamus and hypertension. Physiol Rev 81:1599–1658

    Article  Google Scholar 

  4. Fiorenzo M, Lucia V, Maurizio S, Daniele T, Francesco A (2004) The cerebral cortex of spontaneously hypertensive rats: a quantitative microanatomical study. Clin Exp Hypertens 26:287–303

    Article  Google Scholar 

  5. Fujishima M, Ibayashi S, Fujii K, Mori S (1995) Cerebral blood flow and brain function in hypertension. Hypertens Res Off J Jpn Soc Hypertens 18:111

    Article  CAS  Google Scholar 

  6. Gautier CH, Cook EW (1997) Relationship between startle and cardiovascular reactivity. Psychophysiology 34:87–96

    Article  CAS  Google Scholar 

  7. Gianaros PJ, Wager TD (2015) Brain-body pathways linking psychological stress and physical health. Curr Dir Psychol Sci 24:313

    Article  Google Scholar 

  8. Goit RK, Ansari AH (2016) Reduced parasympathetic tone in newly diagnosed essential hypertension. Indian Heart J 68:153–157

    Article  Google Scholar 

  9. Gonzalez CE, Jennifer P, Beason-Held LL, Resnick SM (2015) Longitudinal changes in cortical thinning associated with hypertension. J Hypertens 33:1242–1248

    Article  CAS  Google Scholar 

  10. Goswami R, Frances MF, Shoemaker JK (2011) Representation of somatosensory inputs within the cortical autonomic network. Neuroimage 54:1211–1220

    Article  Google Scholar 

  11. Grant H, Bhambhani Y, Singhal A (2015) Hemodynamic changes in the prefrontal cortex during working memory in essential hypertension. J Am Soc Hypertens 9:628–639

    Article  Google Scholar 

  12. Haroutunian V, Campbell BA (1981) Development and habituation of the heart rate orienting response to auditory and visual stimuli in the rat. J Comp Physiol Psychol 95:166–174

    Article  CAS  Google Scholar 

  13. Jennings JR, Zanstra Y (2009) Is the brain the essential in hypertension? Neuroimage 47:914–921

    Article  Google Scholar 

  14. Keefe FB, Johnson LC (1970) Cardiovascular responses to auditory stimuli. Psychon Sci 19:335–337

    Article  Google Scholar 

  15. Khurana RK, Wu R (2006) The cold face test: a non-baroreflex mediated test of cardiac vagal function. Clinical Auton Res 16:202–207

    Article  Google Scholar 

  16. Kunkler PE, Hwang BH (1995) Lower GABAA receptor binding in the amygdala and hypothalamus of spontaneously hypertensive rats. Brain Res Bull 36:57–61

    Article  CAS  Google Scholar 

  17. Langewitz W, Rüddel H, Schächinger H (1994) Reduced parasympathetic cardiac control in patients with hypertension at rest and under mental stress. Am Heart J 127:122

    Article  CAS  Google Scholar 

  18. Li DP, Pan HL (2006) Plasticity of GABAergic control of hypothalamic presympathetic neurons in hypertension. Am J Physiol Heart Circ Physiol 290:1110–1119

    Article  Google Scholar 

  19. Li C, Zheng C, Tai C (1995) Detection of ECG characteristic points using wavelet transforms. IEEE Trans Biomed Eng 42:21–28

    Article  CAS  Google Scholar 

  20. Mann KD, Hoyt C, Feldman S, Blunt L, Raymond A, Page-Mccaw PS (2010) Cardiac response to startle stimuli in larval zebrafish: sympathetic and parasympathetic components. Am J Physiol Regul Integr Comp Physiol 298:R1288–R1297

    Article  CAS  Google Scholar 

  21. Norton KN, Luchyshyn TA, Kevin SJ (2013) Evidence for a medial prefrontal cortex-hippocampal axis associated with heart rate control in conscious humans. Brain Res 1538:104–115

    Article  CAS  Google Scholar 

  22. Piccirillo G, Viola E, Nocco M, Durante M, Tarantini S, Marigliano V (2000) Autonomic modulation of heart rate and blood pressure in normotensive offspring of hypertensive subjects. Journal of Laboratory & Clinical Medicine 135:145–152

    Article  CAS  Google Scholar 

  23. Resstel LBM, Corrêa FMA (2006) Medial prefrontal cortex NMDA receptors and nitric oxide modulate the parasympathetic component of the baroreflex. European Journal of Neuroscience 23:481–488

    Article  CAS  Google Scholar 

  24. Resstel LB, Fernandes KB, Corrêa FM (2004) Medial prefrontal cortex modulation of the baroreflex parasympathetic component in the rat. Brain Res 1015:136

    Article  CAS  Google Scholar 

  25. Seryapina AA, Shevelev OB, Moshkin MP, Markel AL, Akulov AE (2017) Stress-sensitive arterial hypertension, haemodynamic changes and brain metabolites in hypertensive ISIAH rats: MRI investigation. A Seryapina AA. Experimental Physiology 102:523–532

    Article  CAS  Google Scholar 

  26. Shonis CA (1994) Altered GABA ergic system in the posterior hypothalamus of the spontaneously hypertensive rat. Biology Neuroscience

  27. Sierra C (2001) Cerebral white matter lesions in essential hypertension. Current Hypertension Reports 3:429–433

    Article  CAS  Google Scholar 

  28. Slart RHJA, Tio RA, Elsinga PH, Schwaiger M (2015) Autonomic innervation of the heart. Springer, Berlin Heidelberg

    Book  Google Scholar 

  29. Sterley TL, Howells FM, Russell VA (2013) Evidence for reduced tonic levels of GABA in the hippocampus of an animal model of ADHD, the spontaneously hypertensive rat. Brain Research 1541:52–60

    Article  CAS  Google Scholar 

  30. Swenne CA (2013) Baroreflex sensitivity: mechanisms and measurement. Netherlands Heart Journal 21:58–60

    Article  CAS  Google Scholar 

  31. Thayer JF, Lane RD (2009) Claude Bernard and the heart-brain connection: further elaboration of a model of neurovisceral integration. Neurosci Biobehav Rev 33:81–88. https://doi.org/10.1016/j.neubiorev.2008.08.004

    Article  PubMed  Google Scholar 

  32. Verberne AJM, Lewis SJ, Worland PJ, Beart PM, Jarrott B, Christie MJ, Louis WJ (1987) Medial prefrontal cortical lesions modulate baroreflex sensitivity in the rat. Brain research 426:243

    Article  CAS  Google Scholar 

  33. Wager TDVAV, Hughes B, Davidson M, Lindquist MA, Ochsner KN (2009) Brain mediators of cardiovascular responses to social threat. Part II: prefrontal- subcortical pathways and relationship with anxiety. NeuroImage 47:836–851

    Article  Google Scholar 

  34. Wager TD, Waugh CE, Lindquist M, Noll DC, Fredrickson BL, Taylor SF (2009) Brain mediators of cardiovascular responses to social threat. Part I: Reciprocal dorsal and ventral sub-regions of the medial prefrontal cortex and heart-rate reactivity. Neuroimage 47:836–851

    Article  Google Scholar 

  35. Wang X, Liu B, Xie L, Yu X, Li M, Zhang J (2016) Cerebral and neural regulation of cardiovascular activity during mental stress. Biomed Eng Online 15:335–347

    Google Scholar 

  36. Winkelmann T, Thayer JF, Pohlack S, Nees F, Grimm O, Flor H (2016) Structural brain correlates of heart rate variability in a healthy young adult population. Brain Struct Funct:1–8

  37. Wong SW, Massé N, Kimmerly DS, Menon RS, Shoemaker JK (2007) Ventral medial prefrontal cortex and cardiovagal control in conscious humans. Neuroimage 35:698–708

    Article  Google Scholar 

  38. Xie L, Li M, Dang S, Li C, Wang X, Liu B, Mei M, Zhang J (2018) Impaired cardiorespiratory coupling in young normotensives with a family history of hypertension. J Hypertens 1

  39. Young BJ, Leaton RN (1994) Fear potentiation of acoustic startle stimulus-evoked heart rate changes in rats. Behav Neurosci 108:1065

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Funding from the Chinese National Natural Science Foundation (No. 11872297 and No. 61302011) is gratefully acknowledged.

Author information

Authors and Affiliations

  1. The Key Laboratory of Biomedical Information Engineering of Ministry of Education, Institute of Health and Rehabilitation Science, School of Life Science and Technology, Xi’an Jiaotong University, No.28, Xianning West Road, Xi’an, 710049, Shaanxi, People’s Republic of China

    Xiaoni Wang, Fadong Zhao, Saisai Yan, Xinzhu Zhang, Lin Xie, Binbin Liu, Xiaohui Di & Jianbao Zhang

  2. Equipment Management and Support College, Engineering University of People’s Armed Police, Xi’an, People’s Republic of China

    Fadong Zhao

  3. School of Materials, The University of Manchester, Manchester, M13 9PL, UK

    Yi Li

Authors
  1. Xiaoni Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fadong Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Saisai Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xinzhu Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lin Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Binbin Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xiaohui Di
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yi Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jianbao Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jianbao Zhang.

Ethics declarations

Funding information

Publication charges for this article have been funded by the Chinese National Natural Science Foundation (No. 11872297).

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, X., Zhao, F., Yan, S. et al. Role of the prefrontal lobe in young normotensives with a family history of hypertension and hypertensives. Pflugers Arch - Eur J Physiol 471, 1397–1406 (2019). https://doi.org/10.1007/s00424-019-02313-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00424-019-02313-z

Keywords

Search

Navigation