Resting heart rate (variability) and cognition relationships reveal cognitively healthy individuals with pathological amyloid/ta
Authors:
Journal: Frontiers in epidemiology
Publication Type: Journal Article
Date: 2023
DOI: NIHMS1919996
ID: 37587981
Abstract
Resting heart rate (HR) and heart rate variability (HRV) have been linked with cognition in the general population and in older individuals. The knowledge of this aspect of heart-brain relationship is relatively absent in older individuals with early Alzheimer's disease (AD) pathology. This study explores relationships of the HR, HRV, and cognition in cognitively healthy individuals with pathological amyloid/tau ratio (CH-PATs) in cerebral spinal fluid (CSF) compared to those with normal ratio (CH-NATs).
Reference List
- Thayer JF, Hansen AL, Saus-Rose E, Johnsen BH. Heart rate variability, prefrontal neural function, and cognitive performance: the neurovisceral integration perspective on self-regulation, adaptation, and health. Ann Behav Med. (2009) 37(2):141–53. 10.1007/s12160-009-9101-z|||Williams DP, Cash C, Rankin C, Bernardi A, Koenig J, Thayer JF. Resting heart rate variability predicts self-reported difficulties in emotion regulation: a focus on different facets of emotion regulation. Front Psychol. (2015) 6:261. 10.3389/fpsyg.2015.00261|||Kataoka N, Shima Y, Nakajima K, Nakamura K. A central master driver of psychosocial stress responses in the rat. Science. (2020) 367(6482):1105–12. 10.1126/science.aaz4639|||Silvani A, Calandra-Buonaura G, Dampney RA, Cortelli P. Brain-heart interactions: physiology and clinical implications. Philos Trans A Math Phys Eng Sci. (2016) 374(2067). 10.1098/rsta.2015.0181|||Thayer JF, Ahs F, Fredrikson M, Sollers JJ, III, Wager TD. A meta-analysis of heart rate variability and neuroimaging studies: implications for heart rate variability as a marker of stress and health. Neurosci Biobehav Rev. (2012) 36(2):747–56. 10.1016/j.neubiorev.2011.11.009|||Leong DP, O'Donnell MJ, Teo K, Smyth A, Joseph P, Gao P, et al. Resting heart rate and decline in cognitive function: observations from the ONTARGET/TRANSCEND studies. Eur Heart J. (2013) 34(Suppl 1):499–500. 10.1093/eurheartj/eht309.P2737|||van der Veen FM, van der Molen MW, Jennings JR. Selective inhibition is indexed by heart rate slowing. Psychophysiology. (2000) 37(5):607–13. 10.1111/1469-8986.3750607|||Williams DP, Thayer JF, Koenig J. Resting cardiac vagal tone predicts intraindividual reaction time variability during an attention task in a sample of young and healthy adults. Psychophysiology. (2016) 53(12):1843–51. 10.1111/psyp.12739|||Cummings J, Lee G, Ritter A, Sabbagh M, Zhong K. Alzheimer’s disease drug development pipeline: 2019. Alzheimers Dement (N Y). (2019) 5:272–93. 10.1016/j.trci.2019.05.008|||Harari O, Cruchaga C, Kauwe JS, Ainscough BJ, Bales K, Pickering EH, et al. Phosphorylated tau-abeta42 ratio as a continuous trait for biomarker discovery for early-stage Alzheimer’s disease in multiplex immunoassay panels of cerebrospinal fluid. Biol Psychiatry. (2014) 75(9):723–31. 10.1016/j.biopsych.2013.11.032|||Nathan PJ, Lim YY, Abbott R, Galluzzi S, Marizzoni M, Babiloni C, et al. Association between CSF biomarkers, hippocampal volume and cognitive function in patients with amnestic mild cognitive impairment (MCI). Neurobiol Aging. (2017) 53:1–10. 10.1016/j.neurobiolaging.2017.01.013|||Harrington MG, Chiang J, Pogoda JM, Gomez M, Thomas K, Marion SD, et al. Executive function changes before memory in preclinical Alzheimer’s pathology: a prospective, cross-sectional, case control study. PLoS One. (2013) 8(11):e79378. 10.1371/journal.pone.0079378|||Rochart R, Liu Q, Fonteh AN, Harrington MG, Arakaki X. Compromised Behavior and Gamma Power During Working Memory in Cognitively Healthy Individuals With Abnormal CSF Amyloid/Tau. Front Aging Neurosci. (2020) 12:574214. 10.3389/fnagi.2020.574214|||Wilder C, Moncrieffe K, Nolty A, Arakaki X, Fonteh AN, Harrington MG. Boston naming test predicts deterioration of cerebrospinal fluid biomarkers in pre-symptomatic Alzheimer’s disease. FASEB J. (2018). 10.1096/fasebj.2018.32.1_supplement.545.1|||Arakaki X, Hung SM, Rochart R, Fonteh AN, Harrington MG. Alpha desynchronization during stroop test unmasks cognitively healthy individuals with abnormal CSF amyloid/tau. Neurobiol Aging. (2022) 112:87–101. 10.1016/j.neurobiolaging.2021.11.009|||Arakaki X, Lee R, King KS, Fonteh AN, Harrington MG. Alpha desynchronization during simple working memory unmasks pathological aging in cognitively healthy individuals. PLoS One. (2019) 14(1):e0208517. 10.1371/journal.pone.0208517|||Arechavala RJ, Rochart R, Kloner RA, Liu A, Wu DA, Hung SM, et al. Task switching reveals abnormal brain-heart electrophysiological signatures in cognitively healthy individuals with abnormal CSF amyloid/tau, a pilot study. Int J Psychophysiol. (2021) 170:102–11. 10.1016/j.ijpsycho.2021.10.007|||Chang WH, Lee IH, Chi MH, Lin SH, Chen KC, Chen PS, et al. Prefrontal cortex modulates the correlations between brain-derived neurotrophic factor level, serotonin, and the autonomic nervous system. Sci Rep. (2018) 8(1):2558. 10.1038/s41598-018-20923-y|||Guntekin B, Akturk T, Arakaki X, Bonanni L, Del Percio C, Edelmayer R, et al. Are there consistent abnormalities in event-related EEG oscillations in patients with Alzheimer’s disease compared to other diseases belonging to dementia? Psychophysiology. (2022) 59(5):e13934. 10.1111/psyp.13934|||Beekly DL, Ramos EM, Lee WW, Deitrich WD, Jacka ME, Wu J, et al. The national Alzheimer’s coordinating center (NACC) database: the uniform data set. Alzheimer Dis Assoc Disord. (2007) 21(3):249–58. 10.1097/WAD.0b013e318142774e|||McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM. Clinical diagnosis of Alzheimer’s disease: report of the NINCDS-ADRDA work group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology. (1984) 34(7):939–44. 10.1212/WNL.34.7.939|||McKhann GM, Knopman DS, Chertkow H, Hyman BT, Jack CR, Jr, Kawas CH, et al. The diagnosis of dementia due to Alzheimer’s disease: recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimers Dement. (2011) 7(3):263–9. 10.1016/j.jalz.2011.03.005|||Petersen RC. Mild cognitive impairment as a diagnostic entity. J Intern Med. (2004) 256(3):183–94. 10.1111/j.1365-2796.2004.01388.x|||Seshadri S, Beiser A, Au R, Wolf PA, Evans DA, Wilson RS, et al. Operationalizing diagnostic criteria for Alzheimer’s disease and other age-related cognitive impairment-part 2. Alzheimers Dement. (2011) 7(1):35–52. 10.1016/j.jalz.2010.12.002|||Elliott KE, McCall KL, Fike DS, Polk J, Raehl C. Assessment of manual blood pressure and heart rate measurement skills of pharmacy students: a follow-up investigation. Am J Pharm Educ. (2008) 72(3):60. 10.5688/aj720360|||Gonzalez Viejo C, Fuentes S, Torrico DD, Dunshea FR. Non-contact heart rate and blood pressure estimations from video analysis and machine learning modelling applied to food sensory responses: a case study for chocolate. Sensors (Basel). (2018) 18:6. 10.3390/s18061802|||Deater-Deckard K, Bell MA. Maternal executive function, heart rate, and EEG alpha reactivity interact in the prediction of harsh parenting. J Fam Psychol. (2017) 31(1):41–50. 10.1037/fam0000286|||Cheng YJ, Macera CA, Church TS, Blair SN. Heart rate reserve as a predictor of cardiovascular and all-cause mortality in men. Med Sci Sports Exerc. (2002) 34(12):1873–8. 10.1097/00005768-200212000-00003|||Zuo W, Wu J. The interaction and pathogenesis between cognitive impairment and common cardiovascular diseases in the elderly. Ther Adv Chronic Dis. (2022) 13:20406223211063020. 10.1177/20406223211063020|||Hestad KA, Engedal K, Hollan I, Girouard H. Editorial: the heart-brain connection in emotions, cognition, and dementia. Front Aging Neurosci. (2022) 14:1074280. 10.3389/fnagi.2022.1074280|||Nicolini P, Lucchi T, Abbate C, Inglese S, Tomasini E, Mari D, et al. Autonomic function predicts cognitive decline in mild cognitive impairment: evidence from power spectral analysis of heart rate variability in a longitudinal study. Front Aging Neurosci. (2022) 14:886023. 10.3389/fnagi.2022.886023|||Fox K, Borer JS, Camm AJ, Danchin N, Ferrari R, Lopez Sendon JL, et al. Resting heart rate in cardiovascular disease. J Am Coll Cardiol. (2007) 50(9):823–30. 10.1016/j.jacc.2007.04.079|||Levine HJ. Rest heart rate and life expectancy. J Am Coll Cardiol. (1997) 30(4):1104–6. 10.1016/S0735-1097(97)00246-5|||Boudoulas KD, Borer JS, Boudoulas H. Heart rate, life expectancy and the cardiovascular system: therapeutic considerations. Cardiology. (2015) 132(4):199–212. 10.1159/000435947|||Dong Y, Jiang L, Wang X, Chen Z, Zhang L, Zhang Z, et al. Central rather than brachial pressures are stronger predictors of cardiovascular outcomes: a longitudinal prospective study in a Chinese population. J Clin Hypertens (Greenwich). (2020) 22(4):623–30. 10.1111/jch.13838|||Roman MJ, Devereux RB, Kizer JR, Lee ET, Galloway JM, Ali T, et al. Central pressure more strongly relates to vascular disease and outcome than does brachial pressure: the strong heart study. Hypertension. (2007) 50(1):197–203. 10.1161/HYPERTENSIONAHA.107.089078|||McEniery CM, Cockcroft JR, Roman MJ, Franklin SS, Wilkinson IB. Central blood pressure: current evidence and clinical importance. Eur Heart J. (2014) 35(26):1719–25. 10.1093/eurheartj/eht565|||Miyashita H. Clinical assessment of central blood pressure. Curr Hypertens Rev. (2012) 8(2):80–90. 10.2174/157340212800840708|||Suleman R, Padwal R, Hamilton P, Senthilselvan A, Alagiakrishnan K. Association between central blood pressure, arterial stiffness, and mild cognitive impairment. Clin Hypertens. (2017) 23:2. 10.1186/s40885-016-0058-5|||Compton RO, Figueroa A, Gonzales JU. Postexercise hypotension in central aortic pressures following walking and its relation to cardiorespiratory fitness. J Sports Med Phys Fitness. (2019) 59(4):717–22. 10.23736/S0022-4707.18.08615-2|||Hintsala HE, Valtonen RIP, Kiviniemi A, Crandall C, Perkiomaki J, Hautala A, et al. Central aortic hemodynamics following acute lower and upper-body exercise in a cold environment among patients with coronary artery disease. Sci Rep. (2021) 11(1):2550. 10.1038/s41598-021-82155-x|||Jouven X, Empana JP, Schwartz PJ, Desnos M, Courbon D, Ducimetiere P. Heart-rate profile during exercise as a predictor of sudden death. N Engl J Med. (2005) 352(19):1951–8. 10.1056/NEJMoa043012|||Fox K, Ford I, Steg PG, Tendera M, Robertson M, Ferrari R, BEAUTIFUL investigators. Heart rate as a prognostic risk factor in patients with coronary artery disease and left-ventricular systolic dysfunction (BEAUTIFUL): a subgroup analysis of a randomised controlled trial. Lancet. (2008) 372(9641):817–21. 10.1016/S0140-6736(08)61171-X|||Kennedy DO, Scholey AB. Glucose administration, heart rate and cognitive performance: effects of increasing mental effort. Psychopharmacology (Berl). (2000) 149(1):63–71. 10.1007/s002139900335|||Boudoulas H, Rittgers SE, Lewis RP, Leier CV, Weissler AM. Changes in diastolic time with various pharmacologic agents: implication for myocardial perfusion. Circulation. (1979) 60(1):164–9. 10.1161/01.CIR.60.1.164|||Novak P. Cerebral blood flow, heart rate, and blood pressure patterns during the tilt test in common orthostatic syndromes. Neurosci J. (2016) 2016:6127340. 10.1155/2016/6127340|||Xing CY, Tarumi T, Meijers RL, Turner M, Repshas J, Xiong L, et al. Arterial pressure, heart rate, and cerebral hemodynamics across the adult life span. Hypertension. (2017) 69(4):712–20. 10.1161/HYPERTENSIONAHA.116.08986|||Custodis F, Schirmer SH, Baumhakel M, Heusch G, Bohm M, Laufs U. Vascular pathophysiology in response to increased heart rate. J Am Coll Cardiol. (2010) 56(24):1973–83. 10.1016/j.jacc.2010.09.014|||Drouin A, Gendron ME, Thorin E, Gillis MA, Mahlberg-Gaudin F, Tardif JC. Chronic heart rate reduction by ivabradine prevents endothelial dysfunction in dyslipidaemic mice. Br J Pharmacol. (2008) 154(4):749–57. 10.1038/bjp.2008.116|||Bealer SL. Systemic angiotensin II alters intrinsic heart rate through central mechanisms. Brain Res Bull. (2002) 58(1):61–5. 10.1016/S0361-9230(02)00756-6|||Mestre H, Tithof J, Du T, Song W, Peng W, Sweeney AM, et al. Flow of cerebrospinal fluid is driven by arterial pulsations and is reduced in hypertension. Nat Commun. (2018) 9(1):4878. 10.1038/s41467-018-07318-3|||Forte G, Favieri F, Casagrande M. Heart rate variability and cognitive function: a systematic review. Front Neurosci. (2019) 13:710. 10.3389/fnins.2019.00710|||Almeida-Santos MA, Barreto-Filho JA, Oliveira JL, Reis FP, da Cunha Oliveira CC, Sousa AC. Aging, heart rate variability and patterns of autonomic regulation of the heart. Arch Gerontol Geriatr. (2016) 63:1–8. 10.1016/j.archger.2015.11.011|||Miyake A, Friedman NP. The nature and organization of individual differences in executive functions: four general conclusions. Curr Dir Psychol Sci. (2012) 21(1):8–14. 10.1177/0963721411429458|||Diamond A. Executive functions. Annu Rev Psychol. (2013) 64:135–68. 10.1146/annurev-psych-113011-143750|||Gallego Hiroyasu EM, Yotsumoto Y. Older adults preserve accuracy but not precision in explicit and implicit rhythmic timing. PLoS One. (2020) 15(10):e0240863. 10.1371/journal.pone.0240863|||Hardwick RM, Forrence AD, Costello MG, Zackowski K, Haith AM. Age-related increases in reaction time result from slower preparation, not delayed initiation. J Neurophysiol. (2022) 128(3):582–92. 10.1152/jn.00072.2022|||Valenza G, Sclocco R, Duggento A, Passamonti L, Napadow V, Barbieri R, et al. The central autonomic network at rest: uncovering functional MRI correlates of time-varying autonomic outflow. Neuroimage. (2019) 197:383–90. 10.1016/j.neuroimage.2019.04.075|||Kim MS, Yoon JH, Hong JM. Early differentiation of dementia with Lewy bodies and Alzheimer’s disease: heart rate variability at mild cognitive impairment stage. Clin Neurophysiol. (2018) 129(8):1570–8. 10.1016/j.clinph.2018.05.004|||Kasanuki K, Iseki E, Fujishiro H, Ando S, Sugiyama H, Kitazawa M, et al. Impaired heart rate variability in patients with dementia with Lewy bodies: efficacy of electrocardiogram as a supporting diagnostic marker. Parkinsonism Relat Disord. (2015) 21(7):749–54. 10.1016/j.parkreldis.2015.04.024|||Nicolini P, Mari D, Abbate C, Inglese S, Bertagnoli L, Tomasini E, et al. Autonomic function in amnestic and non-amnestic mild cognitive impairment: spectral heart rate variability analysis provides evidence for a brain-heart axis. Sci Rep. (2020) 10(1):11661. 10.1038/s41598-020-68131-x|||Galluzzi S, Nicosia F, Geroldi C, Alicandri A, Bonetti M, Romanelli G, et al. Cardiac autonomic dysfunction is associated with white matter lesions in patients with mild cognitive impairment. J Gerontol A Biol Sci Med Sci. (2009) 64(12):1312–5. 10.1093/gerona/glp105|||Giubilei F, Strano S, Imbimbo BP, Tisei P, Calcagnini G, Lino S, et al. Cardiac autonomic dysfunction in patients with Alzheimer disease: possible pathogenetic mechanisms. Alzheimer Dis Assoc Disord. (1998) 12(4):356–61. 10.1097/00002093-199812000-00017|||Aharon-Peretz J, Harel T, Revach M, Ben-Haim SA. Increased sympathetic and decreased parasympathetic cardiac innervation in patients with Alzheimer’s disease. Arch Neurol. (1992) 49(9):919–22. 10.1001/archneur.1992.00530330041013|||Lin F, Ren P, Wang X, Anthony M, Tadin D, Heffner KL. Cortical thickness is associated with altered autonomic function in cognitively impaired and non-impaired older adults. J Physiol. (2017) 595(22):6969–78. 10.1113/JP274714|||Fisher AJ, Medaglia JD, Jeronimus BF. Lack of group-to-individual generalizability is a threat to human subjects research. Proc Natl Acad Sci U S A. (2018) 115(27):E6106–15. 10.1073/pnas.1711978115