The effects of partial sleep restriction and subsequent caffeine ingestion on neurovascular coupling.

Alice B Lester, Gavin Buckingham, Bert Bond
Author Information
  1. Alice B Lester: Exeter Head Impacts, Brain Injury and Trauma (ExHIBIT) Research Group, Department of Public Health and Sport Sciences, University of Exeter, Exeter, UK. ORCID
  2. Gavin Buckingham: Exeter Head Impacts, Brain Injury and Trauma (ExHIBIT) Research Group, Department of Public Health and Sport Sciences, University of Exeter, Exeter, UK.
  3. Bert Bond: Exeter Head Impacts, Brain Injury and Trauma (ExHIBIT) Research Group, Department of Public Health and Sport Sciences, University of Exeter, Exeter, UK.

Abstract

Habitual poor sleep is associated with cerebrovascular disease. Acute sleep deprivation alters the ability to match brain blood flow to metabolism (neurovascular coupling [NVC]) but it is not known how partial sleep restriction affects NVC. When rested, caffeine disrupts NVC, but its effects in the sleep-restricted state are unknown. The purpose of this study was therefore to investigate the effects of partial sleep restriction and subsequent caffeine ingestion on NVC. A total of 17 adults (mean [standard deviation] age 27 [5] years, nine females) completed three separate overnight conditions with morning supplementation: habitual sleep plus placebo (Norm_Pl), habitual sleep plus caffeine (Norm_Caf), and partial (50% habitual sleep) restriction plus caffeine (PSR_Caf). NVC responses were quantified as blood velocity through the posterior (PCAv) and middle (MCAv) cerebral arteries using transcranial Doppler ultrasound during a visual search task and cognitive function tests, respectively. NVC was assessed the evening before and twice the morning after each sleep condition-before and 1-h after caffeine ingestion. NVC responses as a percentage increase in PCAv and MCAv from resting baseline were not different at any timepoint, across all conditions (p > 0.053). MCAv at baseline, and PCAv at baseline, peak, and total area under the curve were lower 1-h after caffeine in both Norm_Caf and PSR_Caf as compared to Norm_Pl (p < 0.05), with no difference between Norm_Caf and PSR_Caf (p > 0.14). In conclusion, NVC was unaltered after 50% sleep loss, and caffeine did not modify the magnitude of the response in the rested or sleep-deprived state. Future research should explore how habitual poor sleep affects cerebrovascular function.

Keywords

References

  1. Addicott, M. A., Yang, L. L., Peiffer, A. M., Burnett, L. R., Burdette, J. H., Chen, M. Y., Hayasaka, S., Kraft, R. A., Maldjian, J. A., & Laurienti, P. J. (2009). The effect of daily caffeine use on cerebral blood flow: How much caffeine can we tolerate? Human Brain Mapping., 30(10), 3102–3114.
  2. Avidan, A. Y. (2006). Sleep and neurologic problems in the elderly. Sleep Medicine Clinics, 1(2), 273–292.
  3. Babson, K. A., Trainor, C. D., Feldner, M. T., & Blumenthal, H. (2010). A test of the effects of acute sleep deprivation on general and specific self‐reported anxiety and depressive symptoms: An experimental extension. Journal of Behavior Therapy and Experimental Psychiatry., 41(3), 297–303.
  4. Bélanger, S., Belleville, S., & Gauthier, S. (2010). Inhibition impairments in Alzheimer's disease, mild cognitive impairment and healthy aging: Effect of congruency proportion in a Stroop task. Neuropsychologia, 48(2), 581–590.
  5. Burma, J. S., Macaulay, A., Copeland, P. V., Khatra, O., Bouliane, K. J., & Smirl, J. D. (2021). Temporal evolution of neurovascular coupling recovery following moderate‐and high‐intensity exercise. Physiological Reports, 9(2), e14695.
  6. Burma, J. S., Van Roessel, R. K., Oni, I. K., Dunn, J. F., & Smirl, J. D. (2022). Neurovascular coupling on trial: How the number of trials completed impacts the accuracy and precision of temporally derived neurovascular coupling estimates. Journal of Cerebral Blood Flow & Metabolism., 42, 1492.
  7. Burma, J. S., Wassmuth, R. M., Kennedy, C. M., Miutz, L. N., Newel, K. T., Carere, J., & Smirl, J. D. (2021). Does task complexity impact the neurovascular coupling response similarly between males and females? Physiological Reports, 9(17), e15020.
  8. Buysse, D. J., Reynolds, C. F., III, Monk, T. H., Berman, S. R., & Kupfer, D. J. (1989). The Pittsburgh sleep quality index: A new instrument for psychiatric practice and research. Psychiatry Research, 28(2), 193–213.
  9. Cain, S. W., Silva, E. J., Chang, A.‐M., Ronda, J. M., & Duffy, J. F. (2011). One night of sleep deprivation affects reaction time, but not interference or facilitation in a Stroop task. Brain and Cognition, 76(1), 37–42.
  10. Chen, Y., & Parrish, T. B. (2009). Caffeine's effects on cerebrovascular reactivity and coupling between cerebral blood flow and oxygen metabolism. NeuroImage, 44(3), 647–652.
  11. Chuah, Y. L., Venkatraman, V., Dinges, D. F., & Chee, M. W. (2006). The neural basis of interindividual variability in inhibitory efficiency after sleep deprivation. Journal of Neuroscience, 26(27), 7156–7162.
  12. Cohen, J. (1988). Statistical power analysis for the behavioral sciences. Lawrence Erlbaum Associates.
  13. Csipo, T., Lipecz, A., Owens, C., Mukli, P., Perry, J. W., Tarantini, S., Balasubramanian, P., Nyúl‐Tóth, Á., Yabluchanska, V., Sorond, F. A., Kellawan, J. M., Purebl, G., Sonntag, W. E., Csiszar, A., Ungvari, Z., & Yabluchanskiy, A. (2021). Sleep deprivation impairs cognitive performance, alters task‐associated cerebral blood flow and decreases cortical neurovascular coupling‐related hemodynamic responses. Scientific Reports, 11(1), 1–13.
  14. Dijk, D.‐J. (2009). Regulation and functional correlates of slow wave sleep. Journal of Clinical Sleep Medicine, 5(2 suppl), S6–S15.
  15. Drummond, S. P., Paulus, M. P., & Tapert, S. F. (2006). Effects of two nights sleep deprivation and two nights recovery sleep on response inhibition. Journal of Sleep Research, 15(3), 261–265.
  16. Durgan, D. J., & Bryan, R. M., Jr. (2012). Cerebrovascular consequences of obstructive sleep apnea. Journal of the American Heart Association., 1(4), e000091.
  17. Field, A. S., Laurienti, P. J., Yen, Y.‐F., Burdette, J. H., & Moody, D. M. (2003). Dietary caffeine consumption and withdrawal: Confounding variables in quantitative cerebral perfusion studies? Radiology, 227(1), 129–135.
  18. Fischer, A. Q., Chaudhary, B. A., Taormina, M. A., & Akhtar, B. (1992). Intracranial hemodynamics in sleep apnea. Chest, 102(5), 1402–1406.
  19. Girouard, H., & Iadecola, C. (2006). Neurovascular coupling in the normal brain and in hypertension, stroke, and Alzheimer disease. Journal of Applied Physiology, 100(1), 328–335.
  20. Kapadia, A., Mirrahimi, A., & Dmytriw, A. A. (2020). Intersection between sleep and neurovascular coupling as the driving pathophysiology of Alzheimer's disease. Medical Hypotheses., 144, 110283.
  21. Karatzi, K., Papamichael, C., Karatzis, E., Papaioannou, T. G., Stamatelopoulos, K., Zakopoulos, N. A., Zampelas, A., & Lekakis, J. (2007). Acute smoke‐induced endothelial dysfunction is more prolonged in smokers than in non‐smokers. International Journal of Cardiology, 120(3), 404–406.
  22. Kocevska, D., Lysen, T. S., Dotinga, A., Koopman‐Verhoeff, M. E., Luijk, M. P., Antypa, N., Biermasz, N. R., Blokstra, A., Brug, J., Burk, W. J., Comijs, H. C., Corpeleijn, E., Dashti, H. S., de Bruin, E. J., de Graaf, R., Derks, I. P. M., Dewald‐Kaufmann, J. F., Elders, P. J. M., Gemke, R. J. B. J., … Tiemeier, H. (2021). Sleep characteristics across the lifespan in 1.1 million people from The Netherlands, United Kingdom and United States: A systematic review and meta‐analysis. Nature Human Behaviour, 5(1), 113–122.
  23. Léger, D., Debellemaniere, E., Rabat, A., Bayon, V., Benchenane, K., & Chennaoui, M. (2018). Slow‐wave sleep: From the cell to the clinic. Sleep Medicine Reviews., 41, 113–132.
  24. Li, J., Vitiello, M. V., & Gooneratne, N. S. (2018). Sleep in normal aging. Sleep Medicine Clinics, 13(1), 1–11.
  25. Lim, Y. Y., Prang, K. H., Cysique, L., Pietrzak, R. H., Snyder, P. J., & Maruff, P. (2009). A method for cross‐cultural adaptation of a verbal memory assessment. Behavior Research Methods., 41(4), 1190–1200.
  26. Lowe, C. J., Safati, A., & Hall, P. A. (2017). The neurocognitive consequences of sleep restriction: A meta‐analytic review. Neuroscience & Biobehavioral Reviews, 80, 586–604.
  27. Maeda, H., Matsumoto, M., Handa, N., Hougaku, H., Ogawa, S., Itoh, T., Tsukamoto, Y., & Kamada, T. (1993). Reactivity of cerebral blood flow to carbon dioxide in various types of ischemic cerebrovascular disease: Evaluation by the transcranial doppler method. Stroke, 24(5), 670–675.
  28. McLellan, T. M., Caldwell, J. A., & Lieberman, H. R. (2016). A review of caffeine's effects on cognitive, physical and occupational performance. Neuroscience and Biobehavioral Reviews, 71, 294–312.
  29. Nurminen, M.‐L., Niittynen, L., Korpela, R., & Vapaatalo, H. (1999). Coffee, caffeine and blood pressure: A critical review. European Journal of Clinical Nutrition., 53(11), 831–839.
  30. Owen, A. M., McMillan, K. M., Laird, A. R., & Bullmore, E. (2005). N‐back working memory paradigm: A meta‐analysis of normative functional neuroimaging studies. Human Brain Mapping., 25(1), 46–59.
  31. Pan, Y., Borragán, G., & Peigneux, P. (2019). Applications of functional near‐infrared spectroscopy in fatigue, sleep deprivation, and social cognition. Brain Topography, 32(6), 998–1012.
  32. Peterson, B. S., Skudlarski, P., Gatenby, J. C., Zhang, H., Anderson, A. W., & Gore, J. C. (1999). An fMRI study of Stroop word‐color interference: Evidence for cingulate subregions subserving multiple distributed attentional systems. Biological Psychiatry, 45(10), 1237–1258.
  33. Poudel, G. R., Innes, C. R., & Jones, R. D. (2012). Cerebral perfusion differences between drowsy and nondrowsy individuals after acute sleep restriction. Sleep, 35(8), 1085–1096.
  34. Reichmuth, K. J., Dopp, J. M., Barczi, S. R., Skatrud, J. B., Wojdyla, P., Hayes, D., Jr., & Morgan, B. J. (2009). Impaired vascular regulation in patients with obstructive sleep apnea: Effects of continuous positive airway pressure treatment. American Journal of Respiratory and Critical Care Medicine., 180(11), 1143–1150.
  35. Rogers, P. J., Heatherley, S. V., Hayward, R. C., Seers, H. E., Hill, J., & Kane, M. (2005). Effects of caffeine and caffeine withdrawal on mood and cognitive performance degraded by sleep restriction. Psychopharmacology, 179(4), 742–752.
  36. Rossa, K. R., Smith, S. S., Allan, A. C., & Sullivan, K. A. (2014). The effects of sleep restriction on executive inhibitory control and affect in young adults. Journal of Adolescent Health, 55(2), 287–292.
  37. Schaedler, T., Santos, J. S., Vincenzi, R. A., Pereira, S. I. R., & Louzada, F. M. (2018). Executive functioning is preserved in healthy young adults under acute sleep restriction. Sleep Science, 11(3), 152–159.
  38. Shabir, O., Berwick, J., & Francis, S. E. (2018). Neurovascular dysfunction in vascular dementia, Alzheimer's and atherosclerosis. BMC Neuroscience, 19(1), 1–16.
  39. Shariffi, B., Lloyd, I. N., Cessac, M. E., Harper, J. L., & Limberg, J. K. (2023). Reproducibility and diurnal variation in middle cerebral artery blood velocity in healthy humans. Experimental Physiology., 108, 692–705.
  40. Shi, L., Chen, S.‐J., Ma, M.‐Y., Bao, Y.‐P., Han, Y., Wang, Y.‐M., Shi, J., Vitiello, M. V., & Lu, L. (2018). Sleep disturbances increase the risk of dementia: A systematic review and meta‐analysis. Sleep Medicine Reviews., 40, 4–16.
  41. Smirl, J. D., Wright, A. D., Bryk, K., & van Donkelaar, P. (2016). Where's Waldo? The utility of a complicated visual search paradigm for transcranial doppler‐based assessments of neurovascular coupling. Journal of Neuroscience Methods., 270, 92–101.
  42. Squair, J. W., Lee, A. H., Sarafis, Z. K., Chan, F., Barak, O. F., Dujic, Z., & Phillips, A. A. (2020). Network analysis identifies consensus physiological measures of neurovascular coupling in humans. Journal of Cerebral Blood Flow & Metabolism., 40(3), 656–666.
  43. Sterniczuk, R., Theou, O., Rusak, B., & Rockwood, K. (2013). Sleep disturbance is associated with sincident dementia and mortality. Current Alzheimer Research., 10(7), 767–775.
  44. Stroop, J. R. (1992). Studies of interference in serial verbal reactions. Journal of Experimental Psychology: General., 121(1), 15–23.
  45. Urbano, F., Roux, F., Schindler, J., & Mohsenin, V. (2008). Impaired cerebral autoregulation in obstructive sleep apnea. Journal of Applied Physiology, 105(6), 1852–1857.
  46. Vidyasagar, R., Greyling, A., Draijer, R., Corfield, D. R., & Parkes, L. M. (2013). The effect of black tea and caffeine on regional cerebral blood flow measured with arterial spin labeling. Journal of Cerebral Blood Flow & Metabolism, 33(6), 963–968.
  47. Willie, C., Colino, F., Bailey, D., Tzeng, Y., Binsted, G., Jones, L., & Ainslie, P. N. (2011). Utility of transcranial doppler ultrasound for the integrative assessment of cerebrovascular function. Journal of Neuroscience Methods., 196(2), 221–237.
  48. Wu, L., Sun, D., & He, Y. (2017). Coffee intake and the incident risk of cognitive disorders: A dose–response meta‐analysis of nine prospective cohort studies. Clinical Nutrition., 36(3), 730–736.
  49. Wu, L., Sun, D., & Tan, Y. (2018). A systematic review and dose‐response meta‐analysis of sleep duration and the occurrence of cognitive disorders. Sleep and Breathing., 22(3), 805–814.
  50. Xu, F., Liu, P., Pekar, J. J., & Lu, H. (2015). Does acute caffeine ingestion alter brain metabolism in young adults? NeuroImage, 110, 39–47.
  51. Zaletel, M., Štrucl, M., Rodi, Z., & Zvan, B. (2004). The relationship between visually evoked cerebral blood flow velocity responses and visual‐evoked potentials. NeuroImage, 22(4), 1784–1789.
  52. Zhu, W. M., Neuhaus, A., Beard, D. J., Sutherland, B. A., & DeLuca, G. C. (2022). Neurovascular coupling mechanisms in health and neurovascular uncoupling in Alzheimer's disease. Brain, 145, 2276–2292.

MeSH Term

Humans
Caffeine
Female
Male
Adult
Sleep Deprivation
Neurovascular Coupling
Ultrasonography, Doppler, Transcranial
Cerebrovascular Circulation
Central Nervous System Stimulants
Blood Flow Velocity
Young Adult

Chemicals

Caffeine
Central Nervous System Stimulants

Word Cloud

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