Mind-body relationships in elite apnea divers during breath holding: A study of autonomic responses to acute hypoxemia

Frontiers in Neuroengineering

Volumn , Issue MARCH 2012, 2012, Pages

  Laurino, Marco ^a,c   Menicucci, Danilo ^b,c   Mastorci, Francesca ^c   Allegrini, Paolo ^b,c   Piarulli, Andrea ^a,b,c   Scilingo, Enzo P ^a   Bedini, Remo ^b,c   Pingitore, Alessandro ^b,c   Passera, Mirko ^b,c   L'Abbate, Antonio ^b,c   Gemignani, Angelo ^a,b,c  

^a UNIVERSITY OF PISA   (Italy)

^b INSTITUTE OF CLINICAL PHYSIOLOGY   (Italy)

^c SCUOLA SUPERIORE SANT ANNA   (Italy)

Author keywords

Apnea; Breath holding; Detrended fluctuation analysis; Entropy; Heart rate variability; Mental control; Skin conductance response

Indexed keywords

ADULT; APNEA; ARTICLE; AUTONOMIC NERVOUS SYSTEM FUNCTION; BREATH HOLDING; CONTROLLED STUDY; DIVER; ELECTROCARDIOGRAM; EMOTION; FACTORIAL ANALYSIS; HEART RATE VARIABILITY; HUMAN; HUMAN EXPERIMENT; HYPOXEMIA; MALE; NORMAL HUMAN; RESPIRATION CONTROL; SKIN CONDUCTANCE; SYMPATHETIC TONE;

SUGARCANE RAMU STUNT DISEASE PHYTOPLASMA;

EID: 84859015817     PISSN: 16626443     EISSN: None     Source Type: Journal    
DOI: 10.3389/fneng.2012.00004     Document Type: Article

References (54)

1. Allegrini, P., Paradisi, P., Menicucci, D., Bedini, R., Gemignani, A., and Fronzoni, L. (2011). Noisy cooperative intermittent processes: from blinking quantum dots to human consciousness. J. Phys. Conf. Ser. 306, 1-10.
2. Alexander, D. M., Trengove, C., Johnston, P., Cooper, T., August, J. P., and Gordon, E. (2005). Separating individual skin conductance responses in a short interstimulus-interval paradigm. J. Neurosci. Methods 146, 116-123.
3. Andersson, J. P., Linr, M. H., Fredsted, A., and Schagatay, E. K. (2004). Cardiovascular and respiratory responses to apneas with and without face immersion in exercising humans. J. Appl. Physiol. 96, 1005-1010.
4. Beckers, F., Ramaekers, D., and Aubert, A. E. (2001). Approximate entropy of heart rate variability: validation of methods and application in heart failure. Cardiovasc. Eng. 1, 177-182.
5. Bernardi, L., Sleight, P., Bandinelli, G., Cencetti, S., Fattorini, L., Wdowczyc-Szulc, J., and Lagi, A. (2001). Effect of rosary prayer and yoga mantras on autonomic cardiovascular rhythms: comparative study. BMJ 323, 1446-1449.
6. Brannan, S., Liotti, M., Egan, G., Shade, R., Madden, L., Robillard, R., Abplanalp, B., Stofer, K., Denton, D., and Fox, P. T. (2001). Neuroimaging of cerebral activations and deactivations associated with hypercapnia and hunger for air. Proc. Natl. Acad. Sci. U.S.A. 98, 2029-2034.
7. Brennan, M., Palaniswami, M., and Kamen, P. (2001). Do existing measures of Poincar plot geometry reflect nonlinear features of heart rate variability? IEEE Trans. Biomed. Eng. 48, 1342-1347.
8. Cabot, J. B. (1990). "Sympathetic preganglionic neurons: cytoarchitecture, ultrastructure, and biophysical properties," in Central Regulation of Autonomic Functions, eds A. D. Loewy and K. M. Spyer (Oxford UK: Oxford university Press), 44-67.
9. Camm, A. J., Malik, M., Bigger, J. T., Breithardt, G., Cerutti, S., Cohen, R. J., Coumel, P., Fallen, E. L., Kennedy, H. L., Kleiger, R. E., Lombardi, F., Malliani, A., Moss, A. J., Rottman, J. N., Schmidt, G., Schwartz, P. J., and Singer, D. H. (1996). Heart rate variability standards of measurement, physiological interpretation, and clinical use. Eur. Heart J. 17, 354-381.
10. Carrillob, E., Moya-Albiola, L., Gonzlez-Bonoa, E., Salvador, A., Ricartea, J., and Gmez-Amorb, J. (2001). Gender differences in cardiovascular and electrodermal responses to public speaking task: the role of anxiety and mood states. Int. J. Psychophysiol. 42, 253-264.
11. Critchley, H. D., Melmed, R. N., Featherstone, E., Mathias, C. J., and Dolan, R. J. (2001). Brain activity during biofeedback relaxation: a functional neuroimaging investigation. Brain 124, 1003-1012.
12. Critchley, H. D., Nagai, Y., Gray, M. A., and Mathias, C. J. (2011). Dissecting axes of autonomic control in humans: insights from neuroimaging. Auton. Neurosci. 161, 34-42.
13. Cysarz, D., and Büssing, A. (2005). Cardiorespiratory synchronization during Zen meditation. Eur. J. Appl. Physiol. 95, 88-95.
14. Cysarz, D., von Bonin, D., Lackner, H., Heusser, P., Moser, M., and Bettermann, H. (2004). Oscillations of heart rate and respiration synchronize during poetry recitation. Am. J. Physiol. Heart Circ. Physiol. 287, 579-587.
15. Davidson, R. J., Kabat-Zinn, J., Schumacher, J., Rosenkranz, M., Muller, D., Santorelli, S. F., Urbanowski, F., Harrington, A., Bonus, K., and Sheridan, J. F. (2003). Alterations in brain and immune function produced by mindfulness meditation. Psychosom. Med. 65, 564-570.
16. Davis, M., and Whalen, P. J. (2001). The amygdala: vigilance and emotion. Mol. Psychiatry 6, 13-34.
17. Delapille, P., Verin, E., Tourny-Chollet, C., and Pasquis, P. (2001). Breath-holding time: effects of non-chemical factors in divers and non-divers. Pflugers Arch. 442, 588-594.
18. Delapille, P., Verin, E., and Tourny-Chollet, C. (2002). Ventilatory adaptations for breath holding in divers. Rev. Mal. Respir. 19, 217-228.
19. Dillbeck, M. C., and Orme-Johnson, D. W. (1987). Physiological differences between tran-scendental meditation and rest. Am. Psychol. 42, 879-881.
20. Eckle, T., Khler, D., Lehmann, R., El Kasmi, K., and Eltzschig, H. K. (2008). Hypoxia-inducible factor-1 is central to cardioprotection: a new paradigm for ischemic preconditioning. Circulation 118, 166-175.
21. Fagius, J., and Sundlf, G. (1986). The diving response in man: effects on sympathetic activity in muscle and skin nerve fascicles. J. Physiol. 337, 429-443.
22. Ferretti, G. (2001). Extreme human breath-hold diving. Eur. J. Appl. Physiol. 84, 254-271.
23. Ferrigno, M., Hickey, D. D., Linr, M. H., and Lundgren, C. E. (1986). Cardiac performance in humans during breath holding. J. Appl. Physiol. 60, 1871-1877.
24. Goldberger, A. L., Amaral, L. A. N., Hausdorff, J. M., Ivanov, P. Ch., Peng, C.-K., and Stanley, H. E. (2002). Fractal dynamics in physiology: alterations with disease and aging. Proc. Natl. Acad. Sci. U.S.A. 99, 2466-2472.
25. Gooden, B. A. (1994). Mechanism of the human diving response. Integr. Physiol. Behav. Sci. 29, 6-16.
26. Grassi, G., Colombo, M., Seravalle, G., Spaziani, D., and Mancia, G. (1998). Dissociation between muscle and skin sympathetic nerve activity in essential hypertension, obesity, and congestive heart failure. Hypertension 31, 64-67.
27. Hagen, T., Taylor, C. T., Lam, F., and Moncada, S. (2003). Redistribution of intracellular oxygen in hypoxia by nitric oxide: effect on HIF1alpha. Science 302, 1975-1978.
28. Hentsch, U., and Ulmer, H. V. (1984). Trainability of underwater breath-holding time. Int. J. Sports Med. 5, 343-347.
29. Heusser, K., Dzamonja, G., Breskovic, T., Steinback, C. D., Diedrich, A., Tank, J., Jordan, J., and Dujic, Z. (2010). Sympathetic and cardiovascular responses to glossopharyngeal insufflation in trained apnea divers. J. Appl. Physiol. 109, 1728-1735.
30. Heusser, K., Dzamonja, G., Tank, J., Palada, I., Valic, Z., Bakovic, D., Obad, A., Ivancev, V., Breskovic, T., Diedrich, A., Joyner, M. J., Luft, F. C., Jordan, J., and Dujic, Z. (2009). Cardiovascular regulation during apnea in elite divers. Hypertension 53, 719-724.
31. Hsin, H., Yang, C., Yeih, D., Shieh, J., and Li, A. (2010). The detrended fluctuation analysis of acute-phase heart-rate variability in acute coronary syndromes A pilot study. Int. J. Cardiol. 140, 252-255.
32. Hurford, W. E., Hong, S. K., Park, Y. S., Ahn, D. W., Shiraki, K., Mohri, M., and Zapol, W. M. (1990). Splenic contraction during breath-hold diving in the Korean ama. J. Appl. Physiol. 69, 932-936.
33. Infante, J. R., Torres-Avisbal, M., Pinel, P., Vallejo, J. A., Peran, F., Gonzalez, F., Contreras, P., Pacheco, C., Roldan, A., and Latre, J. M. (2001). Catecholamine levels in practitioners of the transcendental meditation technique. Physiol. Behav. 72, 141-146.
34. Jänig, W., and Kümmel, H. (1981). Organization of the sympathetic innervation supplying the hairless skin of the cat's paw. J. Auton. Nerv. Syst. 3, 215-230.
35. Jerath, R., Edry, J. W., Barnes, V. A., and Jerath, V. (2006). Physiology of long pranayamic breathing: neural respiratory elements may provide a mechanism that explains how slow deep breathing shifts the autonomic nervous system. Med. Hypotheses 67, 566-571.
36. Jevning, R., Wallace, R. K., and Beidebach, M. (1992). The physiology of meditation: a review. A wakeful hypometabolic integrated response. Neurosci. Biobehav. Rev. 16, 415-424.
37. Kantz, H., and Schreiber, T. (2004). Nonlinear Time Series Analysis. (Cambridge UK: Cambridge University Press).
38. Lee, S. H., Wolf, P. L., Escudero, R., Deutsch, R., Jamieson, S. W., and Thistlethwaite, P. A. (2000). Early expression of angiogenesis factors in acute myocardial ischemia and infarction. N. Engl. J. Med. 342, 626-633.
39. Lin, Y. C., Shida, K. K., and Hong, S. K. (1983). Effects of hypercapnia, hypoxia, and rebreathing on heart rate response during apnea. J. Appl. Physiol. 54, 166-171.
40. Lindholm, P., and Gennser, M. (2005). Aggravated hypoxia during breath-holds after prolonged exercise. Eur. J. Appl. Physiol. 93, 701-707.
41. Liotti, M., Brannan, S., Egan, G., Shade, R., Madden, L., Abplanalp, B., Robillard, R., Lancaster, J., Zamarripa, F. E., Fox, P. T., and Denton, D. (2001). Brain responses associated with consciousness of breathlessness (air hunger). Proc. Natl. Acad. Sci. U.S.A. 98, 2035-2040.
42. MacLean, C. R., Walton, K. G., Wenneberg, S. R., Levitsky, D. K., Mandarino, J. P., Waziri, R., Hillis, S. L., and Schneider, R. H. (1997). Effects of the transcendental meditation program on adaptive mechanisms: changes in hormone levels and responses to stress after 4 months of practice. Psychoneuroendocrinology 22, 277-295.
43. Nishiyama, T., Sugenoya, J., Matsumoto, T., Iwase, S., and Mano, T. (2001). Irregular activation of individual sweat glands in human sole observed by a videomicroscopy. Auton. Neurosci. 88, 117-126.
44. Perini, R., Tironi, A., Gheza, A., Butti, F., Moia, C., and Ferretti, G. (2008). Heart rate and blood pressure time courses during prolonged dry apnoea in breath-hold divers. Eur. J. Appl. Physiol. 104, 1-7.
45. Pincus, S. M. (1991). Approximate entropy as a measure of system complexity. Proc. Natl. Acad. Sci. U.S.A. 88, 2297-2301.
46. Pingitore, A., Gemignani, A., Menicucci, D., Di Bella, G., De Marchi, D., Passera, M., Bedini, R., Ghelarducci, B., and L'Abbate, A. (2008). Cardiovascular response to acute hypoxemia induced by prolonged breath holding in air. Am. J. Physiol. Heart Circ. Physiol. 294, H449-H455.
47. Perkiomaki, J. S., Makikallio, T. H., and Huikuri, H. V. (2000). Nonlinear analysis of heart rate variability: fractal and complexity measures of heart rate behavior. Ann. Noninvasive Electrocardiol. 5, 179-187.
48. Schagatay, E., Andersson, J. P., Halln, M., and Plsson, B. (2001). Selected contribution: role of spleen emptying in prolonging apneas in humans. J. Appl. Physiol. 90, 1623-1629.
49. Sequeira, H., Ba-M'Hamed, S., and Roy, J. C. (1995). Fronto-parietal control of electrodermal activity in the cat. J. Auton. Nerv. syst. 53, 103-114.
50. Sequeira, H., Hot, P., Silvert, L., and Delplanque, S. (2009). Electrical autonomic correlates of emotion. Int. J. Psychophysiol. 71, 50-56.
51. Sobolewski, A., Holt, E., Kublik, E., and Wrbel, A. (2011). Impact of meditation on emotional processing-A visual ERP study. Neurosci. Res. 1, 44-48.
52. Strogatz, S. (1994). Nonlinear Dynamics and Chaos: With Applications to Physics, Biology, Chemistry, and Engineering. (Cambridge MA, USA: Perseus Books).
53. Wenger, M. A., and Bagchi, B. K. (1961). Studies of autonomic functions in practitioners of Yoga in India. Behav. Sci. 6, 1312-1323.
54. Wenneberg, S. R., Schneider, R. H., Walton, K. G., MacLean, C. R., Levitsky, D. K., Salerno, J. W., Wallace, R. K., Mandarino, J. V., Rainforth, M. V., and Waziri, R. (1997). A controlled study of the effects of the transcendental meditation program on cardiovascular reactivity and ambulatory blood pressure. Int. J. Neurosci. 89, 15-28.