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Brain Imaging and Behavior

, Volume 11, Issue 2, pp 461–472 | Cite as

Prefrontal hemodynamic after-effects caused by rebreathing may predict affective states – A multimodal functional near-infrared spectroscopy study

Original Research

Abstract

Brain activity has been shown to be influenced by respiratory behavior. Here, we evaluated whether respiration-induced hypo- or hypercapnia may support differentiation between physiological versus pathological respiratory behavior. In particular, we investigated whether systemic physiological measures could predict the brain’s time-frequency hemodynamics after three respiratory challenges (i.e., breath-holding, rebreathing, and hyperventilation) compared to resting-state. Prefrontal hemodynamics were assessed in healthy subjects (N = 27) using functional near-infrared spectroscopy (fNIRS). Systemic physiological measures were assessed in form of heart rate, partial end-tidal carbon dioxide, respiration rate, and saturation of peripheral oxygen. Time-frequency dynamics were quantified using the wavelet transform coherence (i.e., defined here as cortical-systemic coherence). We found that the three respiratory challenges modulated cortical-systemic coherence differently: (1) After rebreathing, cortical-systemic coherence could be predicted from the amplitude of the heart rate (strong negative correlation). (2) After breath-holding, the same observation was made (moderate negative correlation). (3) After hyperventilation, no significant effect was observed. (4) These effects were found only in the frequency range of very low-frequency oscillations. The presented findings highlight a distinct role of rebreathing in predicting cortical-systemic coupling based on heart rate changes, which may represents a measure of affective states in the brain. The applied multimodal assessment of hemodynamic and systemic physiological measures during respiratory challenges may therefore have potential applications in the differentiation between physiological and pathological respiratory behavior.

Keywords

Respiratory challenge Time-frequency dynamics Cortical-systemic coherence Functional near-infrared spectroscopy Heart rate Partial pressure of carbon dioxide 

Notes

Compliance with ethical standards

This work was funded by the academic career program Filling the Gap (Grant number FTG-1415-007), University of Zurich.

Conflict of Interest

Author LH declares that she has no conflict of interest. Author FS declares that he has no conflict of interest. Author ES declares that he has no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the ethics committee of the Canton Zurich and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

References

  1. Abrams, K., Rassovsky, Y., & Kushner, M. G. (2006). Evidence for respiratory and nonrespiratory subtypes in panic disorder. Depression and Anxiety, 23, 474–481.CrossRefPubMedGoogle Scholar
  2. Adhikari, A., Topiwala, M. A., & Gordon, J. A. (2010). Synchronized activity between the ventral hippocampus and the medial prefrontal cortex during anxiety. Neuron, 65, 257.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Alexopoulos, D., Christodoulou, J., Toulgaridis, T., Sitafidis, G., Klinaki, A., & Vagenakis, A. (1995). Hemodynamic response to hyperventilation test in healthy volunteers. Clinical Cardiology, 18, 636–641.CrossRefPubMedGoogle Scholar
  4. Birn, R. M., Smith, M. A., Jones, T. B., & Bandettini, P. A. (2008). The respiration response function: the temporal dynamics of fMRI signal fluctuations related to changes in respiration. NeuroImage, 40, 644–654.CrossRefPubMedGoogle Scholar
  5. Birn, R. M., Murphy, K., Handwerker, D. A., & Bandettini, P. A. (2009). fMRI in the presence of task-correlated breathing variations. Brain Body Med, 47, 1092–1104.Google Scholar
  6. Boas, D. A., Dale, A. M., & Franceschini, M. A. (2004). Diffuse optical imaging of brain activation: approaches to optimizing image sensitivity, resolution, and accuracy. NeuroImage, 23, S275–S288.CrossRefPubMedGoogle Scholar
  7. Bright, M. G., & Murphy, K. (2013). Reliable quantification of BOLD fMRI cerebrovascular reactivity despite poor breath-hold performance. NeuroImage, 83, 559–568.CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bright, M. G., & Murphy, K. (2015). Is fMRI “noise” really noise? Resting state nuisance regressors remove variance with network structure. NeuroImage, 114, 158–169.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Chai, X. J., Castañón, A. N., Öngür, D., & Whitfield-Gabrieli, S. (2012). Anticorrelations in resting state networks without global signal regression. NeuroImage, 59, 1420–1428.CrossRefPubMedGoogle Scholar
  10. Chang, C., & Glover, G. H. (2009). Effects of model-based physiological noise correction on default mode network anti-correlations and correlations. NeuroImage, 47, 1448–1459.CrossRefPubMedPubMedCentralGoogle Scholar
  11. Coryell, W., Noyes, R., & Clancy, J. (1982). Excess mortality in panic disorder. A comparison with primary unipolar depression. Archives of General Psychiatry, 39, 701–703.CrossRefPubMedGoogle Scholar
  12. Coryell, W., Noyes, R., & House J (1986). Mortality among outpatients with anxiety disorders. The American Journal of Psychiatry, 143, 508–510.CrossRefPubMedGoogle Scholar
  13. Denollet, J., & Brutsaert, D. L. (1998). Personality, disease severity, and the risk of long-term cardiac events in patients with a decreased ejection fraction after myocardial infarction. Circulation, 97, 167–173.CrossRefPubMedGoogle Scholar
  14. Eke, M., & McNally, R. J. (1996). Anxiety sensitivity, suffocation fear, trait anxiety, and breath-holding duration as predictors of response to carbon dioxide challenge. Behaviour Research and Therapy, 34, 603–607.CrossRefPubMedGoogle Scholar
  15. Fox, M., Zhang, D., Snyder, A., & Raichle, M. (2009). The global signal and observed anticorrelated Resting state brain networks. Journal of Neurophysiology, 101, 3270–3283.CrossRefPubMedPubMedCentralGoogle Scholar
  16. Funane, T., Atsumori, H., Katura, T., Obata, A. N., Sato, H., Tanikawa, Y., Okada, E., & Kiguchi, M. (2014). Quantitative evaluation of deep and shallow tissue layers’ contribution to fNIRS signal using multi-distance optodes and independent component analysis. Neuroimage, 85, 150–165.Google Scholar
  17. Gagnon, L., Yücel, M. A., Dehaes, M., Cooper, R. J., Perdue, K. L., Selb, J., Huppert, T. J., Hoge, R. D., & Boas, D. A. (2012). Quantification of the cortical contribution to the NIRS signal over the motor cortex using concurrent NIRS-fMRI measurements. NeuroImage, 59, 3933–3940.CrossRefPubMedGoogle Scholar
  18. Germon, T. J., Evans, P. D., Barnett, N. J., Wall, P., Manara, A. R., & Nelson, R. J. (1999). Cerebral near infrared spectroscopy: emitter-detector separation must be increased. British Journal of Anaesthesia, 82, 831–837.CrossRefPubMedGoogle Scholar
  19. Golestani, A. M., Chang, C., Kwinta, J. B., Khatamian, Y. B., & Jean Chen, J. (2015). 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. NeuroImage, 104, 266–277.CrossRefPubMedGoogle Scholar
  20. Gorman, J. M., Browne, S. T., Papp, L. A., Martinez, J., Welkowitz, L., Coplan, J. D., Goetz, R. R., Kent, J., & Klein, D. F. (1997). Effect of Antipanic Treatment on Response to Carbon Dioxide. Biological Psychiatry, 42, 982–991.CrossRefPubMedGoogle Scholar
  21. Grinsted, A., Moore, J., & Jevrejeva, S. (2004). Application of the cross wavelet transform and wavelet coherence to geophysical time series. Nonlinear Processes in Geophysics, 11, 561–566.CrossRefGoogle Scholar
  22. Grubb, R., Raichle, M., Eichling, J., & Ter-Pogossian, M. (1974). The effects of changes in PaCO2 cerebral blood volume, blood flow, and vascular mean transit time. Stroke, 5, 630–639.CrossRefPubMedGoogle Scholar
  23. Haines, A. P., Imeson, J. D., & Meade, T. W. (1987). Phobic anxiety and ischaemic heart disease. BMJ, 295, 297–299.CrossRefPubMedPubMedCentralGoogle Scholar
  24. Haines, A., Cooper, J., & Meade, T. W. (2001). Psychological characteristics and fatal ischaemic heart disease. Heart, 85, 385–389.CrossRefPubMedPubMedCentralGoogle Scholar
  25. Holper, L., Wolf, M., & Tobler, P. N. (2014a). Comparison of functional near-infrared spectroscopy and electrodermal activity in assessing objective versus subjective risk during risky financial decisions. NeuroImage, 84, 833–842.CrossRefPubMedGoogle Scholar
  26. Holper, L., Scholkmann, F., & Wolf, M. (2014b). The relationship between sympathetic nervous activity and cerebral Hemodynamics and oxygenation: A study using skin conductance measurement and functional near-infrared spectroscopy. Behavioural Brain Research, 270, 95–107.CrossRefPubMedGoogle Scholar
  27. Holper L, Scholkmann F, Seifritz E (2015). Time-frequency dynamics of the sum of intra- and extracerebral hemodynamic functional connectivity during resting-state and respiratory challenges assessed by multimodal functional near-infrared spectroscopy. NeuroImage, 120, 481–492.Google Scholar
  28. Homma, I., & Masaoka, Y. (2008). Breathing rhythms and emotions. Experimental Physiology, 93, 1011–1021.CrossRefPubMedGoogle Scholar
  29. Kastrup, A., Li, T.-Q., Takahashi, A., Glover, G. H., & Moseley, M. E. (1998). Functional magnetic resonance imaging of regional cerebral blood oxygenation changes during breath holding. Stroke, 29, 2641–2645.CrossRefPubMedGoogle Scholar
  30. Kastrup, A., Krüger, G., Glover, G. H., & Moseley, M. E. (1999). Assessment of cerebral oxidative metabolism with breath holding and fMRI. Magnetic Resonance in Medicine, 42, 608–611.CrossRefPubMedGoogle Scholar
  31. Kawachi, I., Colditz, G. A., Ascherio, A., Rimm, E. B., Giovannucci, E., Stampfer, M. J., & Willett, W. C. (1994a). Prospective study of phobic anxiety and risk of coronary heart disease in men. Circulation, 89, 1992–1997.CrossRefPubMedGoogle Scholar
  32. Kawachi, I., Sparrow, D., Vokonas, P. S., & Weiss, S. T. (1994b). Symptoms of anxiety and risk of coronary heart disease. The Normative Aging Study. Circulation, 90, 2225–2229.PubMedGoogle Scholar
  33. Keller, C. J., Bickel, S., Honey, C. J., Groppe, D. M., Entz, L., Craddock, R. C., Lado, F. A., Kelly, C., Milham, M., & Mehta, A. D. (2013). Neurophysiological investigation of spontaneous correlated and anticorrelated fluctuations of the BOLD signal. The Journal of Neuroscience, 33, 6333–6342.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Kim, D.-K., Lee, K.-M., Kim, J., Whang, M.-C., & Kang, S. W. (2013a). Dynamic correlations between heart and brain rhythm during autogenic meditation. Frontiers in Human Neuroscience, 7, 414.PubMedPubMedCentralGoogle Scholar
  35. Kim, D.-K., Rhee, J.-H., & Kang, S. W. (2013b). Reorganization of the brain and heart rhythm during autogenic meditation. Frontiers in Integrative Neuroscience, 7, 109.Google Scholar
  36. Kirilina, E., Jelzow, A., Heine, A., Niessing, M., Wabnitz, H., Brühl, R., Ittermann, B., Jacobs, A., & Tachtsidis, I. (2012a). The physiological origin of task-evoked systemic artefacts in functional near infrared spectroscopy. NeuroImage, 61, 70–81.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Kirilina, E., Jelzow, A., Heine, A., Niessing, M., Wabnitz, H., Brühl, R., Ittermann, B., Jacobs, A. M., & Tachtsidis, I. (2012b). The physiological origin of task-evoked systemic artefacts in functional near infrared spectroscopy. NeuroImage, 61, 70–81.CrossRefPubMedPubMedCentralGoogle Scholar
  38. Kiviniemi V, Remes J, Starck T, Nikkinen J, Haapea M, Silven O, Tervonen O (2009): Mapping Transient Hyperventilation Induced Alterations with Estimates of the Multi-Scale Dynamics of BOLD Signal. Front Neuroinformatics 3.Google Scholar
  39. Kox, M., van Eijk, L. T., Zwaag, J., van den Wildenberg, J., Sweep, F. C. G. J., van der Hoeven, J. G., & Pickkers, P. (2014). Voluntary activation of the sympathetic nervous system and attenuation of the innate immune response in humans. Proceedings of the National Academy of Sciences, 111, 7379–7384.CrossRefGoogle Scholar
  40. Laszlo, G., Clark, T. J. H., Pope, H., & Campbell, E. J. M. (1971). Differences between alveolar and arterial pCO2 during rebreathing experiments in resting human subjects. Respiration Physiology, 12, 36–52.CrossRefPubMedGoogle Scholar
  41. Lemaître, F., Bernier, F., Petit, I., Renard, N., Gardette, B., & Joulia, F. (2005). Heart rate responses during a breath-holding competition in well-trained divers. International Journal of Sports Medicine, 26, 409–413.CrossRefPubMedGoogle Scholar
  42. Lesting, J., Narayanan, R., Kluge, C., Sangha, S., Seidenbecher, T., & Pape (2011). Patterns of coupled theta activity in amygdala-hippocampal-prefrontal cortical circuits during fear extinction. PloS One, 6, e21714.CrossRefPubMedPubMedCentralGoogle Scholar
  43. Likhtik, E., Stujenske, J. M., A Topiwala, M., AZ, H., & JA, G. (2014). Prefrontal entrainment of amygdala activity signals safety in learned fear and innate anxiety. Nature Neuroscience, 17, 106–113.CrossRefPubMedGoogle Scholar
  44. Maddock, R. J., & Carter, C. S. (1991). Hyperventilation-induced panic attacks in panic disorder with agoraphobia. Biological Psychiatry, 29, 843–854.CrossRefPubMedGoogle Scholar
  45. Mastrovito, D. (2013). Interactions between resting-state and task-evoked brain activity suggest a different approach to fMRI analysis. The Journal of Neuroscience, 33, 12912–12914.CrossRefPubMedGoogle Scholar
  46. Nardi, A. E., Valença, A. M., Lopes, F. L., Nascimento, I., Mezzasalma, M. A., & Zin, W. A. (2004). Clinical features of panic patients sensitive to hyperventilation or breath-holding methods for inducing panic attacks. Brazilian Journal of Medical and Biological Research, 37, 251–257.CrossRefPubMedGoogle Scholar
  47. Nardi, A. E., Valença, A. M., Mezzasalma, M. A., Levy, S. P., Lopes, F. L., Nascimento, I., Freire, R. C., Veras, A. B., & Zin, W. A. (2006). Comparison between hyperventilation and breath-holding in panic disorder: patients responsive and non-responsive to both tests. Psychiatry Research, 142, 201–208.CrossRefPubMedGoogle Scholar
  48. Nasrallah, F. A., Yeow, L. Y., Biswal, B., & Chuang, K.-H. (2015). Dependence of BOLD signal fluctuation on arterial blood CO2 and O2: implication for resting-state functional connectivity. NeuroImage, 117, 29–39.CrossRefPubMedGoogle Scholar
  49. Nikulin, V. V., Fedele, T., Mehnert, J., Lipp, A., Noack, C., Steinbrink, J., & Curio, G. (2014). Monochromatic Ultra-slow (~ 0.1 Hz) oscillations in the human electroencephalogram and their relation to Hemodynamics. NeuroImage, 97, 71–80.CrossRefPubMedGoogle Scholar
  50. Obrig, H., Neufang, M., Wenzel, R., Kohl, M., Steinbrink, J., Einhäupl, K., & Villringer, A. (2000). Spontaneous low frequency oscillations of cerebral hemodynamics and metabolism in human adults. NeuroImage, 12, 623–639.CrossRefPubMedGoogle Scholar
  51. Putman, P. (2011). Resting state EEG delta–beta coherence in relation to anxiety, behavioral inhibition, and selective attentional processing of threatening stimuli. International Journal of Psychophysiology, 80, 63–68.CrossRefPubMedGoogle Scholar
  52. Rapee, R. M., Brown, T. A., Antony, M. M., & Barlow, D. H. (1992). Response to hyperventilation and inhalation of 5.5 % carbon dioxide-enriched air across the DSM-III—R anxiety disorders. Journal of Abnormal Psychology, 101, 538–552.CrossRefPubMedGoogle Scholar
  53. Rassovsky, Y., Kushner, M. G., Schwarze, N. J., & Wangensteen, O. D. (2000). Psychological and physiological predictors of response to carbon dioxide challenge in individuals with panic disorder. Journal of Abnormal Psychology, 109, 616–623.CrossRefPubMedGoogle Scholar
  54. Roth WT, Wilhelm FH, Trabert W (1998): Voluntary Breath Holding in Panic and Generalized Anxiety Disorders. Psychosomatic Medicine, 60, 671–679.Google Scholar
  55. Scholkmann, F., Gerber, U., Wolf, M., & Wolf, U. (2013a). End-tidal CO2: An important parameter for a correct interpretation in functional brain studies using speech tasks. NeuroImage, 66, 71–79.CrossRefPubMedGoogle Scholar
  56. Scholkmann, F., Wolf, M., & Wolf, U. (2013b). The effect of inner speech on arterial CO2, cerebral hemodynamics and oxygenation - A functional NIRS study. advances in experimental medicine and biology. Advances in Experimental Medicine and Biology, 789, 81–87.Google Scholar
  57. Scholkmann, F., Kleiser, S., Metz, A. J., Zimmermann, R., Mata Pavia, J., Wolf, U., & Wolf, M. (2014a). A review on continuous wave functional near-infrared spectroscopy and imaging instrumentation and methodology. NeuroImage, 85, 6–27. Google Scholar
  58. Scholkmann, F., Klein, S., Gerber, U., Wolf, M., & Wolf, U. (2014b). Cerebral hemodynamic and oxygenation changes induced by inner and heard speech: a study combining functional near-infrared spectroscopy and capnography. Journal of Biomedical Optics, 19, 017002.CrossRefGoogle Scholar
  59. Soladoye A, Owoyele B, Olatunji L, Adelusi S (2003): Cardiovascular responses to breath-holding with or without face immersion in young adults. Bioscience Research Communications, 15, 59–63.Google Scholar
  60. Stäubli, M., Vogel, F., Bärtsch, P., Flückiger, G., & Ziegler, W. H. (1994). Hyperventilation-induced changes of blood cell counts depend on hypocapnia. European Journal of Applied Physiology, 69, 402–407.CrossRefGoogle Scholar
  61. Sullivan, G. M., Kent, J. M., Kleber, M., Martinez, J. M., Yeragani, V. K., & Gorman, J. M. (2004). Effects of hyperventilation on heart rate and QT variability in panic disorder pre- and post-treatment. Psychiatry Research, 125, 29–39.CrossRefPubMedGoogle Scholar
  62. Tachtsidis, I., & Papaioannou, A. (2013). Investigation of frontal lobe activation with fNIRS and systemic changes during video gaming. Advances in Experimental Medicine and Biology, 789, 89–95.CrossRefPubMedPubMedCentralGoogle Scholar
  63. Tachtsidis, I., Leung, T., Devoto, L., Delpy, D., & Elwell, C. (2008a). Measurement of frontal lobe functional activation and related systemic effects: a near-infrared spectroscopy investigation. Advances in Experimental Medicine and Biology, 614, 397–403.CrossRefPubMedGoogle Scholar
  64. Tachtsidis, I., Leung, T., Tisdall, M., Devendra, P., Smith, M., Delpy, D., & Elwell, C. (2008b). Investigation of frontal cortex, motor cortex and systemic haemodynamic changes during anagram solving. Advances in Experimental Medicine and Biology, 614, 21–28.Google Scholar
  65. Tachtsidis, I., Leung, T., Chopra, A., Koh, P., Reid, C., & Elwell, C. (2009a). False positives in functional nearinfrared topography. Advances in Experimental Medicine and Biology, 645, 307–314.CrossRefPubMedGoogle Scholar
  66. Tachtsidis, I., Leung, T., Chopra, A., Koh, P., Reid, C., & Elwell, C. (2009b). False positives In functional nearinfrared topography. Advances in Experimental Medicine and Biology, 645, 307–314.Google Scholar
  67. Takahashi, T., Takikawa, Y., Kawagoe, R., Shibuya, S., Iwano, T., & Kitazawa, S. (2011). Influence of skin blood flow on near-infrared spectroscopy signals measured on the forehead during a verbal fluency task. NeuroImage, 57, 991–1002.Google Scholar
  68. Thomas, S. A., Friedmann, E., Wimbush, F., & Schron, E. (1997). Psychological factors and survival in the cardiac arrhythmia suppression trial (CAST): a reexamination.  American Journal of Critical Care, 6, 116–126.Google Scholar
  69. Thomason, M. E., Burrows, B. E., Gabrieli, J. D. E., & Glover, G. H. (2005). Breath holding reveals differences in fMRI BOLD signal in children and adults. NeuroImage, 25, 824–837.CrossRefPubMedGoogle Scholar
  70. Tong, Y., Hocke, L. M., Fan, X., Janes, A., & Frederick, B. (2015). Can apparent resting state connectivity arise from systemic fluctuations? Frontiers in Human Neuroscience, 9.Google Scholar
  71. Torrence, C., & Compo, G. (1998). A practical guide to wavelet analysis. Bulletin of the American Meteorological Society, 79, 61–78.CrossRefGoogle Scholar
  72. Trajkovic I, Scholkmann F, Wolf M (2011): Estimating and validating the interbeat intervals of the heart using near-infrared spectroscopy on the human forehead. Journal of Biomedical Optics, 16, 087002. Google Scholar
  73. van den Hout, M., Boek, C., van der Molen, G., Jansen, A., & Griez, E. (1988). Rebreathing to cope with hyperventilation: experimental tests of the paper bag method. Journal of Behavioral Medicine, 11, 303–310.CrossRefPubMedGoogle Scholar
  74. Weissman, M. M., Markowitz, J. S., Ouellette, R., Greenwald, S., & Kahn, J. P. (1990). Panic disorder and cardiovascular/cerebrovascular problems: results from a community survey. The American Journal of Psychiatry, 147, 1504–1508.CrossRefPubMedGoogle Scholar
  75. Woods, S., Charney, D., Loke, J., Goodman, W., Redmond, D., & Heninger, G. (1986). Carbon dioxide sensitivity in panic anxiety: ventilatory and anxiogenic response to carbon dioxide in healthy subjects and patients with panic anxiety before and after alprazolam treatment. Archives of General Psychiatry, 43, 900–909.CrossRefPubMedGoogle Scholar
  76. Xia, M., Wang, J., & He, Y. (2013). BrainNet viewer: A network visualization tool for human brain connectomics. PloS One, 8, e68910.CrossRefPubMedPubMedCentralGoogle Scholar
  77. Xu Y, Graber H, Barbour R (2014): nirsLAB: A Computing Environment for fNIRS Neuroimaging Data Analysis. Biomedical Optics 2014, OSA Technical Digest (online) (Optical Society of America, 2014), paper BM3A.1Google Scholar
  78. Zhao, H., Tanikawa, Y., Gao, F., Onodera, Y., Sassaroli, A., Tanaka, K., & Yamada, Y. (2002). Maps of optical differential pathlength factor of human adult forehead, somatosensory motor and occipital regions at multi-wavelengths in NIR. Physics in Medicine and Biology, 47, 2075–2093.CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Psychiatry, Psychotherapy, and PsychosomaticsPsychiatric Hospital, University of ZurichZürichSwitzerland
  2. 2.Biomedical Optics Research Laboratory, Department of Neonatology, University Hospital ZurichUniversity of ZurichZurichSwitzerland

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