Comprehensive Psychiatry
Volume 48, Issue 2 , Pages 103-112 , March 2007

Anxiety, respiration, and cerebral blood flow: implications for functional brain imaging

  • Nicholas D. Giardino

      Affiliations

    • Department of Radiology, University of Washington School of Medicine, Seattle, WA 98105, USA
    • ,
  • Seth D. Friedman

      Affiliations

    • Department of Radiology, University of Washington School of Medicine, Seattle, WA 98105, USA
    • ,
  • Stephen R. Dager

      Affiliations

    • Department of Radiology, University of Washington School of Medicine, Seattle, WA 98105, USA
    • Department of Psychiatry, University of Washington School of Medicine, Seattle, WA 98105, USA
    • Department of Bioengineering, University of Washington School of Medicine, Seattle, WA 98105, USA
    • Corresponding Author InformationCorresponding author. Neuroimaging Research Group, Department of Radiology, University of Washington, Seattle, WA 98105, USA. Tel.: +1 206 616 1558; fax: +1 206 616 7791.

References 

  1. Posse S, Muller-Gartner HW, Dager SR. Functional magnetic resonance studies of brain activation. Semin Clin Neuropsychiatry. 1996;1(1):76–88
  2. Ogawa S, Lee TM, Kay AR, Tank DW. Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci U S A. 1990;87(24):9868–9872
  3. Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC, Raichle ME. The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci U S A. 2005;102(27):9673–9678
  4. Stark CE, Squire LR. When zero is not zero: the problem of ambiguous baseline conditions in fMRI. Proc Natl Acad Sci U S A. 2001;98(22):12760–12766
  5. Posse S, Binkofski F, Schneider F, Gembris D, Frings W, Habel U, et al. A new approach to measure single-event related brain activity using real-time fMRI: feasibility of sensory, motor, and higher cognitive tasks. Hum Brain Mapp. 2001;12(1):25–41
  6. Fujita N, Shinohara M, Tanaka H, Yutani K, Nakamura H, Murase K. Quantitative mapping of cerebral deoxyhemoglobin content using MR imaging. NeuroImage. 2003;20(4):2071–2083
  7. Posse S, Wiese S, Gembris D, Mathiak K, Kessler C, Grosse-Ruyken ML, et al. Enhancement of BOLD-contrast sensitivity by single-shot multi-echo functional MR imaging. Magn Reson Med. 1999;42(1):87–97
  8. Cohen ER, Rostrup E, Sidaros K, Lund TE, Paulson OB, Ugurbil K, et al. Hypercapnic normalization of BOLD fMRI: comparison across field strengths and pulse sequences. NeuroImage. 2004;23(2):613–624
  9. Bonvento G, Herard AS, Voutsinos-Porche B. The astrocyte-neuron lactate shuttle: a debated but still valuable hypothesis for brain imaging. J Cereb Blood Flow Metab. 2005;25:1394–1399
  10. Logothetis NK, Wandell BA. Interpreting the BOLD signal. Annu Rev Physiol. 2004;66:735–769
  11. Hoge RD, Franceschini MA, Covolan RJ, Huppert T, Mandeville JB, Boas DA. Simultaneous recording of task-induced changes in blood oxygenation, volume, and flow using diffuse optical imaging and arterial spin-labeling MRI. NeuroImage. 2005;25(3):701–707
  12. Lu H, van Zijl PC. Experimental measurement of extravascular parenchymal BOLD effects and tissue oxygen extraction fractions using multi-echo VASO fMRI at 1.5 and 3.0 T. Magn Reson Med. 2005;53(4):808–816
  13. Lai S, Hopkins AL, Haacke EM, Li D, Wasserman BA, Buckley P, et al. Identification of vascular structures as a major source of signal contrast in high resolution 2D and 3D functional activation imaging of the motor cortex at 1.5 T: preliminary results. Magn Reson Med. 1993;30(3):387–392
  14. Saad ZS, Ropella KM, DeYoe EA, Bandettini PA. The spatial extent of the BOLD response. NeuroImage. 2003;19(1):132–144
  15. Sheth SA, Nemoto M, Guiou MW, Walker MA, Toga AW. Spatiotemporal evolution of functional hemodynamic changes and their relationship to neuronal activity. J Cereb Blood Flow Metab. 2005;25(7):830–841
  16. Ross MH, Yurgelun-Todd DA, Renshaw PF, Maas LC, Mendelson JH, Mello NK, et al. Age-related reduction in functional MRI response to photic stimulation. Neurology. 1997;48(1):173–176
  17. Levin JM, Ross MH, Mendelson JH, Mello NK, Cohen BM, Renshaw PF. Sex differences in blood-oxygenation-level–dependent functional MRI with primary visual stimulation. Am J Psychiatry. 1998;155(3):434–436
  18. Levin JM, Frederick Bde B, Ross MH, Fox JF, von Rosenberg HL, Kaufman MJ, et al. Influence of baseline hematocrit and hemodilution on BOLD fMRI activation. Magn Reson Imaging. 2001;19(8):1055–1062
  19. Rasgon NL, Thomas MA, Guze BH, Fairbanks LA, Yue K, Curran JG, et al. Menstrual cycle–related brain metabolite changes using 1H magnetic resonance spectroscopy in premenopausal women: a pilot study. Psychiatry Res. 2001;106(1):47–57
  20. Epperson CN, Haga K, Mason GF, Sellers E, Gueorguieva R, Zhang W, et al. Cortical gamma-aminobutyric acid levels across the menstrual cycle in healthy women and those with premenstrual dysphoric disorder: a proton magnetic resonance spectroscopy study. Arch Gen Psychiatry. 2002;59(9):851–858
  21. Dager SR, Layton ME, Strauss W, Richards TL, Heide A, Friedman SD, et al. Human brain metabolic response to caffeine and the effects of tolerance. Am J Psychiatry. 1999;156(2):229–237
  22. Laurienti PJ, Field AS, Burdette JH, Maldjian JA, Yen YF, Moody DM. Dietary caffeine consumption modulates fMRI measures. NeuroImage. 2002;17(2):751–757
  23. Stein EA, Pankiewicz J, Harsch HH, Cho JK, Fuller SA, Hoffmann RG, et al. Nicotine-induced limbic cortical activation in the human brain: a functional MRI study. Am J Psychiatry. 1998;155(8):1009–1015
  24. Poulin MJ, Liang PJ, Robbins PA. Dynamics of the cerebral blood flow response to step changes in end-tidal Pco2 and Po2 in humans. J Appl Physiol. 1996;81(3):1084–1095
  25. Ide K, Eliasziw M, Poulin MJ. The relationship between middle cerebral artery blood velocity and end-tidal Pco2 in the hypocapnic-hypercapnic range in humans. J Appl Physiol. 2003;95:129–137
  26. Ball S, Shekhar A. Basilar artery response to hyperventilation in panic disorder. Am J Psychiatry. 1997;154(11):1603–1604
  27. Deckersbach T, Dougherty DD, Rauch SL. Functional imaging of mood and anxiety disorders. J Neuroimaging. 2006;16(1):1–10
  28. Bremner JD. Brain imaging in anxiety disorders. Expert Rev Neurotherapeutic. 2004;4(2):275–284
  29. Liberzon I, Phan L. Brain-imaging studies of posttraumatic stress disorder. CNS Spectr. 2003;8:614–650
  30. Phan KL, Wager TD, Taylor SF, Liberzon I. Functional neuroimaging studies of human emotions. CNS Spectr. 2004;9(4):258–266
  31. Rauch SL, Shin LM, Wright CI. Neuroimaging studies of amygdala function in anxiety disorders. Ann NY Acad Sci. 2003;985:389–410
  32. Gorman JM, Kent JM, Sullivan GM, Coplan JD. Neuroanatomical hypothesis of panic disorder, revised. Am J Psychiatry. 2000;157(4):493–505
  33. De Cristofaro MT, Sessarego A, Pupi A, Biondi F, Faravelli C. Brain perfusion abnormalities in drug-naive, lactate-sensitive panic patients: a SPECT study. Biol Psychiatry. 1993;33(7):505–512
  34. Woods SW, Koster K, Krystal JK, Smith EO, Zubal IG, Hoffer PB, et al. Yohimbine alters regional cerebral blood flow in panic disorder. Lancet. 1988;2(8612):678
  35. Bystritsky A, Pontillo D, Powers M, Sabb FW, Craske MG, Bookheimer SY. Functional MRI changes during panic anticipation and imagery exposure. neuroreport. 2001;12(18):3953–3957
  36. Shin LM, Orr SP, Carson MA, Rauch SL, Macklin ML, Lasko NB, et al. Regional cerebral blood flow in the amygdala and medial prefrontal cortex during traumatic imagery in male and female Vietnam veterans with PTSD. Arch Gen Psychiatry. 2004;61(2):168–176
  37. Shin LM, Whalen PJ, Pitman RK, Bush G, Macklin ML, Lasko NB, et al. An fMRI study of anterior cingulate function in posttraumatic stress disorder. Biol Psychiatry. 2001;50(12):932–942
  38. Liberzon I, Taylor SF, Andur R, Jung TD, Chamberlain KR. Brain activation in PTSD in response to trauma-related stimuli. Biol Psychiarty. 1999;45:817–826
  39. Bremner JD, Staib LH, Kaloupek D, Southwick SM, Soufer R, Charney DS. Neural correlates of exposure to traumatic pictures and sound in Vietnam combat veterans with and without posttraumatic stress disorder: a positron emission tomography study. Biol Psychiatry. 1999;45(7):806–816
  40. Rauch S, Wahalen PJ, Shin LM, McInerney SC, Macklin ML. Exaggerated amygdala response to masked facial stimuli in posttraumatic stress disorder: a functional MRI study. Biol Psychiatry. 2000;47:769–776
  41. Papp LA, Martinez JM, Klein DF, Coplan JD, Norman RG, Cole R, et al. Respiratory psychophysiology of panic disorder: three respiratory challenges in 98 subjects. Am J Psychiatry. 1997;154(11):1557–1565
  42. Abelson JL, Weg JG, Nesse RM, Curtis GC. Persistent respiratory irregularity in patients with panic disorder. Biol Psychiatry. 2001;49(7):588–595
  43. Schwartz GE, Goetz RR, Klein DF, Endicott J, Gorman JM. Tidal volume of respiration and “sighing” as indicators of breathing irregularities in panic disorder patients. Anxiety. 1996;2(3):145–148
  44. Wilhelm FH, Trabert W, Roth WT. Physiologic instability in panic disorder and generalized anxiety disorder. Biol Psychiatry. 2001;49(7):596–605
  45. Gomez P, Stahel WA, Danuser B. Respiratory responses during affective picture viewing. Biol Psychol. 2004;67(3):359–373
  46. Boiten FA. The effects of emotional behaviour on components of the respiratory cycle. Biol Psychol. 1998;49(1-2):29–51
  47. Van Diest I, Winters W, Devriese S, Vercamst E, Han JN, Van de Woestijne KP, et al. Hyperventilation beyond fight/flight: respiratory responses during emotional imagery. Psychophysiology. 2001;38(6):961–968
  48. Horvath S, Fenz WD. Specificity in somatic indicants of anxiety in psychoneurotic patients. Percept Mot Skills. 1971;33(1):147–162
  49. Thomason ME, Burrows BE, Gabrieli JD, Glover GH. Breath holding reveals differences in fMRI BOLD signal in children and adults. NeuroImage. 2005;25(3):824–837
  50. Riecker A, Grodd W, Klose U, Schulz JB, Groschel K, Erb M, et al. Relation between regional functional MRI activation and vascular reactivity to carbon dioxide during normal aging. J Cereb Blood Flow Metab. 2003;23(5):565–573
  51. Abbott DF, Opdam HI, Briellmann RS, Jackson GD. Brief breath holding may confound functional magnetic resonance imaging studies. Hum Brain Mapp. 2005;24(4):284–290
  52. Gur RC, Gur RE, Resnick SM, Skolnick BE, Alavi A, Reivich M. The effect of anxiety on cortical cerebral blood flow and metabolism. J Cereb Blood Flow Metab. 1987;7(2):173–177
  53. Giordani B, Boivin M, Berent S, Koeppe B, Rothley J, Modell JG, et al. Anxiety and cerebral cortical metabolism in normal persons. Psychiatry Res Neuroimaging. 1990;35:49–60
  54. MacKenzie R, Sims C, Owens RG, Dixon AK. Patients' perceptions of magnetic resonance imaging. Clin Radiol. 1995;50(3):137–143
  55. Katz RC, Wilson L, Frazer N. Anxiety and its determinants in patients undergoing magnetic resonance imaging. J Behav Ther Exp Psychiatry. 1994;25(2):131–134
  56. Brennan SC, Redd WH, Jacobsen PB, Schorr O, Heelan RT, Sze GK, et al. Anxiety and panic during magnetic resonance scans. Lancet. 1988;2(8609):512
  57. Quirk ME, Letendre AJ, Ciottone RA, Lingley JF. Anxiety in patients undergoing MR imaging. Radiology. 1989;170(2):463–466
  58. Melendez JC, McCrank E. Anxiety-related reactions associated with magnetic resonance imaging examinations. JAMA. 1993;270(6):745–747
  59. Harris LM, Cumming SR, Menzies RG. Predicting anxiety in magnetic resonance imaging scans. Int J Behav Med. 2004;11(1):1–7
  60. Nazemi H, Dager SR. Coping strategies of panic and control subjects undergoing lactate infusion during magnetic resonance imaging confinement. Compr Psychiatry. 2003;44(3):190–197
  61. Warach S, Gur RC, Gur RE, Skolnick BE, Obrist WD, Reivich M. The reproducibility of the 133Xe inhalation technique in resting studies: task order and sex related effects in healthy young adults. J Cereb Blood Flow Metab. 1987;7(6):702–708
  62. Roth WT, Ehlers A, Taylor CB, Margraf J, Agras WS. Skin conductance habituation in panic disorder patients. Biol Psychiatry. 1990;27(11):1231–1243
  63. Masaoka Y, Homma I. The effect of anticipatory anxiety on breathing and metabolism in humans. Respir Physiol. 2001;128(2):171–177
  64. Dager SR, Layton M, Richards T. Neuroimaging findings in anxiety disorders. Semin Clin Neuropsychiatry. 1996;1(1):48–60
  65. Mountz JM, Modell JG, Wilson MW, Curtis GC, Lee MA, Schmaltz S, et al. Positron emission tomographic evaluation of cerebral blood flow during state anxiety in simple phobia. Arch Gen Psychiatry. 1989;46(6):501–504
  66. Mathew RJ, Wilson WH. Hematocrit and anxiety. J Psychosom Res. 1986;30(3):307–311
  67. Mathew RJ, Wilson WH. Behavioral and cerebrovascular effects of caffeine in patients with anxiety disorders. Acta Psychiatr Scand. 1990;82(1):17–22
  68. Edvinsson L, Owman C, Siesjo B. Physiological role of cerebrovascular sympathetic nerves in the autoregulation of cerebral blood flow. Brain Res. 1976;117(3):519–523
  69. Sercombe R, Aubineau P, Edvinsson L, Mamo H, Owman CH, Pinard E, et al. Neurogenic influence on local cerebral blood flow. Effect of catecholamines or sympathetic stimulation as correlated with the sympathetic innervation. Neurology. 1975;25(10):954–963
  70. Gotoh F, Tazaki Y, Meyer JS. Transport of gases through brain and their extravascular vasomotor action. Exp Neurol. 1961;4:48–58
  71. Kontos HA, Wei EP, Raper AJ, Patterson JL. Local mechanism of CO2 action of cat pial arterioles. Stroke. 1977;8(2):226–229
  72. Fenton RA, Rubio R, Berne RM. Adenosine and the acid-base state of vascular smooth muscle. J Appl Physiol. 1981;51(1):179–184
  73. Karaki H, Weiss GB. Effect of transmembrane pH gradient changes on potassium-induced relaxation in vascular smooth muscle. Blood Vessels. 1981;18(1-2):36–44
  74. Grubb RL, Raichle ME, Eichling JO, Ter-Pogossian MM. The effects of changes in PaCO2 on cerebral blood volume, blood flow, and vascular mean transit time. Stroke. 1974;5(5):630–639
  75. Iadecola C, Pelligrino DA, Moskowitz MA, Lassen NA. Nitric oxide synthase inhibition and cerebrovascular regulation. J Cereb Blood Flow Metab. 1994;14(2):175–192
  76. Ido Y, Chang K, Woolsey TA, Williamson JR. NADH: sensor of blood flow need in brain, muscle, and other tissues. FASEB J. 2001;15(8):1419–1421
  77. Leffler CW, Parfenova H. Cerebral arteriolar dilation to hypoxia: role of prostanoids. Am J Physiol. 1997;272(1 Pt 2):H418–H424
  78. Pelligrino DA, Wang Q. Cyclic nucleotide crosstalk and the regulation of cerebral vasodilation. Prog Neurobiol. 1998;56(1):1–18
  79. Faraci FM, Sobey CG. Role of potassium channels in regulation of cerebral vascular tone. J Cereb Blood Flow Metab. 1998;18(10):1047–1063
  80. Long W, Zhao Y, Zhang L, Longo LD. Role of Ca(2+) channels in NE-induced increase in fetal and adult cerebral arteries. Am J Physiol. 1999;277(1 Pt 2):R286–R294
  81. Artru AA, Colley PS. Cerebral blood flow responses to hypocapnia during hypotension. Stroke. 1984;15(5):878–883
  82. Harper AM, Glass HI. Effect of alterations in the arterial carbon dioxide tension on the blood flow through the cerebral cortex at normal and low arterial blood pressures. J Neurol Neurosurg Psychiatry. 1965;28(5):449–452
  83. Gregory P, Ishikawa T, McDowall DG. CO2 responses of the cerebral circulation during drug-induced hypotension in the cat. J Cereb Blood Flow Metab. 1981;1(2):195–201
  84. Jones SC, Bose B, Furlan AJ, Friel HT, Easley KA, Meredith MP, et al. CO2 reactivity and heterogeneity of cerebral blood flow in ischemic, border zone, and normal cortex. Am J Physiol. 1989;257(2 Pt 2):H473–H482
  85. Tominaga S, Strandgaard S, Uemura K, Ito K, Kutsuzawa T. Cerebrovascular CO2 reactivity in normotensive and hypertensive man. Stroke. 1976;7(5):507–510
  86. Rostrup E, Knudsen GM, Law I, Holm S, Larsson HB, Paulson OB. The relationship between cerebral blood flow and volume in humans. NeuroImage. 2005;24(1):1–11
  87. Ito H, Yokoyama I, Iida H, Kinoshita T, Hatazawa J, Shimosegawa E, et al. Regional differences in cerebral vascular response to PaCO2 changes in humans measured by positron emission tomography. J Cereb Blood Flow Metab. 2000;20(8):1264–1270
  88. Posse S, Olthoff U, Weckesser M, Jancke L, Muller-Gartner HW, Dager SR. Regional dynamic signal changes during controlled hyperventilation assessed with blood oxygen level–dependent functional MR imaging. AJNR Am J Neuroradiol. 1997;18(9):1763–1770
  89. Posse S, Kemna LJ, Elghahwagi B, Wiese S, Kiselev VG. Effect of graded hypo- and hypercapnia on fMRI contrast in visual cortex: quantification of T(*)(2) changes by multiecho EPI. Magn Reson Med. 2001;46(2):264–271
  90. Fox PT, Mintun MA, Reiman EM, Raichle ME. Enhanced detection of focal brain responses using intersubject averaging and change-distribution analysis of subtracted PET images. J Cereb Blood Flow Metab. 1988;8(5):642–653
  91. Friston KJ, Frith CD, Liddle PF, Dolan RJ, Lammertsma AA, Frackowiak RS. The relationship between global and local changes in PET scans. J Cereb Blood Flow Metab. 1990;10(4):458–466
  92. Ramsay SC, Murphy K, Shea SA, Friston KJ, Lammertsma AA, Clark JC, et al. Changes in global cerebral blood flow in humans: effect on regional cerebral blood flow during a neural activation task. J Physiol. 1993;471:521–534
  93. Li TQ, Kastrup A, Moseley ME, Glover GH. Changes in baseline cerebral blood flow in humans do not influence regional cerebral blood flow response to photic stimulation. J Magn Reson Imaging. 2000;12(5):757–762
  94. Corfield DR, Murphy K, Josephs O, Adams L, Turner R. Does hypercapnia-induced cerebral vasodilation modulate the hemodynamic response to neural activation?. NeuroImage. 2001;13(6 Pt 1):1207–1211
  95. Shimosegawa E, Kanno I, Hatazawa J, Fujita H, Iida H, Miura S, et al. Photic stimulation study of changing the arterial partial pressure level of carbon dioxide. J Cereb Blood Flow Metab. 1995;15(1):111–114
  96. Bandettini PA, Wong EC. A hypercapnia-based normalization method for improved spatial localization of human brain activation with fMRI. NMR Biomed. 1997;10(4-5):197–203
  97. Weckesser M, Posse S, Olthoff U, Kemna L, Dager S, Muller-Gartner HW. Functional imaging of the visual cortex with bold-contrast MRI: hyperventilation decreases signal response. Magn Reson Med. 1999;41(1):213–216
  98. Kemna LJ, Posse S. Effect of respiratory CO(2) changes on the temporal dynamics of the hemodynamic response in functional MR imaging. NeuroImage. 2001;14(3):642–649
  99. Cohen ER, Ugurbil K, Kim SG. Effect of basal conditions on the magnitude and dynamics of the blood oxygenation level–dependent fMRI response. J Cereb Blood Flow Metab. 2002;22(9):1042–1053
  100. Kashikura K, Kershaw J, Kashikura A, Zhang X, Matsuura T, Kanno I. Hyperoxia modified activation-induced blood oxygenation level–dependent response of human visual cortex (V1): an event-related functional magnetic resonance imaging study. Neurosci Lett. 2001;299(1-2):53–56
  101. Kashikura K, Kershaw J, Kashikura A, Matsuura T, Kanno I. Hyperoxia-enhanced activation-induced hemodynamic response in human VI: an fMRI study. neuroreport. 2000;11(5):903–906
  102. Lindauer U, Gethmann J, Kuhl M, Kohl-Bareis M, Dirnagl U. Neuronal activity-induced changes of local cerebral microvascular blood oxygenation in the rat: effect of systemic hyperoxia or hypoxia. Brain Res. 2003;975(1-2):135–140
  103. Balestrino M, Somjen GG. Concentration of carbon dioxide, interstitial pH and synaptic transmission in hippocampal formation of the rat. J Physiol. 1988;396:247–266
  104. Lee J, Taira T, Pihlaja P, Ransom BR, Kaila K. Effects of CO2 on excitatory transmission apparently caused by changes in intracellular pH in the rat hippocampal slice. Brain Res. 1996;706(2):210–216
  105. Huttunen J, Tolvanen H, Heinonen E, Voipio J, Wikstrom H, Ilmoniemi RJ, et al. Effects of voluntary hyperventilation on cortical sensory responses. Electroencephalographic and magnetoencephalographic studies. Exp Brain Res. 1999;125(3):248–254
  106. Friedman SD, Mathis CM, Hayes C, Renshaw PF, Dager SR. Brain pH response to hyperventilation in panic disorder: preliminary evidence for metabolic dysregulation. Am J Psychiatry. 2006;163:710–715
  107. Dager SR, Friedman SD, Heide A, Layton ME, Richards T, Artru A, et al. Two-dimensional proton echo-planar spectroscopic imaging of brain metabolic changes during lactate-induced panic. Arch Gen Psychiatry. 1999;56(1):70–77
  108. Dager SR, Strauss WL, Marro KI, Richards TL, Metzger GD, Artru AA. Proton magnetic resonance spectroscopy investigation of hyperventilation in subjects with panic disorder and comparison subjects. Am J Psychiatry. 1995;152(5):666–672
  109. Dager SR, Marro KI, Richards TL, Metzger GD. Preliminary application of magnetic resonance spectroscopy to investigate lactate-induced panic. Am J Psychiatry. 1994;151(1):57–63
  110. Biswal B, Yetkin FZ, Haughton VM, Hyde JS. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med. 1995;34(4):537–541
  111. Obrig H, Neufang M, Wenzel R, Kohl M, Steinbrink J, Einhaupl K, et al. Spontaneous low frequency oscillations of cerebral hemodynamics and metabolism in human adults. NeuroImage. 2000;12(6):623–639
  112. Kuo TB, Chern CM, Sheng WY, Wong WJ, Hu HH. Frequency domain analysis of cerebral blood flow velocity and its correlation with arterial blood pressure. J Cereb Blood Flow Metab. 1998;18(3):311–318
  113. Wise RG, Ide K, Poulin MJ, Tracey I. Resting fluctuations in arterial carbon dioxide induce significant low frequency variations in BOLD signal. NeuroImage. 2004;21(4):1652–1664
  114. Diehl RR, Linden D, Lucke D, Berlit P. Spontaneous blood pressure oscillations and cerebral autoregulation. Clin Auton Res. 1998;8(1):7–12
  115. Appel ML, Berger RD, Saul JP, Smith JM, Cohen RJ. Beat to beat variability in cardiovascular variables: noise or music?. J Am Coll Cardiol. 1989;14(5):1139–1148
  116. Hyndman BW. The role of rhythms in homeostasis. Kybernetik. 1974;15(4):227–236
  117. Yates FE. The 10th J. A. F. Stevenson memorial lecture. Outline of a physical theory of physiological systems. Can J Physiol Pharmacol. 1982;60(3):217–248
  118. Rapp PE. Why are so many biological systems periodic?. Prog Neurobiol. 1987;29(3):261–273
  119. Giardino ND, Lehrer PM, Feldman JM. The role of oscillations in self-regulation: a revision of the classical model of homeostasis. In:  Kenney D,  Carlson JG,  McGuigan FJ,  Sheppard JL editor. Stress and health: research and clinical applications. Chur (Switzerland): Harwood Academic Publishers; 1999;p. 27–51
  120. Biswal B, Hudetz AG, Yetkin FZ, Haughton VM, Hyde JS. Hypercapnia reversibly suppresses low-frequency fluctuations in the human motor cortex during rest using echo-planar MRI. J Cereb Blood Flow Metab. 1997;17(3):301–308
  121. Biswal B, DeYoe AE, Hyde JS. Reduction of physiological fluctuations in fMRI using digital filters. Magn Reson Med. 1996;35(1):107–113
  122. Birn RM, Diamond JB, Smith MA, Bandettini PA. Separating respiratory-variation–related fluctuations from neuronal-activity–related fluctuations in fMRI. NeuroImage. 2006;31:1536–1548
  123. Nunn JF, Hill DW. Respiratory dead space and arterial to end-tidal carbon dioxide tension difference in anesthetized man. J Appl Physiol. 1960;15:383–389
  124. Dubois AB, Britt AG, Fenn WO. Alveolar CO2 during the respiratory cycle. J Appl Physiol. 1952;4(7):535–548
  125. Severinghaus JW, Lassen N. Step hypocapnia to separate arterial from tissue Pco2 in the regulation of cerebral blood flow. Circ Res. 1967;20(2):272–278
  126. Hauge A, Thoresen M, Walloe L. Changes in cerebral blood flow during hyperventilation and CO2-breathing measured transcutaneously in humans by a bidirectional, pulsed, ultrasound Doppler blood velocitymeter. Acta Physiol Scand. 1980;110(2):167–173
  127. Ellingsen I, Hauge A, Nicolaysen G, Thoresen M, Walloe L. Changes in human cerebral blood flow due to step changes in PAo2 and PAco2. Acta Physiol Scand. 1987;129(2):157–163
  128. Albrecht RF, Miletich DJ, Ruttle M. Cerebral effects of extended hyperventilation in unanesthetized goats. Stroke. 1987;18(3):649–655
  129. Wilhelm FH, Gerlach AL, Roth WT. Slow recovery from voluntary hyperventilation in panic disorder. Psychosom Med. 2001;63(4):638–649
  130. Reiman EM, Raichle ME, Robins E, Butler FK, Herscovitch P, Fox P, et al. The application of positron emission tomography to the study of panic disorder. Am J Psychiatry. 1986;143(4):469–477

 Current affiliation for N.D. Giardino: Department of Psychiatry, Univesity of Michigan, Ann Arbor, MI.

PII: S0010-440X(06)00135-0

doi: 10.1016/j.comppsych.2006.11.001

Comprehensive Psychiatry
Volume 48, Issue 2 , Pages 103-112 , March 2007

Article Tools

* Image Usage & Resolution