Acids in the brain: A factor in panic?

Journal of Psychopharmacology

Volumn 24, Issue 5, 2010, Pages 639-647

  Esquivel, G ^a   Schruers, K R ^a   Maddock, R J ^b   Colasanti, A ^a   Griez, E J ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Acid base imbalance; Anxiety; Carbon dioxide; Hyperventilation; Lactate; Panic; PH

Indexed keywords

CARBON DIOXIDE; CARBONATE DEHYDRATASE; LACTATE SODIUM;

BLOOD BRAIN BARRIER; BLOOD CARBON DIOXIDE TENSION; CHEMORECEPTOR; DEFENSIVE BEHAVIOR; DISORDERS OF ACID BASE BALANCE; HUMAN; HYPERVENTILATION; HYPOCAPNIA; METABOLIC ACIDOSIS; NERVE CELL NETWORK; NEUROIMAGING; NONHUMAN; PANIC; PRIORITY JOURNAL; RESPIRATORY ACIDOSIS; RESPIRATORY ALKALOSIS; REVIEW; VISUAL STIMULATION;

ACIDOSIS; ACIDOSIS, LACTIC; ACIDOSIS, RESPIRATORY; ANIMALS; BRAIN; BRAIN CHEMISTRY; CARBON DIOXIDE; CHEMORECEPTOR CELLS; HUMANS; HYDROGEN-ION CONCENTRATION; PANIC DISORDER;

EID: 77952143039     PISSN: 02698811     EISSN: 14617285     Source Type: Journal    
DOI: 10.1177/0269881109104847     Document Type: Review

References (95)

1. Abelson, JL, Weg, JG, Nesse, RM, Curtis, GC (2001) Persistent respiratory irregularity in patients with panic disorder. Biol Psychiatry 49: 588-595.
2. Abrams, K., Rassovsky, Y., Kushner, MG (2006) Evidence for respiratory and nonrespiratory subtypes in panic disorder. Depress Anxiety 23: 474-481.
3. American Psychiatric Association (2000) Diagnostic and Statistical Manual of Mental Disorders: DSM-IV-TR, fourth ed. American Psychiatric Association, Washington, DC.
4. Bailey, JE, Argyropoulos, SV, Lightman, SL, Nutt, DJ (2003) Does the brain noradrenaline network mediate the effects of the CO2 challenge ? J Psychopharmacol 17: 252-259.
5. Blanchard, CD, Hynd, AL, Minke, KA, Minemoto, T., Blanchard, RJ (2001) Human defensive behaviors to threat scenarios show parallels to fear- and anxiety-related defense patterns of non-human mammals. Neurosci Biobehav Rev 25: 761-770.
6. Bluher, S., Schulz, M., Bierbach, U., Meixensberger, J., Trobs, RB, Hirsch, W., et al. (2008) Central lactic acidosis, hyperventilation, and respiratory alkalosis: leading clinical features in a 3-year-old boy with malignant meningeal melanoma. Eur J Pediatr 167: 483-485.
7. Bouton, ME, Mineka, S., Barlow, DH (2001) A modern learning theory perspective on the etiology of panic disorder. Psychol Rev 108: 4-32.
8. Briggs, AC, Stretch, DD, Brandon, S. (1993) Subtyping of panic disorder by symptom profile. Br J Psychiatry 163: 201-209.
9. Cadoux-Hudson, TA, Rajagopalan, B., Ledingham, JG, Radda, GK (1990) Response of the human brain to a hypercapnic acid load in vivo. Clin Sci (Lond) 79: 1-3.
10. Caldirola, D., Bellodi, L., Caumo, A., Migliarese, G., Perna, G. (2004) Approximate entropy of respiratory patterns in panic disorder. Am J Psychiatry 161: 79-87. (Pubitemid 38419311) (Pubitemid 38419311) (Pubitemid 38419311)
11. Carr, DB, Sheehan, DV (1984) Panic anxiety: a new biological model. J Clin Psychiatry 45: 323-330.
12. Cohen, ME, White, PD (1951) Life situations, emotions, and neurocirculatory asthenia (anxiety neurosis, neurasthenia, effort syndrome). Psychosom Med 13: 335-357.
13. Colasanti, A., Salamon, E., Schruers, K., van Diest, R., van Duinen, M., Griez, EJ (2008) Carbon dioxide-induced emotion and respiratory symptoms in healthy volunteers. Neuropsychopharmacology 33: 3103-3110.
14. Coplan, JD, Sharma, T., Rosenblum, LA, Friedman, S., Bassoff, TB, Barbour, RL, et al. (1992) Effects of sodium lactate infusion on cisternal lactate and carbon dioxide levels in nonhuman primates. Am J Psychiatry 149: 1369-1373.
15. Cotten, JF, Keshavaprasad, B., Laster, MJ, Eger II, EI, Yost, CS (2006) The ventilatory stimulant doxapram inhibits TASK tandem pore (K2P) potassium channel function but does not affect minimum alveolar anesthetic concentration. Anesth Analg 102: 779-785.
16. Dager, SR, Friedman, SD, Heide, A., Layton, ME, Richards, T., Artru, A., et al. (1999) Two-dimensional proton echo-planar spectroscopic imaging of brain metabolic changes during lactate-induced panic. Arch Gen Psychiatry 56: 70-77.
17. Dager, SR, Marro, KI, Richards, TL, Metzger, GD (1994) Preliminary application of magnetic resonance spectroscopy to investigate lactate-induced panic. Am J Psychiatry 151: 57-63.
18. Dager, SR, Rainey, JM, Kenny, MA, Artru, AA, Metzger, GD, Bowden, DM (1990) Central nervous system effects of lactate infusion in primates. Biol Psychiatry 27: 193-204.
19. Dager, SR, Richards, T., Strauss, W., Artru, A. (1997) Single-voxel 1H-MRS investigation of brain metabolic changes during lactate-induced panic. Psychiatry Res 76: 89-99.
20. Dager, SR, Strauss, WL, Marro, KI, Richards, TL, Metzger, GD, Artru, AA (1995 a) Proton magnetic resonance spectroscopy investigation of hyperventilation in subjects with panic disorder and comparison subjects. Am J Psychiatry 152: 666-672.
21. Dager, SR, Yim, JB, Khalil, GE, Artru, AA, Bowden, DM, Kenny, MA (1995 b) Application of a novel fiber-optic biosensor in situ to investigate the metabolic effect of lactate infusion. Neuropsychopharmacology 12: 307-313.
22. Dalsgaard, MK, Quistorff, B., Danielsen, ER, Selmer, C., Vogelsang, T., Secher, NH (2004) A reduced cerebral metabolic ratio in exercise reflects metabolism and not accumulation of lactate within the human brain. J Physiol 554: 571-578.
23. Damasio, AR (1999) The Feeling of What Happens: Body and Emotion in the Making of Consciousness, first ed. Harcourt Brace, New York.
24. Denton, DA (2006) The Primordial Emotions: The Dawning of Consciousness. Oxford University Press, Oxford.
25. Dienel, GA, Hertz, L. (2001) Glucose and lactate metabolism during brain activation. J Neurosci Res 66: 824-838.
26. Erlichman, JS, Hewitt, A., Damon, TL, Hart, M., Kurascz, J., Li, A., et al. (2008) Inhibition of monocarboxylate transporter 2 in the retrotrapezoid nucleus in rats: a test of the astrocyte-neuron lactate-shuttle hypothesis. J Neurosci 28: 4888-4896.
27. Esquivel, G., Schruers, K., Griez, E. (2008) Experimental models: panic and fear. In: Blanchard, RJ, Griebel, G, Nutt, DJ (eds). Handbook of Anxiety and Fear. Elsevier BV, Amsterdam, pp. 413-435.
28. Friedman, SD, Mathis, CM, Hayes, C., Renshaw, P., Dager, SR (2006) Brain pH response to hyperventilation in panic disorder: preliminary evidence for altered acid-base regulation. Am J Psychiatry 163: 710-715.
29. Goetz, RR, Klein, DF, Papp, LA, Martinez, JM, Gorman, JM (2001) Acute panic inventory symptoms during CO(2) inhalation and room-air hyperventilation among panic disorder patients and normal controls. Depress Anxiety 14: 123-136.
30. Gorman, JM, Askanazi, J., Liebowitz, MR, Fyer, AJ, Stein, J., Kinney, JM, et al. (1984) Response to hyperventilation in a group of patients with panic disorder. Am J Psychiatry 141: 857-861.
31. Gorman, JM, Battista, D., Goetz, RR, Dillon, DJ, Liebowitz, MR, Fyer, AJ, et al. (1989) A comparison of sodium bicarbonate and sodium lactate infusion in the induction of panic attacks. Arch Gen Psychiatry 46: 145-150.
32. Gorman, JM, Fyer, MR, Goetz, R., Askanazi, J., Liebowitz, MR, Fyer, AJ, et al. (1988) Ventilatory physiology of patients with panic disorder. Arch Gen Psychiatry 45: 31-39.
33. Gorman, JM, Goetz, RR, Dillon, D., Liebowitz, MR, Fyer, AJ, Davies, S., et al. (1990) Sodium D-lactate infusion of panic disorder patients. Neuropsychopharmacology 3: 181-189.
34. Gorman, JM, Kent, JM, Sullivan, GM, Coplan, JD (2000) Neuroanatomical hypothesis of panic disorder, revised. Am J Psychiatry 157: 493-505.
35. Gorman, JM, Papp, LA, Coplan, J., Martinez, J., Liebowitz, MR, Klein, DF (1993) The effect of acetazolamide on ventilation in panic disorder patients. Am J Psychiatry 150: 1480-1484.
36. Gorman, JM, Papp, LA, Coplan, JD, Martinez, JM, Lennon, S., Goetz, RR, et al. (1994) Anxiogenic effects of CO2 and hyperventilation in patients with panic disorder. Am J Psychiatry 151: 547-553.
37. Graeff, FG, Del-Ben, CM (2008) Neurobiology of panic disorder: from animal models to brain neuroimaging. Neurosci Biobehav Rev doi:10.1016/j. neurobiorev.2008.05.017.
38. Graeff, FG, Garcia-Leal, C., Del-Ben, CM, Guimaraes, FS (2005) Does the panic attack activate the hypothalamic-pituitary-adrenal axis ? An Acad Bras Cienc 77: 477-491.
39. Griez, E., Schruers, K. (1998) Experimental pathophysiology of panic. J Psychosom Res 45: 493-503.
40. Griez, E., Zandbergen, J., Lousberg, H., van den Hout, M. (1988) Effects of low pulmonary CO2 on panic anxiety. Compr Psychiatry 29: 490-497.
41. Griez, EJ, Colasanti, A., van Diest, R., Salamon, E., Schruers, K. (2007) Carbon dioxide inhalation induces dose-dependent and age-related negative affectivity. PLoS ONE 2: e987.
42. Jensen, KE, Thomsen, C., Henriksen, O. (1988) In vivo measurement of intracellular pH in human brain during different tensions of carbon dioxide in arterial blood. A 31P-NMR study. Acta Physiol Scand 134: 295-298.
43. Klein, DF (1993) False suffocation alarms, spontaneous panics, and related conditions. An integrative hypothesis. Arch Gen Psychiatry 50: 306-317.
44. Kucera, RR, Shapiro, JI, Whalen, MA, Kindig, NB, Filley, GF, Chan, L. (1989) Brain pH effects of NaHCO3 and Carbicarb in lactic acidosis. Crit Care Med 17: 1320-1323.
45. Liotti, M., Brannan, S., Egan, G., Shade, R., Madden, L., Abplanalp, B., et al. (2001) Brain responses associated with consciousness of breathlessness (air hunger). Proc Natl Acad Sci U S A 98: 2035-2040.
46. Lum, LC (1987) Hyperventilation syndromes in medicine and psychiatry: a review. J R Soc Med 80: 229-231.
47. Maddock, RJ (2001) The lactic acid response to alkalosis in panic disorder: an integrative review. J Neuropsychiatry Clin Neurosci 13: 22-34.
48. Maddock, RJ, Buonocore, MH, Copeland, LE, Richards, AL (2008) Elevated brain lactate responses to neural activation in panic disorder: a dynamic 1H-MRS study. Mol Psychiatry [Epub ahead of print].
49. Maddock, RJ, Carter, CS (1991) Hyperventilation-induced panic attacks in panic disorder with agoraphobia. Biol Psychiatry 29: 843-854.
50. Maddock, RJ, Mateo-Bermudez, J. (1990) Elevated serum lactate following hyperventilation during glucose infusion in panic disorder. Biol Psychiatry 27: 411-418.
51. Maren, S. (2007) Neuroscience. The threatened brain. Science 317: 1043-1044.
52. Martoft, L., Stodkilde-Jorgensen, H., Forslid, A., Pedersen, HD, Jorgensen, PF (2003) CO2 induced acute respiratory acidosis and brain tissue intracellular pH: a 31P NMR study in swine. Lab Anim 37: 241-248.
53. Mathew, RJ, Wilson, WH, Tant, S. (1989) Responses to hypercarbia induced by acetazolamide in panic disorder patients. Am J Psychiatry 146: 996-1000.
54. McNaughton, N., Corr, PJ (2004) A two-dimensional neuropsychology of defense: fear/anxiety and defensive distance. Neurosci Biobehav Rev 28: 285-305.
55. Mobbs, D., Petrovic, P., Marchant, JL, Hassabis, D., Weiskopf, N., Seymour, B., et al. (2007) When fear is near: threat imminence elicits prefrontal-periaqueductal gray shifts in humans. Science 317: 1079-1083.
56. Nakashima, K., Yamashita, T., Kashiwagi, S., Nakayama, N., Kitahara, T., Ito, H. (1996) The effect of sodium bicarbonate on CBF and intracellular pH in man: stable Xe-CT and 31P-MRS. Acta Neurol Scand Suppl 166: 96-98.
57. Nardi, AE, Lopes, FL, Valenca, AM, Nascimento, I., Mezzasalma, MA, Zin, WA (2004 a) Psychopathological description of hyperventilation-induced panic attacks: a comparison with spontaneous panic attacks. Psychopathology 37: 29-35.
58. Nardi, AE, Valenca, AM, Lopes, FL, Nascimento, I., Mezzasalma, MA, Zin, WA (2004 b) Clinical features of panic patients sensitive to hyperventilation or breath-holding methods for inducing panic attacks. Braz J Med Biol Res 37: 251-257.
59. Nardi, AE, Valenca, AM, Lopes, FL, Nascimento, I., Veras, AB, Freire, RC, et al. (2006 a) Psychopathological profile of 35% CO2 challenge test-induced panic attacks: a comparison with spontaneous panic attacks. Compr Psychiatry 47: 209-214.
60. Nardi, AE, Valenca, AM, Mezzasalma, MA, Lopes, FL, Nascimento, I., Veras, AB, et al. (2006 b) 35% Carbon dioxide and breath-holding challenge tests in panic disorder: a comparison with spontaneous panic attacks. Depress Anxiety 23: 236-244.
61. Nardi, AE, Valenca, AM, Nascimento, I., Zin, WA (2001) Hyperventilation challenge test in panic disorder and depression with panic attacks. Psychiatry Res 105: 57-65.
62. Panksepp, J. (1998) Affective Neuroscience, first ed. Oxford University Press, New York.
63. Papp, LA, Martinez, JM, Klein, DF, Coplan, JD, Norman, RG, Cole, R., et al. (1997) Respiratory psychophysiology of panic disorder: three respiratory challenges in 98 subjects. Am J Psychiatry 154: 1557-1565.
64. Pellerin, L., Bouzier-Sore, AK, Aubert, A., Serres, S., Merle, M., Costalat, R., et al. (2007) Activity-dependent regulation of energy metabolism by astrocytes: an update. Glia 55: 1251-1262.
65. Pitts Jr., FN, McClure Jr., JN (1967) Lactate metabolism in anxiety neurosis. N Engl J Med 277: 1329-1336.
66. Protopopescu, X., Pan, H., Tuescher, O., Cloitre, M., Goldstein, M., Engelien, A., et al. (2006) Increased brainstem volume in panic disorder: a voxel-based morphometric study. Neuroreport 17: 361-363.
67. Putnam, RW (2001) Intracellular pH regulation of neurons in chemosensitive and nonchemosensitive areas of brain slices. Respir Physiol 129: 37-56.
68. Putnam, RW, Filosa, JA, Ritucci, NA (2004) Cellular mechanisms involved in CO(2) and acid signaling in chemosensitive neurons. Am J Physiol Cell Physiol 287: C1493 - C1526.
69. Rassovsky, Y., Kushner, MG (2003) Carbon dioxide in the study of panic disorder: issues of definition, methodology, and outcome. J Anxiety Disord 17: 1-32.
70. Richerson, GB (2004) Serotonergic neurons as carbon dioxide sensors that maintain pH homeostasis. Nat Rev Neurosci 5: 449-461.
71. Scheller, D., Kolb, J., Tegtmeier, F. (1992) Lactate and pH change in close correlation in the extracellular space of the rat brain during cortical spreading depression. Neurosci Lett 135: 83-86.
72. Schruers, K., Klaassen, T., Pols, H., Overbeek, T., Deutz, NE, Griez, E. (2000) Effects of tryptophan depletion on carbon dioxide provoked panic in panic disorder patients. Psychiatry Res 93: 179-187.
73. Schruers, KRJ, van de Mortel, H., Overbeek, T., Griez, E. (2004) Symptom profiles of natural and laboratory panic attacks. Acta Neuropsychiatrica 16: 101-106.
74. Severson, CA, Wang, W., Pieribone, VA, Dohle, CI, Richerson, GB (2003) Midbrain serotonergic neurons are central pH chemoreceptors. Nat Neurosci 6: 1139-1140.
75. Shapiro, JI, Whalen, M., Kucera, R., Kindig, N., Filley, G., Chan, L. (1989) Brain pH responses to sodium bicarbonate and Carbicarb during systemic acidosis. Am J Physiol 256: H1316 - H1321.
76. Stein, MB, Millar, TW, Larsen, DK, Kryger, MH (1995) Irregular breathing during sleep in patients with panic disorder. Am J Psychiatry 152: 1168-1173.
77. Swenson, ER, Hughes, JM (1993) Effects of acute and chronic acetazolamide on resting ventilation and ventilatory responses in men. J Appl Physiol 74: 230-237.
78. Tarulli, AW, Lim, C., Bui, JD, Saper, CB, Alexander, MP (2005) Central neurogenic hyperventilation: a case report and discussion of pathophysiology. Arch Neurol 62: 1632-1634.
79. Tsacopoulos, M., Magistretti, PJ (1996) Metabolic coupling between glia and neurons. J Neurosci 16: 877-885.
80. Uehara, T., Sumiyoshi, T., Itoh, H., Kurata, K. (2008) Lactate production and neurotransmitters; evidence from microdialysis studies. Pharmacol Biochem Behav 90: 273-281.
81. Uehara, T., Sumiyoshi, T., Matsuoka, T., Tanaka, K., Tsunoda, M., Itoh, H., et al. (2005) Enhancement of lactate metabolism in the basolateral amygdala by physical and psychological stress: role of benzodiazepine receptors. Brain Res 1065: 86-91.
82. Van den Hout, MA, Griez, E. (1984) Panic symptoms after inhalation of carbon dioxide. Br J Psychiatry 144: 503-507.
83. van Duinen, MA, Schruers, KR, Jaegers, E., Maes, M., Griez, EJ (2004) Hypothalamic-pituitary-adrenal axis function following a 35% CO2 inhalation in healthy volunteers. Prog Neuropsychopharmacol Biol Psychiatry 28: 279-283.
84. van Duinen, MA, Schruers, KR, Maes, M., Griez, EJ (2005) CO2 challenge results in hypothalamic-pituitary-adrenal activation in healthy volunteers. J Psychopharmacol 19: 243-247.
85. van Duinen, MA, Schruers, KR, Maes, M., Griez, EJ (2007) CO2 challenge induced HPA axis activation in panic. Int J Neuropsychopharmacol 10: 797-804.
86. van Rijen, PC, Luyten, PR, van der Sprenkel, JW, Kraaier, V., van Huffelen, AC, Tulleken, CA, et al. (1989) 1H and 31P NMR measurement of cerebral lactate, high-energy phosphate levels, and pH in humans during voluntary hyperventilation: associated EEG, capnographic, and Doppler findings. Magn Reson Med 10: 182-193.
87. Washburn, CP, Sirois, JE, Talley, EM, Guyenet, PG, Bayliss, DA (2002) Serotonergic raphe neurons express TASK channel transcripts and a TASK-like pH- and halothane-sensitive K+ conductance. J Neurosci 22: 1256-1265.
88. Wemmie, JA, Askwith, CC, Lamani, E., Cassell, MD, Freeman Jr., JH, Welsh, MJ (2003) Acid-sensing ion channel 1 is localized in brain regions with high synaptic density and contributes to fear conditioning. J Neurosci 23: 5496-5502.
89. Wemmie, JA, Coryell, MW, Askwith, CC, Lamani, E., Leonard, AS, Sigmund, CD, et al. (2004) Overexpression of acid-sensing ion channel 1a in transgenic mice increases acquired fear-related behavior. Proc Natl Acad Sci U S A 101: 3621-3626.
90. Wilhelm, FH, Gerlach, AL, Roth, WT (2001) Slow recovery from voluntary hyperventilation in panic disorder. Psychosom Med 63: 638-649.
91. Williams, RH, Jensen, LT, Verkhratsky, A., Fugger, L., Burdakov, D. (2007) Control of hypothalamic orexin neurons by acid and CO2. Proc Natl Acad Sci U S A 104: 10685-10690.
92. Yeragani, VK, Radhakrishna, RK, Tancer, M., Uhde, T. (2002) Nonlinear measures of respiration: respiratory irregularity and increased chaos of respiration in patients with panic disorder. Neuropsychobiology 46: 111-120.
93. Zandbergen, J., Lousberg, HH, Pols, H., de Loof, C., Griez, EJ (1990) Hypercarbia versus hypocarbia in panic disorder. J Affect Disord 18: 75-81.
94. Zandbergen, J., Pols, H., De Loof, C., Lousberg, H., Griez, E. (1989) Effect of hypercapnia and other disturbances in the acid-base-balance on panic disorder. Hillside J Clin Psychiatry 11: 185-197.
95. Zandbergen, J., Pols, H., Fernandez, I., Griez, E. (1991) An analysis of panic symptoms during hypercarbia compared to hypocarbia in patients with panic attacks. J Affect Disord 23: 131-136.