Neurobiology of panic and Ph chemosensation in the brain

Dialogues in Clinical Neuroscience

Volumn 13, Issue 4, 2011, Pages 475-483

  Wemmie, John A ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Brain ph; Chemosensation; Co 2; Lactate; Panic disorder; Provocation challenge

Indexed keywords

ACID SENSING ION CHANNEL; ADRENERGIC RECEPTOR STIMULATING AGENT; BICARBONATE; CAFFEINE; DOXAPRAM; FLUMAZENIL; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 40; LACTATE SODIUM; LACTIC ACID; MONOCARBOXYLATE TRANSPORTER; N METHYL DEXTRO ASPARTIC ACID; OPIATE ANTAGONIST; SEROTONIN; SEROTONIN AGONIST; TANDEM PORE DOMAIN POTASSIUM CHANNEL; TETRAGASTRIN; TRANSIENT RECEPTOR POTENTIAL CHANNEL; CARBON DIOXIDE;

ACIDOSIS; AMYGDALOID NUCLEUS; ARTICLE; BLOOD BRAIN BARRIER; BRAIN LEVEL; CARBON DIOXIDE BREATHING; CELL PH; CHEMOSENSITIVITY; CINGULATE GYRUS; FAMILY HISTORY; FEAR; HIPPOCAMPUS; HUMAN; HYPERVENTILATION; INSULA; LOCUS CERULEUS; MOLECULAR SENSOR; NERVE CELL PLASTICITY; NEUROBIOLOGY; NONHUMAN; PANIC; PARABRACHIAL NUCLEUS; PH; PREFRONTAL CORTEX; PROVOCATION; RAPHE NUCLEUS; ANIMAL; CHEMORECEPTOR; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; REVIEW;

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

EID: 84857684126     PISSN: 12948322     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (92)

1. Kessler RC, Chiu WT, Jin R, Ruscio AM, Shear K, Walters EE. The epidemiology of panic attacks, panic disorder, and agoraphobia in the National Comorbidity Survey Replication. Arch Gen Psychiatry. 2006;63:415-424.
2. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. 4th ed, Text Revision. Washington, DC: American Psychiatric Association; 2000.
3. Kessler RC, Chiu WT, Demler O, Merikangas KR, Walters EE. Prevalence, severity, and comorbidity of 12-month DSM-IV disorders in the National Comorbidity Survey Replication. Arch Gen Psychiatry. 2005;62:617-627.
4. Moynihan JE, Gevirtz RN. Respiratory and cognitive subtypes of panic. Preliminary validation of Ley's model. Behav Modif. 2001;25:555-583.
5. Klein DF. False suffocation alarms, spontaneous panics, and related conditions. An integrative hypothesis. Arch Gen Psychiatry. 1993;50:306-317.
6. Smoller JW, Pollack MH, Otto MW, Rosenbaum JF, Kradin RL. Panic anxiety, dyspnea, and respiratory disease. Theoretical and clinical considerations. Am J Respir Crit Care Med. 1996;154:6-17.
7. Giardino ND, Curtis JL, Abelson JL, et al. The impact of panic disorder on interoception and dyspnea reports in chronic obstructive pulmonary disease. Biol Psychol. 2010;84:142-146.
8. Livermore N, Sharpe L, Mckenzie D. Panic attacks and panic disorder in chronic obstructive pulmonary disease: a cognitive behavioral perspective. Resp Med. 2010;104:1246-1253.
9. Bouwer C, Stein DJ. Association of panic disorder with a history of traumatic suffocation. Am J Psychiatry. 1997;154:1566-1570.
10. Drury AN. The percentage of carbon dioxide in the alveolar air, and the tolerance to accumulating carbon dioxide in case of co-called "irritable heart". Heart. 1918;7:165-173.
11. Cohen ME, White PD. Life situations, emotions, and neurocirculatory asthenia (anxiety neurosis, neurasthenia, effort syndrome). Psychosom Med. 1951;13:335-357.
12. Pitts FN, McClure JN. Lactate metabolism in anxiety neurosis. N Engl J Med. 1967;227:1329-1336.
13. Ley R. The modification of breathing behavior. Pavlovian and operant control in emotion and cognition. Behav Modif. 1999;23:441-479.
14. Gorman JM, Kent JM, Sullivan GM, Coplan JD. Neuroanatomical hypothesis of panic disorder, revised. Am J Psychiatry. 2000;157:493-505.
15. Nardi AE, Freire R, Zin WA. Panic disorder and control of breathing. Resp Physio Neurobiol. 2009;167:133-143.
16. Mezzasalma MA, Valença AM, Lopes FL, Nascimento I, Zin WA, Nardi AE. [Neuroanatomy of panic disorder]. Rev Bras Psiquiatr. 2004;26:202-206.
17. Lee YJ, Curtis GC, Weg JG, Abelson JL, Modell JG, Campbell KM. Panic attacks induced by doxapram. Biol Psychiatry. 1993;33:295-297.
18. de Montigny, C. Cholecystokinin tetrapeptide induces panic-like attacks in healthy volunteers. Preliminary findings. Arch Gen Psychiatry. 1989;46:511-517.
19. Esquivel G, Schruers K, Griez E. Experimental models: panic and fear. In: Blanchard RJ, Griebel G, Nutt D, eds. Handbook of Anxiety and Fear. Amsterdam, the Netherlands: Elsevier; 2008:413-434.
20. Nutt DJ, Glue P, Lawson C. Wilson S. Flumazenil provocation of panic attacks. Evidence for altered benzodiazepine receptor sensitivity in panic disorder. Arch Gen Psychiatry. 1990;47:917-925.
21. Charney DS, Heninger GR, Jatlow PI. Increased anxiogenic effects of caffeine in panic disorders. Arch Gen Psychiatry. 1985;42:233-243.
22. Maremmani I, Marini G, Fornai F. Naltrexone-induced panic attacks. Am J Psychiatry. 1998;155:447.
23. Preter M, Lee SH, Petkova E, Vannucci M, Kim S, Klein DF. Controlled cross-over study in normal subjects of naloxone-preceding-lactate infusions; respiratory and subjective responses: relationship to endogenous opioid system, suffocation false alarm theory and childhood parental loss. Psychol Med. 2011;41:385-393.
24. Rassovsky Y, Kushner MG. Carbon dioxide in the study of panic disorder: issues of definition, methodology, and outcome. J Anx Disord. 2003;17:1-32.
25. Peskind ER, Jensen CF, Pascualy M, et al. Sodium lactate and hypertonic sodium chloride induce equivalent panic incidence, panic symptoms, and hypernatremia in panic disorder. Biol Psychiatry. 1998;44:1007-1016.
26. 2-induced panic attacks: a twin study. Am J Psychiatry. 1998;155:1184-1188.
27. Sajdyk TJ, Shekhar A. Sodium lactate elicits anxiety in rats after repeated GABA receptor blockade in the basolateral amygdala. Eur J Pharmacol. 2000;394:265-273.
28. Shekhar A, Sajdyk TJ, Gehlert DR, Rainnie DG. The amygdala, panic disorder, and cardiovascular responses. Ann N Y Acad Sci. 2003;985:308-325.
29. Johnson P, Truitt W, Fitz SD, et al. A key role for orexin in panic anxiety. Nat Med. 2010;16:111-115.
30. Sullivan GM, Apergis J, Gorman JM, LeDoux JE. Rodent doxapram model of panic: behavioral effects and c-Fos immunoreactivity in the amygdala. Biol Psychiatry. 2003;53:863-870.
31. Mongeluzi, DL Rosellini, RA, Ley, R, Caldarone, BJ, Stock, HS. The conditioning of dyspneic suffocation fear. Effects of carbon dioxide concentration on behavioral freezing and analgesia. Behav Modif. 2003;27:620-636.
32. Ziemann AE, Allen JE, Dahdaleh NS, et al. The amygdala is a chemosensor that detects carbon dioxide and acidosis to elicit fear behavior. Cell. 2009;139:1012-1021.
33. Johnson P, Fitz SD, Hollis JH, et al. Induction of c-Fos in 'panic/defence'-related brain circuits following brief hypercarbic gas exposure. J Psychopharmacol (Oxford). 2011;25:26-36.
34. Gorman J, Liebowitz M, Fyer A, et al. Lactate infusions in obsessivecompulsive disorder. Am J Psychiatry. 1985;142:864.
35. Esquivel G, Schruers KR, Maddock RJ, Colasanti A, Griez EJ. Acids in the brain: a factor in panic? J Psychopharmacol. 2010;24:639-647.
36. Gorman JM, Fyer MR, Goetz R, et al. Ventilatory physiology of patients with panic disorder. Arch Gen Psychiatry. 1988;45:31-39.
37. Goetz RR, Gorman JM, Dillon DJ, et al. Do panic disorder patients indiscriminately endorse somatic complaints? Psychiatry Res. 1989;29:207-213.
38. Freire R, Perna G, Nardi AE. Panic disorder respiratory subtype: psychopathology, laboratory challenge tests, and response to treatment. Harv Rev Psychiatry. 2010;18:220-229.
39. Goetz RR, Klein DF, Gorman JM. Symptoms essential to the experience of sodium lactate-induced panic. Neuropsychopharmacology. 1996;14:355-366.
40. Sinha SS, Coplan JD, Pine DS, Martinez JA, Klein DF, Gorman JM. Panic induced by carbon dioxide inhalation and lack of hypothalamic-pituitaryadrenal axis activation. Psychiatry Res. 1999;86:93-98.
41. 2 challenge induced HPA axis activation in panic. Int J Neuropsychopharmacol. 2007;10:797-804.
42. Abelson JL, Liberzon I. Dose response of adrenocorticotropin and cortisol to the CCK-B agonist pentagastrin. Neuropsychopharmacology. 1999;21:485-494.
43. Belgorodsky A, Knyazhansky L, Loewenthal U, Arbelle J, Cohen H, Benjamin J. Effects of the cortisol synthesis inhibitor metyrapone on the response to carbon dioxide challenge in panic disorder. Depress Anxiety. 2005;21:143-148.
44. Zandbergen J, Pols H, De Loof C, Lousberg H, Griez E. Effect of hypercapnia and other disturbances in the acid-base-balance on panic disorder. Hillside J Clin Psychiatry. 1989;11:185-197.
45. Richerson GB. Cellular mechanisms of sensitivity to pH in the mammalian respiratory system. In: Kaila K, Ransom BR, eds. pH and Brain Function. New York, NY: Wiley-Liss, Inc; 1998:509-533.
46. Pellerin L, Bouzier-Sore AK, Aubert A, et al. Activity-dependent regulation of energy metabolism by astrocytes: an update. Glia. 2007;55:1251-1262.
47. Suzuki A, Stern SA, Bozdagi O, et al. Astrocyte-neuron lactate transport is required for long-term memory formation. Cell. 2011;144:810-823.
48. Olsson M, Ho HP, Annerbrink K, Thylefors J, Eriksson E. Respiratory responses to intravenous infusion of sodium lactate in male and female Wistar rats. Neuropsychopharmacology. 2002;27:85-91.
49. Dager SR, Friedman SD, Heide A, et al. Two-dimensional proton echoplanar spectroscopic imaging of brain metabolic changes during lactateinduced panic. Arch Gen Psychiatry. 1999;56:70-77.
50. Cotten JF, Keshavaprasad B, Laster MJ, Eger EI, Yost CS. The ventilatory stimulant doxapram inhibits TASK tandem pore (K2P) potassium channel function but does not affect minimum alveolar anesthetic concentration. Anesth Analg. 2006;102:779-785.
51. Bayliss DA, Sirois JE, Talley EM. The TASK family: two-pore domain background K+ channels. Mol Interv. 2003;3:205-219.
52. Abelson JL, Weg JG, Nesse RM, Curtis GC. Persistent respiratory irregularity in patients with panic disorder. Biol Psychiatry. 2001;49:588-595.
53. Philibert RA, Nelson JJ, Sandhu HK, Crowe RR, Coryell WH. Association of an exonic LDHA polymorphism with altered respiratory response in probands at high risk for panic disorder. Am J Med Genet. 2003;117B:11-17.
54. Coryell W, Dindo L, Fyer A, Pine DS. Onset of spontaneous panic attacks: a prospective study of risk factors. Psychosom Med. 2006;68:754-757.
55. Coryell W, Fyer A, Pine D, Martinez J, Arndt S. Aberrant respiratory sensitivity to CO(2) as a trait of familial panic disorder. Biol Psychiatry. 2001;49:582-587.
56. Papp LA, Martinez JM, Klein DF, et al. Respiratory psychophysiology of panic disorder: three respiratory challenges in 98 subjects. Am J Psychiatry. 1997;154:1557-1565.
57. Meuret AE, Wilhelm FH, Ritz T, Roth WT. Feedback of end-tidal pCO(2) as a therapeutic approach for panic disorder. J Psychiatr Res. 2007;42:560-568.
58. Hegel MT, Ferguson RJ. Psychophysiological assessment of respiratory function in panic disorder: evidence for a hyperventilation subtype. Psychosom Med. 1997;59:224-230.
59. 2, and bicarbonate levels after blockade of panic attacks. Psychiatry Res. 1985;14:57-65.
60. Briggs AC, Stretch DD, Brandon S. Subtyping of panic disorder by symptom profile. Br J Psychiatry. 1993;163:201-209.
61. Stewart PA. Independent and dependent variables of acid-base control. Respir Physiol. 1978;33:9-26.
62. Maddock RJ, Buonocore MH, Copeland LE, Richards AL. Elevated brain lactate responses to neural activation in panic disorder: a dynamic 1H-MRS study. Mol Psychiatry. 2009;14:537-545.
63. 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;152:666-672.
64. Dager SR, Yim JB, Khalil GE, Artru AA, Bowden DM, Kenny MA. Application of a novel fiber-optic biosensor in situ to investigate the metabolic effect of lactate infusion. Neuropsychopharmacology. 1995;12:307-313.
65. Friedman SD, Mathis CM, Hayes C, Renshaw P, Dager SR. Brain pH response to hyperventilation in panic disorder: preliminary evidence for altered acid-base regulation. Am J Psychiatry. 2006;163:710-715.
66. Nattie E. Central chemoreceptors, pH, and respiratory control. In: Kaila K, Ransom BR, eds. pH and Brain Function. New York, NY: Wiley-Liss, Inc. 1998:535-560.
67. Marina N, Abdala AP, Trapp S, et al. Essential role of Phox2b-expressing ventrolateral brainstem neurons in the chemosensory control of inspiration and expiration. J Neurosci. 2010;30:12466-12473.
68. Nattie G, Li A. Multiple central chemoreceptor sites: cell types and function in vivo. Adv Exp Med Biol. 2008;605:343-347.
69. Nattie E, Li A. Central chemoreception is a complex system function that involves multiple brain stem sites. J Appl Physiol. 2009;106:1464-1466.
70. Amiel J, Laudier B, Attié-Bitach T, et al. Polyalanine expansion and frameshift mutations of the paired-like homeobox gene PHOX2B in congenital central hypoventilation syndrome. Nat Genet. 2003;33:459-461.
71. Richerson GB, Wang W, Hodges MR, Dohle CI, Diez-Sampedro A. Homing in on the specific phenotype(s) of central respiratory chemoreceptors. Exp Physiol. 2005;90:259-266; discussion 266-259.
72. Tresguerres M, Buck J, Levin LR. Physiological carbon dioxide, bicarbonate, and pH sensing. Pflugers Arch. 2010; 460:953-964.
73. Buckler KJ. Two-pore domain k(+) channels and their role in chemoreception. Adv Exp Med Biol. 2010;661:15-30.
74. Mulkey DK, Talley EM, Stornetta RL, et al. TASK channels determine pH sensitivity in select respiratory neurons but do not contribute to central respiratory chemosensitivity. J Neurosci. 2007;27:14049-14058.
75. Trapp S, Aller MI, Wisden W, Gourine AV. A role for TASK-1 (KCNK3) channels in the chemosensory control of breathing. J Neurosci. 2008;28:8844-8850.
76. 2 sensitivity. Proc Natl Acad Sci U S A. 2010;107:2325-2330.
77. 2 chemosensitivity of locus coeruleus neurons. J Neurophysiol. 2011;105:2791-2801.
78. 2 to cortical excitability via pH. Neuron. 2005;48:1011-1023.
79. Birdsong WT, Fierro L, Williams FG, et al. Sensing muscle ischemia: coincident detection of acid and ATP via interplay of two ion channels. Neuron. 2010;68:739-749.
80. DeVries SH. Exocytosed protons feedback to suppress the Ca(2+) current in mammalian cone photoreceptors. Neuron. 2001;32:1107-1117.
81. Makani S, Chesler M. Endogenous alkaline transients boost postsynaptic NMDA receptor responses in hippocampal CA1 pyramidal neurons. J Neurosci. 2007;27:7438-7446.
82. Waldmann R, Lazdunski M. H+-gated cation channels: neuronal acid sensors in the NaC/DEG family of ion channels. Curr Opin Neurobiol. 1998;8:418-424.
83. Krishtal O. The ASICs: signaling molecules? Modulators? Trends Neurosci. 2003;26:477-483.
84. Wemmie JA, Price MP, Welsh MJ. Acid-sensing ion channels: advances, questions and therapeutic opportunities. Trends Neurosci. 2006;29:578-586.
85. Trapp S, Tucker SJ, Gourine AV. Respiratory responses to hypercapnia and hypoxia in mice with genetic ablation of Kir5.1 (Kcnj16). Exp Physiol. 2011;96:451-459.
86. McGuire J, Herman JP, Ghosal S, Eaton K, Sallee FR, Sah R. Acid-sensing by the T cell death-associated gene 8 (TDAG8) receptor cloned from rat brain. Biochem Biophys Res Comm. 2009;378:420-425.
87. Severson CA, Wang W, Pieribone VA, Dohle CI, Richerson GB. Midbrain serotonergic neurons are central pH chemoreceptors. Nat Neurosci. 2003;6:1139-1140.
88. 2. Proc Natl Acad Sci U S A. 2010;107:16354-16359.
89. Buchanan G, Richerson G. Role of chemoreceptors in mediating dyspnea. Respir Physiol Neurobiol. 2009;167:9-19.
90. 2. Proc Natl Acad Sci U S A. 2007;104:10685-10690.
91. Wemmie JA, Askwith CC, Lamani E, Cassell MD, Freeman JHJ, Welsh MJ. Acid-sensing ion channel 1 is localized in brain regions with high synaptic density and contributes to fear conditioning. J Neurosci. 2003;23:5496-5502.
92. Coryell M, Ziemann AE, Westmoreland PJ, et al. Targeting ASIC1a reduces innate fear and alters neuronal activity in the fear circuit. Biol Psychiatry. 2007;62:1140-1148.