Panic anxiety in humans with bilateral amygdala lesions: Pharmacological induction via cardiorespiratory interoceptive pathways

Journal of Neuroscience

Volumn 36, Issue 12, 2016, Pages 3559-3566

  Khalsa, Sahib S ^a,b,c   Feinstein, Justin S ^a,b,e   Li, Wei ^d   Feusner, Jamie D ^c   Adolphs, Ralph ^e   Hurlemann, Rene ^f  

^a LAUREATE INSTITUTE FOR BRAIN RESEARCH   (United States)

^b UNIVERSITY OF TULSA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d California Institute of Technology ^*  (United States)

^e CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^f UNIVERSITY OF BONN   (Germany)

Author keywords

Amygdala lesion; Anxiety; Emotion; Heartbeat; Interoception; Respiration

Indexed keywords

ISOPRENALINE; BETA ADRENERGIC RECEPTOR STIMULATING AGENT;

ADULT; AMPLITUDE MODULATION; AMYGDALOID NUCLEUS; ANXIETY DISORDER; ARTICLE; AWARENESS; CARDIORESPIRATORY FITNESS; CASE REPORT; CONTROLLED STUDY; FEMALE; FUNCTIONAL NEUROIMAGING; HEART RATE; HUMAN; INTEROCEPTION; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; SCORING SYSTEM; SIGNAL TRANSDUCTION; SKIN CONDUCTANCE; AMYGDALA; CHEMICALLY INDUCED; DRUG EFFECTS; HEART; INNERVATION; LUNG; MALE; PANIC; PATHOLOGY; PATHOPHYSIOLOGY; SENSORY NERVE; TWINS;

ADRENERGIC BETA-AGONISTS; ADULT; AFFERENT PATHWAYS; AMYGDALA; FEMALE; HEART; HUMANS; INTEROCEPTION; ISOPROTERENOL; LUNG; MALE; PANIC DISORDER;

EID: 84961664677     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4109-15.2016     Document Type: Article

References (73)

1. Adolphs R (2013) The biology of fear. Curr Biol 23:R79–R93. CrossRef Medline
2. Adolphs R, Gosselin F, Buchanan TW, Tranel D, Schyns P, Damasio AR (2005) A mechanism for impaired fear recognition after amygdala damage. Nature 433:68–72. CrossRef Medline
3. Alvarez RP, Chen G, Bodurka J, Kaplan R, Grillon C (2011) Phasic and sustained fear in humans elicits distinct patterns of brain activity. Neuroimage 55:389–400. CrossRef Medline
4. Amaral DG, Adolphs R (2015) Living without an amygdala. New York: Guilford. In press.
5. Asahina M, Suzuki A, Mori M, Kanesaka T, Hattori T (2003) Emotional sweating response in a patient with bilateral amygdala damage. Int J Psychophysiol 47:87–93. CrossRef Medline
6. Bach DR, Hurlemann R, Dolan RJ (2015) Impaired threat prioritisation after selective bilateral amygdala lesions. Cortex 63:206–213. CrossRef Medline
7. Balon R, Pohl R, Yeragani VK, Rainey JM, Weinberg P (1988) Lactate- and isoproterenol-induced panic attacks in panic disorder patients and controls. Psychiatry Res 23:153–160. CrossRef Medline
8. Battaglia M, Ogliari A, Harris J, Spatola CA, Pesenti-Gritti P, Reichborn-Kjennerud T, Torgersen S, Kringlen E, Tambs K (2007) A genetic study of the acute anxious response to carbon dioxide stimulation in man. J Psychiatr Res 41: 906–917. CrossRef Medline
9. Becker B, Mihov Y, Scheele D, Kendrick KM, Feinstein JS, Matusch A, Aydin M, Reich H, Urbach H, Oros-Peusquens AM, Shah NJ, Kunz WS, Schlaepfer TE, Zilles K, Maier W, Hurlemann R (2012) Fear processing and social networking in the absence of a functional amygdala. Biol Psychiatry 72:70–77. CrossRef Medline
10. Bellodi L, Perna G, Caldirola D, Arancio C, Bertani A, Di Bella D (1998) CO2-induced panic attacks: a twin study. Am J Psychiatry 155:1184–1188. CrossRef Medline
11. Borges N, Sarmento A, Azevedo I (1999) Dynamics of experimental vasogenic brain oedema in the rat: changes induced by adrenergic drugs. J Auton Pharmacol 19:209–217. CrossRef Medline
12. Brannan S, Liotti M, Egan G, Shade R, Madden L, Robillard R, Abplanalp B, Stofer K, Denton D, Fox PT (2001) Neuroimaging of cerebral activations and deactivations associated with hypercapnia and hunger for air. Proc Natl Acad Sci U S A 98:2029–2034. CrossRef Medline
13. Büchel C, Dolan RJ, Armony JL, Friston KJ (1999) Amygdala-hippocampal involvement in human aversive trace conditioning revealed through event-related functional magnetic resonance imaging. J Neurosci 19: 10869–10876. Medline
14. Cantril H, Hunt WA (1932) Emotional effects produced by the injection of adrenalin. Am J Psychol 44:300–307. CrossRef
15. Cechetto DF (1987) Central representation of visceral function. Fed Proc 46:17–23. Medline
16. Colasanti A, Esquivel G, Schruers KJ, Griez EJ (2012) On the psychotropic effects of carbon dioxide. Curr Pharm Des 18:5627–5637. CrossRef Medline
17. Coplan JD, Lydiard RB (1998) Brain circuits in panic disorder. Biol Psychiatry 44:1264–1276. CrossRef Medline
18. 2 as a trait of familial panic disorder. Biol Psychiatry 49:582–587. CrossRef Medline
19. Craske MG, Kircanski K, Epstein A, Wittchen HU, Pine DS, Lewis-Fernández R, Hinton D (2010) Panic disorder: a review of DSM-IV panic disorder and proposals for DSM-V. Depress Anxiety 27:93–112. CrossRef Medline
20. Crawford JR, Garthwaite PH (2002) Investigation of the single case in neuropsychology: confidence limits on the abnormality of test scores and test score differences. Neuropsychologia 40:1196–1208. CrossRef Medline
21. Crawford JR, Garthwaite PH, Howell DC, Venneri A (2003) Intra-individual measures of association in neuropsychology: inferential methods for comparing a single case with a control or normative sample. J Int Neuropsychol Soc 9:989–1000. CrossRef Medline
22. Davenport PW, Chan PY, Zhang W, Chou YL (2007) Detection threshold for inspiratory resistive loads and respiratory-related evoked potentials. J Appl Physiol 102:276–285. CrossRef Medline
23. Davis M, Whalen PJ (2001) The amygdala: vigilance and emotion. Mol Psychiatry 6:13–34. CrossRef Medline
24. Davis M, Walker DL, Miles L, Grillon C (2010) Phasic vs sustained fear in rats and humans: role of the extended amygdala in fear vs anxiety. Neuropsychopharmacology 35:105–135. CrossRef Medline
25. Duvarci S, Bauer EP, Paré D (2009) The bed nucleus of the stria terminalis mediates inter-individual variations in anxiety and fear. J Neurosci 29: 10357–10361. CrossRef Medline
26. Esquivel G, Schruers KR, Maddock RJ, Colasanti A, Griez EJ (2010) Acids in the brain: a factor in panic? J Psychopharmacol 24:639–647. CrossRef Medline
27. Etkin A, Wager TD (2007) Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. Am J Psychiatry 164:1476–1488. CrossRef Medline
28. Feinstein JS, Adolphs R, Damasio A, Tranel D (2011) The human amygdala and the induction and experience of fear. Curr Biol 21:34–38. CrossRef Medline
29. Feinstein JS, Buzza C, Hurlemann R, Follmer RL, Dahdaleh NS, Coryell WH, Welsh MJ, Tranel D, Wemmie JA (2013) Fear and panic in humans with bilateral amygdala damage. Nat Neurosci 16:270–272. CrossRef Medline
30. Gafford GM, Ressler KJ (2015) Mouse models of fear-related disorders: cell-type-specific manipulations in amygdala. Neuroscience. Advance online publication. CrossRef Medline
31. Garfinkel SN, Minati L, Gray MA, Seth AK, Dolan RJ, Critchley HD (2014) Fear from the heart: sensitivity to fear stimuli depends on individual heartbeats. J Neurosci 34:6573–6582. CrossRef Medline
32. Goossens L, Leibold N, Peeters R, Esquivel G, Knuts I, Backes W, Marcelis M, Hofman P, Griez E, Schruers K (2014) Brainstem response to hypercapnia: a symptom provocation study into the pathophysiology of panic disorder. J Psychopharmacol 28:449–456. CrossRef Medline
33. Gulbandilar E, Cimbiz A, Sari M, Ozden H (2008) Relationship between skin resistance level and static balance in type II diabetic subjects. Diabetes Res Clin Pract 82:335–339. CrossRef Medline
34. Guyenet PG, Abbott SB (2013) Chemoreception and asphyxia-induced arousal. Respir Physiol Neurobiol 188:333–343. CrossRef Medline
35. Hamann SB, Stefanacci L, Squire LR, Adolphs R, Tranel D, Damasio H, Damasio A (1996) Recognizing facial emotion. Nature 379:497. CrossRef Medline
36. James W (1884) What is an emotion? Mind 9:188–205.
37. Johnson PL, Fitz SD, Hollis JH, Moratalla R, Lightman SL, Shekhar A, Lowry CA (2011) Induction of c-Fos in “panic/defence”-related brain circuits following brief hypercarbic gas exposure. J Psychopharmacol 25:26–36. CrossRef Medline
38. Khalsa SS, Rudrauf D, Feinstein JS, Tranel D (2009a) The pathways of interoceptive awareness. Nat Neurosci 12:1494–1496. CrossRef Medline
39. Khalsa SS, Rudrauf D, Sandesara C, Olshansky B, Tranel D (2009b) Bolus isoproterenol infusions provide a reliable method for assessing interoceptive awareness. Int J Psychophysiol 72:34–45. CrossRef Medline
40. Khalsa SS, Craske MG, Li W, Vangala S, Strober M, Feusner JD (2015) Altered interoceptive awareness in anorexia nervosa: effects of meal anticipation, consumption and bodily arousal. Int J Eat Disord 48:889–897. CrossRef Medline
41. Koenigs M, Huey ED, Raymont V, Cheon B, Solomon J, Wassermann EM, Grafman J (2008) Focal brain damage protects against post-traumatic stress disorder in combat veterans. Nat Neurosci 11:232–237. CrossRef Medline
42. Lang CG (1885) The mechanisms of the emotions. In: The classical psychologist: selections illustrating psychology from Anaxagoras to Wundt, pp 672–684. Boston: Houghton Mifflin.
43. Lawrence AJ, Watkins D, Jarrott B (1995) Visualization of beta-adrenoceptor binding sites on human inferior vagal ganglia and their axonal transport along the rat vagus nerve. J Hypertens 13:631–635. CrossRef Medline
44. LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23: 155–184. CrossRef Medline
45. LeDoux JE (2013) The slippery slope of fear. Trends Cogn Sci 17:155–156. CrossRef Medline
46. Liebowitz MR, Fyer AJ, Gorman JM, Dillon D, Appleby IL, Levy G, Anderson S, Levitt M, Palij M, Davies SO. (1984) Lactate provocation of panic attacks: I. Clinical and behavioral findings. Arch Gen Psychiatry 41: 764–770. CrossRef Medline
47. Maddock RJ, Carter CS (1991) Hyperventilation-induced panic attacks in panic disorder with agoraphobia. Biol Psychiatry 29:843–854. CrossRef Medline
48. Maddock RJ, Buonocore MH, Miller AR, Yoon JH, Soosman SK, Unruh AM (2013) Abnormal activity-dependent brain lactate and glutamate plus glutamine responses in panic disorder. Biol Psychiatry 73:1111–1119. CrossRef Medline
49. Magnotta VA, Johnson CP, Follmer R, Wemmie JA (2014) Functional t1rho imaging in panic disorder. Biol Psychiatry 75:884–891. CrossRef Medline
50. Maranon G (1924) Contribution a l’etude de l’action emotive de l’adr-enaline. Revue Française d’Endocrinologie 2:301–325.
51. Meadows ME, Kaplan RF (1994) Dissociation of autonomic and subjective responses to emotional slides in right hemisphere damaged patients. Neuropsychologia 32:847–856. CrossRef Medline
52. Miyashita T, Williams CL (2006) Epinephrine administration increases neural impulses propagated along the vagus nerve: role of peripheral beta-adrenergic receptors. Neurobiol Learn Mem 85:116–124. CrossRef Medline
53. Mobbs D, Yu R, Rowe JB, Eich H, FeldmanHall O, Dalgleish T (2010) Neural activity associated with monitoring the oscillating threat value of a tarantula. Proc Natl Acad Sci U S A 107:20582–20586. CrossRef Medline
54. Murphy VA, Johanson CE (1985) Adrenergic-induced enhancement of brain barrier system permeability to small nonelectrolytes: choroid plexus versus cerebral capillaries. J Cereb Blood Flow Metab 5:401–412. CrossRef Medline
55. 2, brainstem chemoreceptors and breathing. Prog Neurobiol 59:299–331. CrossRef Medline
56. Nesse RM, Cameron OG, Curtis GC, McCann DS, Huber-Smith MJ (1984) Adrenergic function in patients with panic anxiety. Arch Gen Psychiatry 41:771–776. CrossRef Medline
57. Oler JA, Fox AS, Shelton SE, Rogers J, Dyer TD, Davidson RJ, Shelledy W, Oakes TR, Blangero J, Kalin NH (2010) Amygdalar and hippocampal substrates of anxious temperament differ in their heritability. Nature 466: 864–868. CrossRef Medline
58. Pattinson KT, Mitsis GD, Harvey AK, Jbabdi S, Dirckx S, Mayhew SD, Rogers R, Tracey I, Wise RG (2009) Determination of the human brainstem respiratory control network and its cortical connections in vivo using functional and structural imaging. Neuroimage 44:295–305. CrossRef Medline
59. Pine DS, Klein RG, Roberson-Nay R, Mannuzza S, Moulton JL 3rd, Wolde-hawariat G, Guardino M (2005) Response to 5% carbon dioxide in children and adolescents: relationship to panic disorder in parents and anxiety disorders in subjects. Arch Gen Psychiatry 62:73–80. CrossRef Medline
60. Pohl R, Yeragani VK, Balon R, Rainey JM, Lycaki H, Ortiz A, Berchou R, Weinberg P (1988) Isoproterenol-induced panic attacks. Biol Psychiatry 24:891–902. CrossRef Medline
61. 2. eLife 4:e07051. CrossRef Medline
62. Savage JE, McMichael O, Gorlin EI, Beadel JR, Teachman B, Vladimirov VI, Hettema JM, Roberson-Nay R (2015) Validation of candidate anxiety disorder genes using a carbon dioxide challenge task. Biol Psychol 109: 61–66. CrossRef Medline
63. Schachter S, Singer JE (1962) Cognitive, social, and psychological determinants of emotional state. Psychol Rev 69:379–399. CrossRef Medline
64. Scheele D, Mihov Y, Kendrick KM, Feinstein JS, Reich H, Maier W, Hurlemann R (2012) Amygdala lesion profoundly alters altruistic punishment. Biol Psychiatry 72:e5–7. CrossRef Medline
65. Shekhar A, Keim SR (1997) The circumventricular organs form a potential neural pathway for lactate sensitivity: implications for panic disorder. J Neurosci 17:9726–9735. Medline
66. Spunt RP, Elison JT, Dufour N, Hurlemann R, Saxe R, Adolphs R (2015) Amygdala lesions do not compromise the cortical network for false-belief reasoning. Proc Natl Acad Sci U S A 112:4827–4832. CrossRef Medline
67. Taugher RJ, Lu Y, Wang Y, Kreple CJ, Ghobbeh A, Fan R, Sowers LP, Wemmie JA (2014) The bed nucleus of the stria terminalis is critical for anxiety-related behavior evoked by CO2 and acidosis. J Neurosci 34: 10247–10255. CrossRef Medline
68. Terleph TA, Klein RG, Roberson-Nay R, Mannuzza S, Moulton JL III, Wol-dehawariat G, Guardino M, Pine DS (2006) Stress responsivity and HPA axis activity in juveniles: results from a home-based CO2 inhalation study. Am J Psychiatry 163:738–740. CrossRef Medline
69. Tranel D, Damasio H (1989) Intact electrodermal skin conductance responses after bilateral amygdala damage. Neuropsychologia 27:381–390. CrossRef Medline
70. Tranel D, Damasio H (1994) Neuroanatomical correlates of electrodermal skin conductance responses. Psychophysiology 31:427–438. CrossRef Medline
71. Tye KM, Prakash R, Kim SY, Fenno LE, Grosenick L, Zarabi H, Thompson KR, Gradinaru V, Ramakrishnan C, Deisseroth K (2011) Amygdala circuitry mediating reversible and bidirectional control of anxiety. Nature 471:358–362. CrossRef Medline
72. Wiest G, Lehner-Baumgartner E, Baumgartner C (2006) Panic attacks in an individual with bilateral selective lesions of the amygdala. Arch Neurol 63:1798–1801. CrossRef Medline
73. Ziemann AE, Allen JE, Dahdaleh NS, Drebot II, Coryell MW, Wunsch AM, Lynch CM, Faraci FM, Howard MA III, Welsh MJ, Wemmie JA (2009) The amygdala is a chemosensor that detects carbon dioxide and acidosis to elicit fear behavior. Cell 139:1012–1021. CrossRef Medline