Subchronic SSRI administration reduces insula response during affective anticipation in healthy volunteers

International Journal of Neuropsychopharmacology

Volumn 12, Issue 8, 2009, Pages 1009-1020

  Simmons, Alan N ^a,b   Arce, Estibaliz ^a   Lovero, Kathryn L ^b   Stein, Murray B ^a,b   Paulus, Martin P ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

Author keywords

Anticipation; Escitalopram; FMRI; Insula; SSRI

Indexed keywords

BIOLOGICAL MARKER; ESCITALOPRAM; PLACEBO;

ADULT; ANTICIPATION; ANXIETY; ARTICLE; ASSOCIATION; CINGULATE GYRUS; CONTROLLED STUDY; DRUG DOSE REDUCTION; DRUG EFFECT; DRUG WITHDRAWAL; EMOTION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; INSULA; NORMAL HUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; STIMULUS RESPONSE; TASK PERFORMANCE; TRANQUILIZING ACTIVITY;

ADULT; ATTENTION; BRAIN MAPPING; CEREBRAL CORTEX; CITALOPRAM; CROSS-OVER STUDIES; DOUBLE-BLIND METHOD; EMOTIONS; FEMALE; GYRUS CINGULI; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; NEUROPSYCHOLOGICAL TESTS; OXYGEN; PHOTIC STIMULATION; PSYCHOMOTOR PERFORMANCE; SEROTONIN UPTAKE INHIBITORS; YOUNG ADULT;

EID: 69749088033     PISSN: 14611457     EISSN: 14695111     Source Type: Journal    
DOI: 10.1017/S1461145709990149     Document Type: Article

References (118)

1. Amodio DM, Frith CD (2006). Meeting of minds: the medial frontal cortex and social cognition. Nature Reviews Neuroscience 7, 268-277.
2. An X, Bandler R, Ongur D, Price JL (1998). Prefrontal cortical projections to longitudinal columns in the midbrain periaqueductal gray in macaque monkeys. Journal of Comparative Neurology 401, 455-479.
3. Arce E, Miller DA, Feinstein JS, Stein MB, Paulus MP (2006). Lorazepam dose-dependently decreases risk-taking related activation in limbic areas. Psychopharmacology (Berlin) 189, 105-116.
4. Arce E, Simmons AN, Lovero KL, Stein MB, Paulus MP (2007). Escitalopram effects on insula and amygdala BOLD activation during emotional processing. Psychopharmacology (Berlins) 196, 661-672.
5. Augustine JR (1996). Circuitary and functional aspects of the insular lobe in primates including humans. Brain Research Reviews 22, 229-244.
6. Bagdy G, Graf M, Anheuer ZE, Modos EA, Kantor S (2001). Anxiety-like effects induced by acute fluoxetine, sertraline or m-CPP treatment are reversed by pretreatment with the 5-HT2C receptor antagonist SB-242084 but not the 5-HT1A receptor antagonist WAY-100635. International Journal of Neuropsychopharmacology 4, 399-408.
7. Beauregard M, Levesque J, Bourgouin P (2001). Neural correlates of conscious self-regulation of emotion. Journal of Neuroscience 21, RC165.
8. Beck AT, Ward CH, Medelson M, Mock J, Erbaugh J (1961). An inventory for measuring depression. Archives of General Psychiatry 4, 561-571.
9. Bermpohl F, Pascual-Leone A, Amedi A, Merabet LB, et al. (2006a). Attentional modulation of emotional stimulus processing: an fMRI study using emotional expectancy. Human Brain Mapping 27, 662-677.
10. Bermpohl F, Pascual-Leone A, Amedi A, Merabet LB, et al. (2006b). Dissociable networks for the expectancy and perception of emotional stimuli in the human brain. Neuroimage 30, 588-600.
11. Bermudez-Rattoni F, Ramirez-Lugo L, Gutierrez R, Miranda MI (2004). Molecular signals into the insular cortex and amygdala during aversive gustatory memory formation. Cellular and Molecular Neurobiology 24, 25-36.
12. 11C]MDL 100,907. American Journal of Psychiatry 163, 1580-1587.
13. Bremner JD, Vermetten E, Vythilingam M, Afzal N, et al. (2004). Neural correlates of the classic color and emotional stroop in women with abuse-related posttraumatic stress disorder. Biological Psychiatry 55, 612-620.
14. Britton JC, Phan KL, Taylor SF, Fig LM, Liberzon I (2005). Corticolimbic blood flow in posttraumatic stress disorder during script-driven imagery. Biological Psychiatry 57, 832-840.
15. Brown SM, Hariri AR (2006). Neuroimaging studies of serotonin gene polymorphisms: exploring the interplay of genes, brain, and behavior. Cognitive, Affective, and Behavioral Neuroscience 6, 44-52.
16. Browning M, Reid C, Cowen PJ, Goodwin GM, Harmer C (2007). A single dose of citalopram increases fear recognition in healthy subjects. Journal of Psychopharmacology 21, 684-690.
17. Burke WJ, Gergel I, Bose A (2002). Fixed-dose trial of the single isomer SSRI escitalopram in depressed outpatients. Journal of Clinical Psychiatry 63, 331-336.
18. Bush G, Luu P, Posner MI (2000). Cognitive and emotional influences in anterior cingulate cortex. Trends in Cognitive Sciences 4, 215-222.
19. Bystritsky A, Pontillo D, Powers M, Sabb FW, et al. (2001). Functional MRI changes during panic anticipation and imagery exposure. Neuroreport 12, 3953-3957.
20. Carrasco JL, Sandner C (2005). Clinical effects of pharmacological variations in selective serotonin reuptake inhibitors: an overview. International Journal of Clinical Practice 59, 1428-1434.
21. Chen CH, Ridler K, Suckling J, Williams S, et al. (2007). Brain imaging correlates of depressive symptom severity and predictors of symptom improvement after antidepressant treatment. Biological Psychiatry 62, 407-414.
22. Chua P, Krams M, Toni I, Passingham R, olan R (1999). A functional anatomy of anticipatory anxiety. Neuroimage 9, 563-571.
23. Cox RW (1996). AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research 29, 162-173.
24. Craig AD (2002). How do you feel? Interoception: the sense of the physiological condition of the body. Nature Reviews Neuroscience 3, 655-666.
25. Craig AD (2003). Interoception: the sense of the physiological condition of the body. Current Opinion in Neurobiology 13, 500-505.
26. Craig ADB (2005). Forebrain emotional asymmetry: a neuroanatomical basis? Trends in Cognitive Sciences 9, 566-571.
27. Critchley HD (2004). The human cortex responds to an interoceptive challenge. Proceedings of the National Academy of Sciences USA 101, 6333-6334.
28. Critchley HD, Mathias CJ, Dolan RJ (2001). Neural activity in the human brain relating to uncertainty and arousal during anticipation. Neuron 29, 537-545.
29. Critchley HD, Mathias CJ, Josephs O, O'Doherty J, et al. (2003). Human cingulate cortex and autonomic control: converging neuroimaging and clinical evidence. Brain 126, 2139-2152.
30. Deakin JF (1998). The role of serotonin in panic, anxiety and depression. International Clinical Psychopharmacology 13 (Suppl. 4), S1-5.
31. Del-Ben CM, Deakin JF, McKie S, Delvai NA, et al. (2005). The effect of citalopram pretreatment on neuronal responses to neuropsychological tasks in normal volunteers: an FMRI study. Neuropsychopharmacology 30, 1724-1734.
32. Derogatis LR, Melisaratos N (1983). The brief symptom inventory: an introductory report. Psychological Medicine 13, 595-605.
33. Devinsky O, Morrell MJ, Vogt BA (1995). Contributions of anterior cingulate cortex to behavior. Brain 118, 279-306.
34. Dupont S, Bouilleret V, Hasboun D, Semah F, Baulac M (2003). Functional anatomy of the insula: new insights from imaging. Surgical and Radiologic Anatomy 25, 113-119.
35. Etkin A, Wager TD (2007). Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. American Journal of Psychiatry 164, 1476-1488.
36. Eysenck MW (1997). Anxiety and Cognition: a Unified Theory. Hove, UK: Psychology Press.
37. Feldman JL, Mitchell GS, Nattie EE (2003). Breathing. Annual Review of Neuroscience 26, 239-266.
38. Fernandez M, Pissiota A, Frans O, von Knorring L, et al. (2001). Brain function in a patient with torture related post-traumatic stress disorder before and after fluoxetine treatment: a positron emission tomography provocation study. Neuroscience Letters 297, 101-104.
39. First MB, Spitzer RL, Gibbon M, Williams JBW (2002). Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Non-patient Edition (SCID-I/NP). New York Biometrics Research, New York State Psychiatric Institute.
40. Fox MD, Snyder AZ, Vincent JL, Corbetta M, et al. (2005). The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proceedings of the National Academy of Sciences USA 102, 9673-9678.
41. Fu CH, Williams SC, Brammer MJ, Suckling J, et al. (2007). Neural responses to happy facial expressions in major depression following antidepressant treatment. American Journal of Psychiatry 164, 599-607.
42. Fu CH, Williams SC, Cleare AJ, Brammer MJ, et al. (2004). Attenuation of the neural response to sad faces in major depression by antidepressant treatment: a prospective, event-related functional magnetic resonance imaging study. Archives of General Psychiatry 61, 877-889.
43. Goldapple K, Segal Z, Garson C, Lau M, et al. (2004). Modulation of cortical-limbic pathways in major depression: treatment-specific effects of cognitive behavior therapy. Archives of General Psychiatry 61, 34-41.
44. Graeff FG, Guimaraes FS, DeAndrade T, Deakin JFW (1996). Role of 5-HT in stress, anxiety, and depression. Pharmacology Biochemistry and Behavior 54, 129-141.
45. Greenwood BN, Strong PV, Brooks L, Fleshner M (2008). Anxiety-like behaviors produced by acute fluoxetine administration in male Fischer 344 rats are prevented by prior exercise. Psychopharmacology (Berlin) 199, 209-222.
46. Grillon C (2008). Models and mechanisms of anxiety: evidence from startle studies. Psychopharmacology (Berlin) 199, 421-437.
47. Grillon C, Levenson J, Pine DS (2007). A single dose of the selective serotonin reuptake inhibitor citalopram exacerbates anxiety in humans: a fear-potentiated startle study. Neuropsychopharmacology 32, 225-231.
48. Gusnard DA, Akbudak E, Shulman GL, Raichle ME (2001). Medial prefrontal cortex and self-referential mental activity: relation to a default mode of brain function. Proceedings of the National Academy of Sciences USA 98, 4259-4264.
49. Hariri AR, Brown SM (2006). Serotonin. American Journal of Psychiatry 163, 12.
50. Hariri AR, Drabant EM, Weinberger DR (2006). Imaging genetics: perspectives from studies of genetically driven variation in serotonin function and corticolimbic affective processing. Biological Psychiatry 59, 888-897.
51. Harmer CJ, Mackay CE, Reid CB, Cowen PJ, Goodwin GM (2006). Antidepressant drug treatment modifies the neural processing of nonconscious threat cues. Biological Psychiatry 59, 816-820.
52. Harmer CJ, Shelley NC, Cowen PJ, Goodwin GM (2004). Increased positive versus negative affective perception and memory in healthy volunteers following selective serotonin and norepinephrine reuptake inhibition. American Journal of Psychiatry 161, 1256-1263.
53. Heatherton TF, Wyland CL, Macrae CN, Demos KE, et al. (2006). Medial prefrontal activity differentiates self from close others. Scan 1, 18-25.
54. Hood SD, Hince DA, Robinson H, Cirillo M, et al. (2006). Serotonin regulation of the human stress response. Psychoneuroendocrinology 31, 1087-1097.
55. Huettel SA, Mack PB, McCarthy G (2002). Perceiving patterns in random series: dynamic processing of sequence in prefrontal cortex. Nature Neuroscience 5, 485-490.
56. Johnson SC, Schmitz TW, Kawahara-Baccus TN, Rowley HA, et al. (2005). The cerebral response during subjective choice with and without self-reference. Journal of Cognitive Neuroscience 17, 1897-1906.
57. Kalisch R, Wiech K, Critchley HD, Dolan RJ (2006). Levels of appraisal: a medial prefrontal role in high-level appraisal of emotional material. Neuroimage 30, 1458-1466.
58. Keenan JP, Wheeler MA, Gallup Jr. G.G., Pascual-Leone A (2000). Self-recognition and the right prefrontal cortex. Trends in Cognitive Sciences 4, 338-344.
59. Kennedy SH, Evans KR, Kruger S, Mayberg HS, et al. (2001). Changes in regional brain glucose metabolism measured with positron emission tomography after paroxetine treatment of major depression. American Journal of Psychiatry 158, 899-905.
60. Kent JM, Coplan JD, Gorman JM (1998). Clinical utility of the selective serotonin reuptake inhibitors in the spectrum of anxiety. Biological Psychiatry 44, 812-824.
61. 123I]ADAM in healthy subjects administered different doses of escitalopram or citalopram. Psychopharmacology (Berlin) 188, 263-272.
62. 123I]ADAM SPECT study. Psychopharmacology (Berlin) 191, 333-339.
63. Lang PJ, Bradley MM, Cuthbert BN (1998). Emotion and motivation: measuring affective perception. Journal of Clinical Neurophysiology 15, 397-408.
64. Lanzenberger RR, Mitterhauser M, Spindelegger C, Wadsak W, et al. (2007). Reduced serotonin-1A receptor binding in social anxiety disorder. Biological Psychiatry 61, 1081-1089.
65. Likhtik E, Pelletier JG, Paz R, Pare D (2005). Prefrontal control of the amygdala. Journal of Neuroscience 25, 7429-7437.
66. Lorberbaum JP, Kose S, Johnson MR, Arana GW, et al. (2004). Neural correlates of speech anticipatory anxiety in generalized social phobia. Neuroreport 15, 2701-2705.
67. Malizia AL, Cunningham VJ, Bell CJ, Liddle PF, et al. (1998). Decreased brain GABA(A)-benzodiazepine receptor binding in panic disorder: preliminary results from a quantitative PET study. Archives of General Psychiatry 55, 715-720.
68. Mars RB, Coles MG, Grol MJ, Holroyd CB, et al. (2005). Neural dynamics of error processing in medial frontal cortex. Neuroimage 28, 1007-1013.
69. Masand PS, Gupta S (1999). Selective serotonin-reuptake inhibitors: an update. Harvard Review of Psychiatry 7, 69-84.
70. Masaoka Y, Homma I (1997). Anxiety and respiratory patterns: their relationship during mental stress and physical load. International Journal of Psychophysiology 27, 153-159.
71. Masaoka Y, Homma I (2001). The effect of anticipatory anxiety on breathing and metabolism in humans. Respiratory Physiology and Neurobiology 128, 171-177.
72. Masaoka Y, Onaka Y, Shimizu Y, Sakurai S, Homma I (2007). State anxiety dependent on perspiration during mental stress and deep inspiration. Journal of Physiological Sciences 57, 121-126.
73. Mattick RP, Clarke JC (1998). Development and validation of measures of social phobia scrutiny fear and social interaction anxiety. Behaviour Research and Therapy 36, 455-470.
74. Mayberg HS (2002). Modulating limbic-cortical circuits in depression: targets of antidepressant treatments. Seminars in Clinical Neuropsychiatry 7, 255-268.
75. Meyer JH, Kapur S, Eisfeld B, Brown GM, et al. (2001). The effect of paroxetine on 5-HT(2A) receptors in depression: an [(18)F]setoperone PET imaging study. American Journal of Psychiatry 158, 78-85.
76. Mineka S, Watson D, Clark LA (1998). Comorbidity of anxiety and unipolar mood disorders. Annual Review Psychology 49, 377-412.
77. Nitschke JB, Sarinopoulos I, Mackiewicz KL, Schaefer HS, Davidson RJ (2006). Functional neuroanatomy of aversion and its anticipation. Neuroimage 29, 106-116.
78. Northoff G, Bermpohl F (2004). Cortical midline structures and the self. Trends in Cognitive Sciences 8, 102-107.
79. Nutt DJ, Forshall S, Bell C, Rich A, et al. (1999). Mechanisms of action of selective serotonin reuptake inhibitors in the treatment of psychiatric disorders. European Neuropsychopharmacology 9 (Suppl. 3), S81-86.
80. Obrist PA, Webb RA, Sutterer JR (1969). Heart rate and somatic changes during aversive conditioning and a simple reaction time task. Psychophysiology 5, 696-723.
81. Ongur D, An X, Price JL (1998). Prefrontal cortical projections to the hypothalamus in macaque monkeys. Journal of Comparative Neurology 401, 480-505.
82. Ongur D, Ferry AT, Price JL (2003). Architectonic subdivision of the human orbital and medial prefrontal cortex. Journal of Comparative Neurology 460, 425-449.
83. Paulus MP, Feinstein JS, Castillo G, Simmons AN, Stein MB (2005). Dose-dependent decrease of activation in bilateral amygdala and insula by lorazepam during emotion processing. Archives of General Psychiatry 62, 282-288.
84. Paulus MP, RogalskyC, Simmons A, Feinstein JS, Stein MB (2003). Increased activation in the right insula during risk-taking decision making is related to harm avoidance and neuroticism. Neuroimage 19, 1439-1448.
85. Paulus MP, Stein MB (2006). An insular view of anxiety. Biological Psychiatry 60, 383-387.
86. Paulus MP, Stein MB (2007). Role of functional magnetic resonance imaging in drug discovery. Neuropsychology Review 17, 179-188.
87. Phan KL, Britton JC, Taylor SF, Fig LM, Liberzon I (2006). Corticolimbic blood flow during nontraumatic emotional processing in posttraumatic stress disorder. Archives of General Psychiatry 63, 184-192.
88. Phan KL, Taylor SF, Welsh RC, Decker LR, et al. (2003). Activation of the medial prefrontal cortex and extended amygdala by individual ratings of emotional arousal: a fMRI study. Biological Psychiatry 53, 211-215.
89. Ploghaus A, Tracey I, Gati JS, Clare S, et al. (1999). Dissociating pain from its anticipation in the human brain. Science 284, 1979-1981.
90. Porro CA, Baraldi P, Pagnoni G, Serafini M, et al. (2002). Does anticipation of pain affect cortical nociceptive systems? Journal of Neuroscience 22, 3206-3214.
91. Quirk GJ, Likhtik E, Pelletier JG, Pare D (2003). Stimulation of medial prefrontal cortex decreases the responsiveness of central amygdala output neurons. Journal of Neuroscience 23, 8800-8807.
92. Ressler KJ, Mayberg HS (2007). Targeting abnormal neural circuits in mood and anxiety disorders: from the laboratory to the clinic. Nature Neuroscience 10, 1116-1124.
93. Richter DW, Manzke T, Wilken B, Ponimaskin E (2003). Serotonin receptors: guardians of stable breathing. Trends in Molecular Medicine 9, 542-548.
94. Rose EJ, Simonotto E, Spencer EP, Ebmeier KP (2006). The effects of escitalopram on working memory and brain activity in healthy adults during performance of the n-back task. Psychopharmacology (Berlin) 185, 339-347.
95. Sawamoto N, Honda M, Okada T, Hanakawa T, et al. (2000). Expectation of pain enhances responses to nonpainful somatosensory stimulation in the anterior cingulate cortex and parietal operculum/posterior insula: an event-related functional magnetic resonance imaging study. Journal of Neuroscience 20, 7438-7445.
96. Sheline YI, Barch DM, Donnelly JM, Ollinger JM, et al. (2001). Increased amygdala response to masked emotional faces in depressed subjects resolves with antidepressant treatment: an fMRI study. Biological Psychiatry 50, 651-658.
97. Shi CJ, Cassell MD (1998). Cortical, thalamic, and amygdaloid connections of the anterior and posterior insular cortices. Journal of Comparative Neurology 399, 440-468.
98. Simmons A, Matthews SC, Stein MB, Paulus MP (2004). Anticipation of emotionally aversive visual stimuli activates right insula. Neuroreport 15, 2261-2265.
99. Simmons A, Strigo I, Matthews SC, Paulus MP, Stein MB (2006). Anticipation of aversive visual stimuli is associated with increased insula activation in anxiety-prone subjects. Biological Psychiatry 60, 402-409.
100. Simmons AN, Paulus MP, Thorpe SR, Matthews SC, et al. (2008). Functional activation and neural networks in women with posttraumatic stress disorder related to intimate partner violence. Biological Psychiatry 64, 681-690.
101. Simpson Jr. J.R., Drevets WC, Snyder AZ, Gusnard DA, Raichle ME (2001). Emotion-induced changes in human medial prefrontal cortex: II. During anticipatory anxiety. Proceedings of the National Academy of Sciences USA 98, 688-693.
102. Sotres-Bayon F, Cain CK, LeDoux JE (2006). Brain mechanisms of fear extinction: historical perspectives on the contribution of prefrontal cortex. Biological Psychiatry 60, 329-336.
103. Spielberger CD, Gorsuch RL, Lushene R, Vagg PR, Jacobs GA (1983). Manual for the State-Trait Anxiety Inventory. Palo Alto, CA: Consulting Psychologists.
104. Stein MB, Simmons AN, Feinstein JS, Paulus MP (2006). Increased amygdala and insula activation during emotion processing in anxiety-prone subjects. American Journal of Psychiatry 164, 318-327.
105. Strigo I, Simmons A, Craig AD, Paulus MP (2006). Breathing and BOLD fMRI: Watch Out. Atlanta, GA: Society for Neuroscience.
106. Takahashi H, Yahata N, Koeda M, Takano A, et al. (2005). Effects of dopaminergic and serotonergic manipulation on emotional processing: a pharmacological fMRI study. Neuroimage 27, 991-1001.
107. Talairach J, Tournoux P (1998). Co-planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging. New York, NY: Thieme Medical Publishers, Inc.
108. Taylor MJ, Freemantle N, Geddes JR, Bhagwagar Z (2006). Early onset of selective serotonin reuptake inhibitor antidepressant action: systematic review and meta-analysis. Archives of General Psychiatry 63, 1217-1223.
109. Van der Linden G, van Heerden B, Warwick J, Wessels C, et al. (2000a). Functional brain imaging and pharmacotherapy in social phobia: single photon emission computed tomography before and after treatment with the selective serotonin reuptake inhibitor citalopram. Progress in Neuro-Psychopharmacology and Biological Psychiatry 24, 419-438.
110. van der Linden GJ, Stein DJ, van Balkom AJ (2000b). The efficacy of the selective serotonin reuptake inhibitors for social anxiety disorder (social phobia): a meta-analysis of randomized controlled trials. International Clinical Psychopharmacology 15 (Suppl. 2), S15-23.
111. Vaswani M, Linda FK, Ramesh S (2003). Role of selective serotonin reuptake inhibitors in psychiatric disorders: a comprehensive review. Progress in Neuro-Psychopharmacology and Biological Psychiatry 27, 85-102.
112. Vollm B, Richardson P, McKie S, Elliott R, et al. (2006). Serotonergic modulation of neuronal responses to behavioural inhibition and reinforcing stimuli: an fMRI study in healthy volunteers. European Journal of Neuroscience 23, 552-560.
113. Wade A, Michael Lemming O, Bang Hedegaard K (2002). Escitalopram 10 mg/day is effective and well tolerated in a placebo-controlled study in depression in primary care. International Clinical Psychopharmacology 17, 95-102.
114. Waugh J, Goa KL (2003). Escitalopram: a review of its use in the management of major depressive and anxiety disorders. CNS Drugs 17, 343-362.
115. Whalen PJ, Bush G, McNally RJ, Wilhelm S, et al. (1998). The emotional counting Stroop paradigm: a functional magnetic resonance imaging probe of the anterior cingulate affective division. Biological Psychiatry 44, 1219-1228.
116. Wicker B, Ruby P, Royet JP, Fonlupt P (2003). A relation between rest and the self in the brain? Brain Research Reviews 43, 224-230.
117. Wise RG, Tracey I (2006). The role of fMRI in drug discovery. Journal of Magnetic Resonance Imaging 23, 862-876.
118. Wright CI, Martis B, McMullin K, Shin LM, Rauch SL (2003). Amygdala and insular responses to emotionally valenced human faces in small animal specific phobia. Biological Psychiatry 54, 1067-1076.