Psychiatry Research: Neuroimaging
Volume 172, Issue 2 , Pages 103-108 , 15 May 2009

Disentangling the web of fear: Amygdala reactivity and functional connectivity in spider and snake phobia

  • Fredrik Åhs

      Affiliations

    • Department of Psychology, Uppsala University, Uppsala, Sweden
    • Corresponding Author InformationCorresponding author. Department of Psychology, Uppsala University, Box 1225, SE-751 42 Uppsala, Sweden. Tel.: +46 18 471 78 43; fax: +46 18 471 21 23.
    • ,
  • Anna Pissiota

      Affiliations

    • Unit for Transcultural Psychiatry, Uppsala University, Uppsala, Sweden
    • ,
  • Åsa Michelgård

      Affiliations

    • Department of Clinical Neuroscience, Uppsala University, Uppsala, Sweden
    • ,
  • Örjan Frans

      Affiliations

    • Department of Psychology, Uppsala University, Uppsala, Sweden
    • ,
  • Tomas Furmark

      Affiliations

    • Department of Psychology, Uppsala University, Uppsala, Sweden
    • ,
  • Lieuwe Appel

      Affiliations

    • Uppsala Imanet, GE Healthcare, Uppsala, Sweden
    • ,
  • Mats Fredrikson

      Affiliations

    • Department of Psychology, Uppsala University, Uppsala, Sweden

Received 19 June 2008 ,Revised 23 September 2008 ,Accepted 11 November 2008.

References 

  1. Alkire MT, Haier RJ, Fallon JH, Cahill L. Hippocampal, but not amygdala, activity at encoding correlates with long-term, free recall of nonemotional information. Proceedings of the National Academy of Sciences of the United States of America. 1998;95(24):14506–14510
  2. American Psychiatric Association . Diagnostic and Statistical Manual of Mental Disorders, Fourth Ed. Washington, DC: American Psychiatric Press; 1994;
  3. Baas D, Aleman A, Kahn RS. Lateralization of amygdala activation: a systematic review of functional neuroimaging studies. Brain Research. 2004;45(2):96–103
  4. Buchel C, Dolan RJ. Classical fear conditioning in functional neuroimaging. Current Opinion Neurobiology. 2000;10(2):219–223
  5. Cannistraro PA, Rauch SL. Neural circuitry of anxiety: evidence from structural and functional neuroimaging studies. Psychopharmacologyl Bulletin. 2003;37(4):8–25
  6. Carlsson K, Petersson KM, Lundqvist D, Karlsson A, Ingvar M, Öhman A. Fear and the amygdala: manipulation of awareness generates differential cerebral responses to phobic and fear-relevant (but nonfeared) stimuli. Emotion. 2004;4(4):340–353
  7. Davis M, Whalen PJ. The amygdala: vigilance and emotion. Molecular Psychiatry. 2001;6(1):13–34
  8. Dilger S, Straube T, Mentzel HJ, Fitzek C, Reichenbach JR, Hecht H, et al. Brain activation to phobia-related pictures in spider phobic humans: an event-related functional magnetic resonance imaging study. Neuroscience Letters. 2003;348(1):29–32
  9. Etkin A, Wager TD. Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. American Journal of Psychiatry. 2007;164(10):1476–1488
  10. Fredrikson M. Reliability and validity of some specific fear questionnaires. Scandinavian Journal of Psychology. 1983;24(4):331–334
  11. Fredrikson M, Furmark T. Amygdaloid regional cerebral blood flow and subjective fear during symptom provocation in anxiety disorders. Annals of the New York Academy of Science. 2003;985:341–347
  12. Fredrikson M, Wik G, Greitz T, Eriksson L, Stone-Elander S, Ericson K, et al. Regional cerebral blood flow during experimental phobic fear. Psychophysiology. 1993;30(1):126–130
  13. Fredrikson M, Wik G, Annas P, Ericson K, Stone-Elander S. Functional neuroanatomy of visually elicited simple phobic fear: additional data and theoretical analysis. Psychophysiology. 1995;32(1):43–48
  14. Friston KJ, Holmes AP, Worsley KJ, Poline JB, Frith CD, Frackowiak RSJ. Statistical parametric maps in functional imaging: a general linear approach. Human Brain Mapping. 1994;2:189–210
  15. Furmark T, Fischer H, Wik G, Larsson M, Fredrikson M. The amygdala and individual differences in human fear conditioning. Neuroreport. 1997;8(18):3957–3960
  16. Genovese CR, Lazar NA, Nichols T. Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage. 2002;15(4):870–878
  17. Goosens L, Schruers K, Peeters R, Griez E, Sunaert S. Visual presentation of phobic stimuli: amygdala activation via an extrageniculostriate pathway?. Psychiatry Research: Neuroimaging. 2007;155(2):113–120
  18. Goosens L, Sunaert S, Peeters R, Griez EJ, Schruers KR. Amygdala hyperfunction in phobic fear normalizes after exposure. Biological Psychiatry. 2007;62(10):1119–1125
  19. Johanson A, Gustafson L, Passant U, Risberg J, Smith G, Warkentin S, et al. Brain function in spider phobia. Psychiatry Research: Neuroimaging. 1998;84(2–3):101–111
  20. 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. Archives of General Psychiatry. 2005;62(6):617–627
  21. Kim H, Somerville LH, Johnstone T, Alexander AL, Whalen PJ. Inverse amygdala and medial prefrontal cortex responses to surprised faces. Neuroreport. 2003;14(18):2317–2322
  22. Klorman R, Weerts TC, Hastings JE, Melamed BG, Lang PJ. Psychometric description of some specific fear questionnaires. Behavior Therapy. 1974;5(3):401–409
  23. Lancaster JL, Woldorff MG, Parsons LM, Liotti M, Freitas CS, Rainey L, et al. Automated Talairach atlas labels for functional brain mapping. Human Brain Mapping. 2000;10(3):120–131
  24. Larson CL, Schaefer HS, Siegle GJ, Jackson CA, Anderle MJ, Davidson RJ. Fear is fast in phobic individuals: amygdala activation in response to fear-relevant stimuli. Biological Psychiatry. 2006;60(4):410–417
  25. LeDoux J. The emotional brain, fear, and the amygdala. Cellular and Molecular Neurobiology. 2003;23(4–5):727–738
  26. Mai JK, Assheuer J, Paxinos G. Atlas of the Human Brain. San Diego: Elsevier Academic Press; 2004;
  27. Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage. 2003;19(3):1233–1239
  28. Maren S, Quirk GJ. Neuronal signalling of fear memory. Nature Reviews. 2004;5(11):844–852
  29. Meyer-Lindenberg A, Mervis CB, Sarpal D, Koch P, Steele S, Kohn P, et al. Functional, structural, and metabolic abnormalities of the hippocampal formation in Williams syndrome. Journal of Clinical Investigation. 2005;115(7):1888–1895
  30. Michelgård A, Appel L, Pissiota A, Frans O, Långström B, Bergström M, et al. Symptom provocation in specific phobia affects the substance P neurokinin-1 receptor system. Biological Psychiatry. 2007;61(8):1002–1006
  31. Milad MR, Rauch SL, Pitman RK, Quirk GJ. Fear extinction in rats: implications for human brain imaging and anxiety disorders. Biological Psychology. 2006;73(1):61–71
  32. 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. Archives of General Psychiatry. 1989;46(6):501–504
  33. O'Carroll RE, Moffoot AP, Van Beck M, Dougall N, Murray C, Ebmeier KP, et al. The effect of anxiety induction on the regional uptake of 99mTc-exametazime in simple phobia as shown by single photon emission tomography (SPET). Journal of Affective Disorders. 1993;28(3):203–210
  34. Paquette V, Levesque J, Mensour B, Leroux JM, Beaudoin G, Bourgouin P, et al. “Change the mind and you change the brain”: effects of cognitive-behavioral therapy on the neural correlates of spider phobia. Neuroimage. 2003;18(2):401–409
  35. Pezawas L, Meyer-Lindenberg A, Drabant EM, Verchinski BA, Munoz KE, Kolachana BS, et al. 5-HTTLPR polymorphism impacts human cingulate–amygdala interactions: a genetic susceptibility mechanism for depression. Nature Neuroscience. 2005;8(6):828–834
  36. Phelps EA, Delgado MR, Nearing KI, LeDoux JE. Extinction learning in humans: role of the amygdala and vmPFC. Neuron. 2004;43(6):897–905
  37. Pissiota A, Frans O, Fernandez M, von Knorring L, Fischer H, Fredrikson M. Neurofunctional correlates of posttraumatic stress disorder: a PET symptom provocation study. European Archives of Psychiatry and Clinical Neuroscience. 2002;252(2):68–75
  38. Pissiota A, Frans O, Michelgård A, Appel L, Långström B, Flaten MA, et al. Amygdala and anterior cingulate cortex activation during affective startle modulation: a PET study of fear. European Journal of Neuroscience. 2003;18(5):1325–1331
  39. Quirk GJ, Garcia R, Gonzalez-Lima F. Prefrontal mechanisms in extinction of conditioned fear. Biological Psychiatry. 2006;60(4):337–343
  40. Rauch SL, Savage CR, Alpert NM, Miguel EC, Baer L, Breiter HC, et al. A positron emission tomographic study of simple phobic symptom provocation. Archives of General Psychiatry. 1995;52(1):20–28
  41. Rolls ET. The orbitofrontal cortex and reward. Cerebral Cortex. 2000;10(3):284–294
  42. Sabatinelli D, Lang PJ, Keil A, Bradley MM. Parallel amygdala and inferotemporal activation reflect emotional intensity and fear relevance. Neuroimage. 2005;24(4):1265–1270
  43. Sabatinelli D, Lang PJ, Keil A, Bradley MM. Emotional perception: correlation of functional MRI and event-related potentials. Cerebral Cortex. 2007;17(5):1085–1091
  44. Schienle A, Schafer A, Walter B, Stark R, Vaitl D. Brain activation of spider phobics towards disorder-relevant, generally disgust- and fear-inducing pictures. Neuroscience Letters. 2005;388(1):1–6
  45. Schienle A, Schafer A, Hermann A, Rohrmann S, Vaitl D. Symptom provocation and reduction in patients suffering from spider phobia: An fMRI study on exposure therapy. European Archives of Psychiatry and Clinical Neuroscience. 2007;257(8):486–493
  46. 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. Biological Psychiatry. 2001;50(12):932–942
  47. Shin LM, Rauch SL, Pitman RK. Amygdala, medial prefrontal cortex, and hippocampal function in PTSD. Annals of the New York Academy of Science. 2006;1071:67–79
  48. Snyder JJ, Chatterjee A. The frontal cortex and exogenous attentional orienting. Journal of Cognitive Neuroscience. 2006;18(11):1913–1923
  49. Stein JL, Wiedholz LM, Bassett DS, Weinberger DR, Zink CF, Mattay VS, et al. A validated network of effective amygdala connectivity. Neuroimage. 2007;36(3):736–745
  50. Straube T, Mentzel HJ, Glauer M, Miltner WH. Brain activation to phobia-related words in phobic subjects. Neuroscience Letters. 2004;372(3):204–208
  51. Straube T, Glauer M, Dilger S, Mentzel HJ, Miltner WH. Effects of cognitive-behavioral therapy on brain activation in specific phobia. Neuroimage. 2006;29(1):125–135
  52. Straube T, Mentzel HJ, Miltner WH. Neural mechanisms of automatic and direct processing of phobogenic stimuli in specific phobia. Biological Psychiatry. 2006;59(2):162–170
  53. Talairach J, Tournoux P. Co-planar Stereotactic Atlas of the Human Brain. Stuttgart: Georg Thieme Verlag; 1988;
  54. Tillfors M, Furmark T, Marteinsdottir I, Fischer H, Pissiota A, Langstrom B, et al. Cerebral blood flow in subjects with social phobia during stressful speaking tasks: a PET study. American Journal of Psychiatry. 2001;158(8):1220–1226
  55. Veltman DJ, Tuinebreijer WE, Winkelman D, Lammertsma AA, Witter MP, Dolan RJ, et al. Neurophysiological correlates of habituation during exposure in spider phobia. Psychiatry Research: Neuroimaging. 2004;132(2):149–158
  56. Vuilleumier P, Driver J. Modulation of visual processing by attention and emotion: windows on causal interactions between human brain regions. Philosophical transactions of the Royal Society of London. 2007;362(1481):837–855
  57. Wik G, Fredrikson M, Ericson K, Eriksson L, Stone-Elander S, Greitz T. A functional cerebral response to frightening visual stimulation. Psychiatry Research: Neuroimaging. 1993;50(1):15–24

PII: S0925-4927(08)00186-8

doi: 10.1016/j.pscychresns.2008.11.004

Psychiatry Research: Neuroimaging
Volume 172, Issue 2 , Pages 103-108 , 15 May 2009

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