Advertisement

Journal of Neural Transmission

, Volume 116, Issue 6, pp 747–757 | Cite as

Attention and amygdala activity: an fMRI study with spider pictures in spider phobia

  • Georg W. AlpersEmail author
  • Antje B. M. Gerdes
  • Bernadette Lagarie
  • Katharina Tabbert
  • Dieter Vaitl
  • Rudolf Stark
Basic Neurosciences, Genetics and Immunology - Original Article

Abstract

Facilitated detection of threatening visual cues is thought to be adaptive. In theory, detection of threat cues should activate the amygdala independently from allocation of attention. However, previous studies using emotional facial expressions as well as phobic cues yielded contradictory results. We used fMRI to examine whether the allocation of attention to components of superimposed spider and bird displays modulates amygdala activation. Nineteen spider-phobic women were instructed to identify either a moving or a stationary animal in briefly presented double-exposure displays. Amygdala activation followed a dose–response relationship: Compared to congruent neutral displays (two birds), amygdala activation was most pronounced in response to congruent phobic displays (two spiders) and less but still significant in response to mixed displays (spider and bird) when attention was focused on the phobic component. When attention was focused on the neutral component, mixed displays did not result in significant amygdala activation. This was confirmed in a significant parametric graduation of the amygdala activation in the order of congruent phobic displays, mixed displays with attention focus on the spider, mixed displays with focus on the bird and congruent neutral displays. These results challenge the notion that amygdala activation in response to briefly presented phobic cues is independent from attention.

Keywords

Spider phobia fMRI Attention Visual processing Emotion Amygdala 

Notes

Acknowledgments

The pictures used to prepare the double-exposure pictures shown in this study were graciously provided by Wolfgang Miltner, Jena. This work was supported by the Research Group Emotion and Behavior which is sponsored by the German Research Society (DFG).

Conflict of interest statement

None declared.

References

  1. Adolphs R (2004) Emotional vision. [comment]. Nat Neurosci 7:1167–1168PubMedCrossRefGoogle Scholar
  2. Alpers GW (2008) Eye-catching: right hemisphere attentional bias for emotional pictures. Laterality: Asymmetries of Body. Brain Cogn 13:158–178Google Scholar
  3. Anders S, Birbaumer N, Sadowski B, Erb M, Mader I, Grodd W, Lotze M (2004) Parietal somatosensory association cortex mediates affective blindsight. Nat Neurosci 7:339–340PubMedCrossRefGoogle Scholar
  4. Anderson AK, Christoff K, Panitz D, De Rosa E, Gabrieli JD (2003) Neural correlates of the automatic processing of threat facial signals. J Neurosci 23:5627–5633PubMedGoogle Scholar
  5. Bar-Haim Y, Lamy D, Pergamin L, Bakermans-Kranenburg MJ, van Ijzendoorn MH (2007) Threat-related attentional bias in anxious and nonanxious individuals: a meta-analytic study. Psychol Bull 133:1–24PubMedCrossRefGoogle Scholar
  6. Becker ES, Rinck M (2004) Sensitivity and response bias in fear of spiders. Cogn Emot 18:961–976CrossRefGoogle Scholar
  7. Blair KS, Smith BW, Mitchell DG, Morton J, Vythilingam M, Pessoa L, Fridberg D, Zametkin A, Sturman D, Nelson EE, Drevets WC, Pine DS, Martin A, Blair RJ (2007) Modulation of emotion by cognition and cognition by emotion. Neuroimage 35:430–440PubMedCrossRefGoogle Scholar
  8. Carlsson K, Petersson KM, Lundqvist D, Karlsson A, Ingvar M, Öhman A (2004) Fear and the amygdala: manipulation of awareness generates differential cerebral responses to phobic and fear-relevant (but nonfeared) stimuli. Emotion 4:340–353PubMedCrossRefGoogle Scholar
  9. Davis M, Whalen PJ (2001) The amygdala: vigilance and emotion. Mol Psychiatry 6:13–34PubMedCrossRefGoogle Scholar
  10. Dilger S, Straube T, Mentzel HJ, Fitzek C, Reichenbach JR, Hecht H, Krieschel S, Gutberlet I, Miltner WH (2003) Brain activation to phobia-related pictures in spider phobic humans: an event-related functional magnetic resonance imaging study. Neurosci Lett 348:29–32PubMedCrossRefGoogle Scholar
  11. Dolan RJ, Vuilleumier P (2003) Amygdala automaticity in emotional processing. Ann N Y Acad Sci 985:348–355PubMedGoogle Scholar
  12. Fredrikson M (1993) Regional cerebral blood flow during experimental phobic fear. Psychophysiology 30:126–130PubMedGoogle Scholar
  13. Fredrikson M, Wik G, Annas P, Ericson K, Stone-Elander S (1995) Functional neuroanatomy of visually elicited simple phobic fear: additional data and theoretical analysis. Psychophysiology 32:43–48PubMedCrossRefGoogle Scholar
  14. Gerdes ABM, Alpers GW (2007) Toward and away from spiders: attentional engagement and disengagement in spider phobic patients. Psychophysiology 44:S35Google Scholar
  15. Gerdes ABM, Alpers GW, Pauli P (2008a) When spiders appear suddenly: spider phobic patients are distracted by task-irrelevant spiders. Behav Res Ther 46:174–187PubMedCrossRefGoogle Scholar
  16. Gerdes ABM, Uhl G, Alpers GW (2008b) Spiders are special: Harmfulness does not explain why they are feared. Evol Hum Behav (in press)Google Scholar
  17. Goetsch VL, Taylor CB, Segall GM, Trabert W (1993) Positron emission tomography evaluation of behavior therapy for simple phobia. W Va J Psychol Res Pract 42–47Google Scholar
  18. Habel U, Windischberger C, Derntl B, Robinson S, Kryspin-Exner I, Gur RC, Moser E (2007) Amygdala activation and facial expressions: explicit emotion discrimination versus implicit emotion processing. Neuropsychologia 45:2369–2377PubMedCrossRefGoogle Scholar
  19. Hamm AO, Weike AI, Schupp HT, Treig T, Dressel A, Kessler C (2003) Affective blindsight: intact fear conditioning to a visual cue in a cortically blind patient. Brain 126:267–275PubMedCrossRefGoogle Scholar
  20. Kolassa IT, Musial F, Mohr A, Trippe RH, Miltner WH (2005) Electrophysiological correlates of threat processing in spider phobics. Psychophysiology 42:520–530PubMedGoogle Scholar
  21. Lang PJ (1980) Behavioral treatment and bio-behavioral assessment: computer applications. In: Sidowski JB, Johnson JH, Williams TA (eds) Technology in mental health care delivery. Ablex, Norwood, pp 119–137Google Scholar
  22. Laux L, Glanzmann P, Schaffner P, Spielberger CD (1981) Das State-Trait-Angstinventar. Beltz Test Gesellschaft, WeinheimGoogle Scholar
  23. LeDoux JE (1998) Fear and the brain: where have we been, and where are we going? Biol Psychiatry 44:1229–1238PubMedCrossRefGoogle Scholar
  24. Lipp OV, Derakshan N, Waters AM, Logies S (2004) Snakes and cats in the flower bed: fast detection is not specific to pictures of fear-relevant animals. Emotion 4:233–250PubMedCrossRefGoogle Scholar
  25. Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH (2003) An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19:1233–1239PubMedCrossRefGoogle Scholar
  26. Maldjian JA, Laurienti PJ, Burdette JH (2004) Precentral gyrus discrepancy in electronic versions of the Talairach Atlas. Neuroimage 21:450–455PubMedCrossRefGoogle Scholar
  27. Maxwell JS, Davidson RJ (2004) Unequally masked: indexing differences in the perceptual salience of “unseen” facial expressions. Cogn Emot 18:1009–1026CrossRefGoogle Scholar
  28. Merboldt KD, Fransson P, Bruhn H, Frahm J (2001) Functional MRI of the human amygdala? Neuroimage 14:253–257PubMedCrossRefGoogle Scholar
  29. Miltner WHR, Krieschel S, Hecht H, Trippe R, Weiss T (2004) Eye movements and behavioral responses to threatening and nonthreatening stimuli during visual search in phobic and nonphobic subjects. Emotion 4:323–339PubMedCrossRefGoogle Scholar
  30. Moors A, De Houwer J (2006) Automaticity: a theoretical and conceptual analysis. Psychol Bull 132:297–326PubMedCrossRefGoogle Scholar
  31. Mountz JM, Modell JG, Wilson MW, Curtis GC (1989) Positron emission tomographic evaluation of cerebral blood flow during state anxiety in simple phobia. Arch Gen Psychiatry 46:501–504Google Scholar
  32. O’Craven KM, Downing PE, Kanwisher N (1999) fMRI evidence for objects as the units of attentional selection. Nature 401:584–587PubMedCrossRefGoogle Scholar
  33. Öhman A (1997) As fast as the blink of an eye: evolutionary preparedness for preattentive processing of threat. In: Lang PJ, Simons RF, Balaban MT (eds) Attention and orienting: sensory and motivational processes. Lawrence Erlbaum Associates, Mahwah, pp 165–184Google Scholar
  34. Öhman A, Mineka S (2001) Fears, phobias, and preparedness: toward an evolved module of fear and fear learning. Psychol Rev 108:483–522PubMedCrossRefGoogle Scholar
  35. Öhman A, Soares JJ (1994) “Unconscious anxiety”: phobic responses to masked stimuli. J Abnorm Psychol 103:231–240PubMedCrossRefGoogle Scholar
  36. Paquette V, Levesque J, Mensour B, Leroux JM, Beaudoin G, Bourgouin P, Beauregard M (2003) “Change the mind and you change the brain”: effects of cognitive-behavioral therapy on the neural correlates of spider phobia. Neuroimage 18:401–409PubMedCrossRefGoogle Scholar
  37. Pessoa L, McKenna M, Gutierrez E, Ungerleider LG (2002) Neural processing of emotional faces requires attention. Proc Natl Acad Sci USA 99:11458–11463PubMedCrossRefGoogle Scholar
  38. Pessoa L, Padmala S, Morland T (2005) Fate of unattended fearful faces in the amygdala is determined by both attentional resources and cognitive modulation. Neuroimage 28:249–255PubMedCrossRefGoogle Scholar
  39. Pessoa L, Japee S, Sturman D, Ungerleider LG (2006) Target visibility and visual awareness modulate amygdala responses to fearful faces. Cereb Cortex 16:366–375PubMedCrossRefGoogle Scholar
  40. Phan KL, Wager TD, Taylor SF, Liberzon I (2004) Functional neuroimaging studies of human emotions. CNS Spectr 9:258–266PubMedGoogle Scholar
  41. Pissiota A, Frans O, Michelgard A, Appel L, Langstrom B, Flaten MA, Fredrikson M (2003) Amygdala and anterior cingulate cortex activation during affective startle modulation: a PET study of fear. Eur J Neurosci 18:1325–1331PubMedCrossRefGoogle Scholar
  42. Prokasy WF, Ebel HC (1967) Three components of the classically conditioned GSR in human subjects. J Exp Psychol 73:247–256CrossRefGoogle Scholar
  43. Rauch SL, Savage CR, Alpert NM, Miguel EC, Baer L, Breiter HC, Fischman AJ, Manzo PA, Moretti C, Jenike MA (1995) A positron emission tomographic study of simple phobic symptom provocation. Arch Gen Psychiatry 52:20–28PubMedGoogle Scholar
  44. Rauch SL, Shin LM, Wright CI (2003) Neuroimaging studies of amygdala function in anxiety disorders. Ann N Y Acad Sci 985:389–410PubMedCrossRefGoogle Scholar
  45. Rinck M, Becker ES (2006) Spider fearful individuals attend to threat, then quickly avoid it: evidence from eye movements. J Abnorm Psychol 115:231–238PubMedCrossRefGoogle Scholar
  46. Rinck M, Bundschuh S, Engler S, Müller A, Wissmann J, Ellwart T, Becker ES (2002) Reliabilität und Validität dreier Instrumente zur Messung von Angst vor Spinnen. Diagnostica 48:141–149CrossRefGoogle Scholar
  47. Schaller E, Gerdes A, Alpers GW (2006) Angst ungleich Ekel: Der Fragebogen zu Ekel und Angst vor Spinnen. In: Alpers GW, Krebs H, Mühlberger A, Weyers P, Pauli P (eds) Wissenschaftliche Beiträge zum 24. Symposium der Fachgruppe Klinische Psychologie und Psychotherapie. Pabst, Lengerich, p 105Google Scholar
  48. Schienle A, Schäfer A (2006) Neuronale Korrelate der Expositionstherapie bei Patienten mit spezifischen Phobien. Verhaltenstherapie 16:104–110CrossRefGoogle Scholar
  49. Straube T, Glauer M, Dilger S, Mentzel HJ, Miltner WH (2006a) Effects of cognitive-behavioral therapy on brain activation in specific phobia. Neuroimage 29:125–135PubMedCrossRefGoogle Scholar
  50. Straube T, Mentzel HJ, Miltner WH (2006b) Neural mechanisms of automatic and direct processing of phobogenic stimuli in specific phobia. Biol Psychiatry 59:162–170PubMedCrossRefGoogle Scholar
  51. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15:273–289PubMedCrossRefGoogle Scholar
  52. Veltman DJ, Tuinebreijer WE, Winkelman D, Lammertsma AA, Witter MP, Dolan RJ, Emmelkamp PMG (2004) Neurophysiological correlates of habituation during exposure in spider phobia. Psychiatry Res 132:149–158PubMedCrossRefGoogle Scholar
  53. Wik G, Fredrikson M, Fischer H (1997) Evidence of altered cerebral blood-flow relationships in acute phobia. Int J Neurosci 91:253–263PubMedCrossRefGoogle Scholar
  54. Wittchen H-U, Zaudig M, Fydrich T (1997) SKID—Strukturiertes klinisches Interview für DSM IV Achse I und II. Hogrefe, GöttingenGoogle Scholar
  55. Yantis S (2005) How visual salience wins the battle for awareness. Nat Neurosci 8:975–977PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Georg W. Alpers
    • 1
    Email author
  • Antje B. M. Gerdes
    • 1
  • Bernadette Lagarie
    • 2
  • Katharina Tabbert
    • 2
  • Dieter Vaitl
    • 2
  • Rudolf Stark
    • 2
  1. 1.Biological Psychology, Clinical Psychology, and PsychotherapyUniversity of WürzburgWürzburgGermany
  2. 2.Bender Institute of NeuroimagingUniversity of GiessenGiessenGermany

Personalised recommendations