Skip to main content
Log in

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

  • Basic Neurosciences, Genetics and Immunology - Original Article
  • Published:
Journal of Neural Transmission Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Notes

  1. Anxiety: congruent phobic M = 3.44, SD = 2.21; mixed M = 3.37, SD = 1.95; congruent neutral M = 1.21, SD = 0.71. Disgust: congruent phobic M = 5.21, SD = 2.59; mixed M = 4.47, SD = 2.17; congruent neutral M = 1.32, SD = 0.75. Valence: congruent phobic M = 6.58, SD = 1.77; mixed M = 5.74, SD = 1.56; congruent neutral M = 2.53, SD = 1.35. Arousal: congruent phobic M = 5.21, SD = 1.65; mixed M = 5.32, SD = 1.67; congruent neutral M = 2.00, SD = 1.33.

References

  • Adolphs R (2004) Emotional vision. [comment]. Nat Neurosci 7:1167–1168

    Article  PubMed  CAS  Google Scholar 

  • Alpers GW (2008) Eye-catching: right hemisphere attentional bias for emotional pictures. Laterality: Asymmetries of Body. Brain Cogn 13:158–178

    Google Scholar 

  • Anders S, Birbaumer N, Sadowski B, Erb M, Mader I, Grodd W, Lotze M (2004) Parietal somatosensory association cortex mediates affective blindsight. Nat Neurosci 7:339–340

    Article  PubMed  CAS  Google Scholar 

  • Anderson AK, Christoff K, Panitz D, De Rosa E, Gabrieli JD (2003) Neural correlates of the automatic processing of threat facial signals. J Neurosci 23:5627–5633

    PubMed  CAS  Google Scholar 

  • 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 133:1–24

    Article  PubMed  Google Scholar 

  • Becker ES, Rinck M (2004) Sensitivity and response bias in fear of spiders. Cogn Emot 18:961–976

    Article  Google Scholar 

  • 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 35:430–440

    Article  PubMed  CAS  Google Scholar 

  • 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 4:340–353

    Article  PubMed  Google Scholar 

  • Davis M, Whalen PJ (2001) The amygdala: vigilance and emotion. Mol Psychiatry 6:13–34

    Article  PubMed  CAS  Google Scholar 

  • 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 348:29–32

    Article  PubMed  CAS  Google Scholar 

  • Dolan RJ, Vuilleumier P (2003) Amygdala automaticity in emotional processing. Ann N Y Acad Sci 985:348–355

    PubMed  CAS  Google Scholar 

  • Fredrikson M (1993) Regional cerebral blood flow during experimental phobic fear. Psychophysiology 30:126–130

    PubMed  CAS  Google Scholar 

  • 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 32:43–48

    Article  PubMed  CAS  Google Scholar 

  • Gerdes ABM, Alpers GW (2007) Toward and away from spiders: attentional engagement and disengagement in spider phobic patients. Psychophysiology 44:S35

    Google Scholar 

  • Gerdes ABM, Alpers GW, Pauli P (2008a) When spiders appear suddenly: spider phobic patients are distracted by task-irrelevant spiders. Behav Res Ther 46:174–187

    Article  PubMed  Google Scholar 

  • Gerdes ABM, Uhl G, Alpers GW (2008b) Spiders are special: Harmfulness does not explain why they are feared. Evol Hum Behav (in press)

  • 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 42–47

  • 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 45:2369–2377

    Article  PubMed  Google Scholar 

  • 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 126:267–275

    Article  PubMed  Google Scholar 

  • Kolassa IT, Musial F, Mohr A, Trippe RH, Miltner WH (2005) Electrophysiological correlates of threat processing in spider phobics. Psychophysiology 42:520–530

    PubMed  Google Scholar 

  • 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 119–137

    Google Scholar 

  • Laux L, Glanzmann P, Schaffner P, Spielberger CD (1981) Das State-Trait-Angstinventar. Beltz Test Gesellschaft, Weinheim

    Google Scholar 

  • LeDoux JE (1998) Fear and the brain: where have we been, and where are we going? Biol Psychiatry 44:1229–1238

    Article  PubMed  CAS  Google Scholar 

  • 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 4:233–250

    Article  PubMed  Google Scholar 

  • Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH (2003) An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19:1233–1239

    Article  PubMed  Google Scholar 

  • Maldjian JA, Laurienti PJ, Burdette JH (2004) Precentral gyrus discrepancy in electronic versions of the Talairach Atlas. Neuroimage 21:450–455

    Article  PubMed  Google Scholar 

  • Maxwell JS, Davidson RJ (2004) Unequally masked: indexing differences in the perceptual salience of “unseen” facial expressions. Cogn Emot 18:1009–1026

    Article  Google Scholar 

  • Merboldt KD, Fransson P, Bruhn H, Frahm J (2001) Functional MRI of the human amygdala? Neuroimage 14:253–257

    Article  PubMed  CAS  Google Scholar 

  • 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 4:323–339

    Article  PubMed  Google Scholar 

  • Moors A, De Houwer J (2006) Automaticity: a theoretical and conceptual analysis. Psychol Bull 132:297–326

    Article  PubMed  Google Scholar 

  • 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 46:501–504

    Google Scholar 

  • O’Craven KM, Downing PE, Kanwisher N (1999) fMRI evidence for objects as the units of attentional selection. Nature 401:584–587

    Article  PubMed  Google Scholar 

  • 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 165–184

    Google Scholar 

  • Öhman A, Mineka S (2001) Fears, phobias, and preparedness: toward an evolved module of fear and fear learning. Psychol Rev 108:483–522

    Article  PubMed  Google Scholar 

  • Öhman A, Soares JJ (1994) “Unconscious anxiety”: phobic responses to masked stimuli. J Abnorm Psychol 103:231–240

    Article  PubMed  Google Scholar 

  • 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 18:401–409

    Article  PubMed  Google Scholar 

  • Pessoa L, McKenna M, Gutierrez E, Ungerleider LG (2002) Neural processing of emotional faces requires attention. Proc Natl Acad Sci USA 99:11458–11463

    Article  PubMed  CAS  Google Scholar 

  • 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 28:249–255

    Article  PubMed  Google Scholar 

  • Pessoa L, Japee S, Sturman D, Ungerleider LG (2006) Target visibility and visual awareness modulate amygdala responses to fearful faces. Cereb Cortex 16:366–375

    Article  PubMed  Google Scholar 

  • Phan KL, Wager TD, Taylor SF, Liberzon I (2004) Functional neuroimaging studies of human emotions. CNS Spectr 9:258–266

    PubMed  Google Scholar 

  • 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 18:1325–1331

    Article  PubMed  Google Scholar 

  • Prokasy WF, Ebel HC (1967) Three components of the classically conditioned GSR in human subjects. J Exp Psychol 73:247–256

    Article  Google Scholar 

  • 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 52:20–28

    PubMed  CAS  Google Scholar 

  • Rauch SL, Shin LM, Wright CI (2003) Neuroimaging studies of amygdala function in anxiety disorders. Ann N Y Acad Sci 985:389–410

    Article  PubMed  Google Scholar 

  • Rinck M, Becker ES (2006) Spider fearful individuals attend to threat, then quickly avoid it: evidence from eye movements. J Abnorm Psychol 115:231–238

    Article  PubMed  Google Scholar 

  • 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 48:141–149

    Article  Google Scholar 

  • 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 105

  • Schienle A, Schäfer A (2006) Neuronale Korrelate der Expositionstherapie bei Patienten mit spezifischen Phobien. Verhaltenstherapie 16:104–110

    Article  Google Scholar 

  • Straube T, Glauer M, Dilger S, Mentzel HJ, Miltner WH (2006a) Effects of cognitive-behavioral therapy on brain activation in specific phobia. Neuroimage 29:125–135

    Article  PubMed  Google Scholar 

  • Straube T, Mentzel HJ, Miltner WH (2006b) Neural mechanisms of automatic and direct processing of phobogenic stimuli in specific phobia. Biol Psychiatry 59:162–170

    Article  PubMed  Google Scholar 

  • 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 15:273–289

    Article  PubMed  CAS  Google Scholar 

  • 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 132:149–158

    Article  PubMed  Google Scholar 

  • Wik G, Fredrikson M, Fischer H (1997) Evidence of altered cerebral blood-flow relationships in acute phobia. Int J Neurosci 91:253–263

    Article  PubMed  CAS  Google Scholar 

  • Wittchen H-U, Zaudig M, Fydrich T (1997) SKID—Strukturiertes klinisches Interview für DSM IV Achse I und II. Hogrefe, Göttingen

    Google Scholar 

  • Yantis S (2005) How visual salience wins the battle for awareness. Nat Neurosci 8:975–977

    Article  PubMed  CAS  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Georg W. Alpers.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Alpers, G.W., Gerdes, A.B.M., Lagarie, B. et al. Attention and amygdala activity: an fMRI study with spider pictures in spider phobia. J Neural Transm 116, 747–757 (2009). https://doi.org/10.1007/s00702-008-0106-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00702-008-0106-8

Keywords

Navigation