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Abstracts
  • Tabbert, K., Stark, R., Kirsch, P., & Vaitl, D. (2005). Hemodynamic responses of the amygdala, the orbitofrontal cortex and the visual cortex during a fear conditioning paradigm. International Journal of Psychophysiology : Official Journal of the International Organization of Psychophysiology, 57(1), 15–23. https://doi.org/10.1016/j.ijpsycho.2005.01.007

    Functional magnetic resonance imaging (fMRI) studies consistently demonstrate an enhanced activation of the visual cortex in reaction to emotionally salient visual stimuli. This increase of activation is probably modulated by top-down processes, that are initiated in emotion processing structures, specifically the amygdala and the orbitofrontal cortex. In the present fMRI study, a differential fear conditioning paradigm was applied to investigate this assumed modulation. Hemodynamic responses towards a neutral visual stimulus (CS+) predicting an electrical stimulation (UCS) were compared with responses towards a neutral and unpaired stimulus (CS-). Thereby, particularly the time courses of neural responses were considered. Skin conductance measures were concurrently recorded. Our results show that the differentiation between CS+ and CS- within the amygdala and the extended visual cortex was accomplished during a late acquisition phase. In the orbitofrontal cortex the differentiation occurred at an earlier stage and was then sustained throughout acquisition. It is suggested that these altering activation patterns are reflecting different phases of learning, integrating the analyzed regions to varying degrees. Additionally, the results indicate that statistical analyses comprising a temporal variation of hemodynamic responses are more likely to detect amygdala activation.

  • Merz, C. J., Stark, R., Vaitl, D., Tabbert, K., & Wolf, O. T. (2013). Stress hormones are associated with the neuronal correlates of instructed fear conditioning. Biological Psychology, 92(1), 82–89. https://doi.org/10.1016/j.biopsycho.2012.02.017

    The effects of sex and stress hormones on classical fear conditioning have been subject of recent experimental studies. A correlation approach between basal cortisol concentrations and neuronal activation in fear-related structures seems to be a promising alternative approach in order to foster our understanding of how cortisol influences emotional learning. In this functional magnetic resonance imaging study, participants with varying sex hormone status (20 men, 15 women taking oral contraceptives, 15 women tested in the luteal phase) underwent an instructed fear conditioning protocol with geometrical figures as conditioned stimuli and an electrical stimulation as unconditioned stimulus. Salivary cortisol concentrations were measured and afterwards correlated with fear conditioned brain responses. Results revealed a positive correlation between basal cortisol levels and differential activation in the amygdala in men and OC women only. These results suggest that elevated endogenous cortisol levels are associated with enhanced fear anticipation depending on current sex hormone availability.

  • Alpers, G. W., Gerdes, A. B. M., Lagarie, B., Tabbert, K., Vaitl, D., & Stark, R. (2009). Attention and amygdala activity: an fMRI study with spider pictures in spider phobia. Journal of Neural Transmission (Vienna, Austria : 1996), 116(6), 747–757. https://doi.org/10.1007/s00702-008-0106-8

    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.

  • Merz, C. J., Tabbert, K., Schweckendiek, J., Klucken, T., Vaitl, D., Stark, R., & Wolf, O. T. (2010). Investigating the impact of sex and cortisol on implicit fear conditioning with fMRI. Psychoneuroendocrinology, 35(1), 33–46. https://doi.org/10.1016/j.psyneuen.2009.07.009

    Fear conditioning is influenced by stress but opposing effects in males and females have often been reported. In a previous human functional magnetic resonance imaging (fMRI) study, we observed acute effects of the stress hormone cortisol on prefrontal structures. Men showed evidence for impaired fear conditioning after cortisol treatment, while the opposite pattern was found for women. In the current experiment, we tested whether similar sex-dependent effects would occur on the neural level if contingency awareness was prevented experimentally to investigate implicit learning processes. A differential fear conditioning experiment with transcutaneous electrical stimulation as unconditioned stimulus and geometric figures as conditioned stimuli (CS) was conducted. One figure was always paired (CS+), whereas the other (CS-) was never paired with the UCS. Thirty-nine (19 female) subjects participated in this fMRI study, receiving either placebo or 30 mg cortisol (hydrocortisone) before conditioning. Dependent variables were skin conductance responses (SCRs) and neural activity (BOLD signal). In line with prior findings in unaware participants, no differential learning could be observed for the SCRs. However, a sex x cortisol interaction was detected with a reduced mean response to the CS after cortisol treatment in men, while the opposite pattern was observed in women (enhanced mean SCR under cortisol). In the contrast CS+ minus CS-, neural activity showed a sex x cortisol interaction in the insula and further trends in the hippocampus and the thalamus. In these regions, cortisol reduced the CS+/CS- differentiation in men but enhanced it in women. In contrast to these sex specific effects, differential amygdala activation was found in the placebo group but not in the cortisol group, irrespective of sex. Further, differential neural activity in the amygdala and thalamus were positively correlated with the SCRs in the placebo group only. The present study in contingency unaware participants illustrates that cortisol has in some brain regions sex specific effects on neural correlates of emotional learning. These effects might translate into a different vulnerability of the two sexes for anxiety disorders.

  • Stark, R., Wolf, O. T., Tabbert, K., Kagerer, S., Zimmermann, M., Kirsch, P., Schienle, A., & Vaitl, D. (2006). Influence of the stress hormone cortisol on fear conditioning in humans: evidence for sex differences in the response of the prefrontal cortex. NeuroImage, 32(3), 1290–1298. https://doi.org/10.1016/j.neuroimage.2006.05.046

    The stress hormone cortisol is known to influence declarative memory and associative learning. In animals, stress has often been reported to have opposing effects on memory and learning in males and females. In humans, the effects of cortisol have mainly been studied at the behavioral level. The aim of the present experiment was to characterize the effects of a single cortisol dose (30 mg) on the hemodynamic correlates of fear conditioning. In a double-blind group comparison study subjects (17 females and 17 males) received 30 mg cortisol or placebo orally before participating in a discriminative fear conditioning paradigm. Results revealed that cortisol impaired electrodermal signs of learning (the first interval response) in males, while no conditioned SCRs emerged for the females independent of treatment. fMRI results showed that cortisol reduced activity for the CS+ > CS- comparison in the anterior cingulate, the lateral orbitofrontal cortex and the medial prefrontal cortex in males. Opposite findings (increase in these regions under cortisol) were detected in females. In addition, cortisol reduced the habituation in the CS+ > CS- contrast in the dorsolateral prefrontal cortex independent of sex. Finally, cortisol also modified the response to the electric shock (the UCS) by enhancing the activity of the anterior as well as the posterior cingulate. In sum, these findings demonstrate that in humans cortisol mostly influences prefrontal brain activation during fear conditioning and that these effects appear to be modulated by sex.

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