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Modulating adaptation to emotional faces by spatial frequency filtering

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Abstract

In four experiments, we investigated the presence and strength of perceptual aftereffects to emotional faces, using spatial frequency filtering to manipulate awareness of emotional content. We presented angry and happy faces as adapters and used a control condition without adaptation. Participants were subsequently requested to judge the friendliness level of a neutral target face. We confirmed the well-known aftereffect for unfiltered emotional faces in Experiment 1. In the experiment, friendliness judgments were greater for the angry than the happy or the control condition. In Experiment 2, in which the “hidden” emotional expression contained in the low spatial frequencies (LSF) was superimposed to the neutral expression presented in the rest of SF of the same image (emotional hybrid faces), the difference in friendliness judgments between angry and happy was significant, but none of the two conditions significantly differed from the control. In Experiment 3, faces were presented at LSF, confirmed a difference between the two emotions, but only the judgments of angry faces differed from the control condition. In Experiment 4, we extended the initial finding to stimuli presented at middle and high spatial frequencies (M-HSF). Finally, a comparison among all experiments revealed that the aftereffect was stronger with angry faces filtered at M-HSF than all of the other filtering conditions, whereas there were no differences for happy faces. We conclude that spatial frequency filtering influences aftereffects and that these effects are also related to emotional awareness. The results are discussed with reference to the dual route model of visual perception.

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References

  • Adams, W. J., Gray, K. L., Garner, M., & Graf, E. W. (2010). High-level face adaptation without awareness. Psychological Science, 21(2), 205–210.

    Article  PubMed  Google Scholar 

  • Blakemore, C., & Campbell, F. W. (1969). On the existence of neurones in the human visual system selectively sensitive to the orientation and size of retinal images. Journal of Physiology, 203, 237–260.

    Article  PubMed  PubMed Central  Google Scholar 

  • Butler, A., Oruc, I., Fox, C. J., & Barton, J. J. (2008). Factors contributing to the adaptation aftereffects of facial expression. Brain Research, 1191, 116–126.

    Article  PubMed  Google Scholar 

  • Chen, J., Yang, H., Wang, A., & Fang, F. (2010). Perceptual consequences of face viewpoint adaptation: Face viewpoint aftereffect, changes of differential sensitivity to face view, and their relationship. Journal of Vision, 10(3), 1–11.

    Article  Google Scholar 

  • Costen, N. P., Parker, D. M., & Craw, I. (1996). Effect of highpass and lowpass spatial filtering on face identification. Perception and Psychophysics, 58, 602–612.

    Article  PubMed  Google Scholar 

  • D’Ascenzo, S., Tommasi, L., & Laeng, B. (2014). Imagining sex and adapting to it: Different aftereffects after perceiving versus imagining faces. Vision Research, 96, 45–52.

    Article  PubMed  Google Scholar 

  • Dannlowski, U., Ohrmann, P., Bauer, J., Kugel, H., Arolt, V., Heindel, W., & Suslow, T. (2007). Amygdala reactivity predicts automatic negative evaluations for facial emotions. Psychiatry Research: Neuroimaging, 154(1), 13–20. doi:10.1016/j.pscychresns.2006.05.005.

    Article  PubMed  Google Scholar 

  • Eastwood, J. D., Smilek, D., & Merikle, P. M. (2001). Differential attentional guidance by unattended faces expressing positive and negative emotion. Perception and Psychophysics, 63(6), 1004–1013.

    Article  PubMed  Google Scholar 

  • Fox, C. J., & Barton, J. J. S. (2007). What is adapted in face adaptation? The neural representations of expression in the human visual system. Brain Research, 1127, 80–89.

    Article  PubMed  Google Scholar 

  • Gao, X., & Maurer, D. (2011). A comparison of spatial frequency tuning for the recognition of facial identity and facial expressions in adults and children. Vision Research, 51, 508–519. doi:10.1016/j.visres.2011.01.011.

    Article  PubMed  Google Scholar 

  • Gold, J., Bennett, P. J., & Sekuler, A. B. (1999). Identification of band-pass filtered letters and faces by human and ideal observers. Vision Research, 39, 3537–3560.

    Article  PubMed  Google Scholar 

  • Goolsby, B. A., Grabowecky, M., & Suzuki, S. (2005). Adaptive modulation of color salience contingent upon global form coding and task relevance. Vision Research, 45(7), 901–930.

    Article  PubMed  Google Scholar 

  • Graham, N. V. S. (1989). Visual pattern analyzers. New York: Oxford University Press.

    Book  Google Scholar 

  • Jiang, Y., & He, S. (2006). Cortical responses to invisible faces: Dissociating subsystems for facial-information processing. Current Biology, 16(20), 2023–2029.

    Article  PubMed  Google Scholar 

  • Johnson, M. H. (2005). Subcortical face processing. Nature Reviews Neuroscience, 6, 766–774. doi:10.1038/nrn1766.

    Article  PubMed  Google Scholar 

  • Khalid, S., Ansorge, U., & Finkbeiner, M. (2015). Supraliminal but no subliminal priming by high-spatial frequency faces in a face-sex discrimination task. Psychology, 6(12), 1486.

    Article  Google Scholar 

  • Kumar, D., & Srinivasan, N. (2011). Emotion perception is mediated by spatial frequency content. Emotion, 11(5), 1144. doi:10.1037/a0025453.

    Article  PubMed  Google Scholar 

  • Laeng, B., Profeti, I., Saether, L., Adolfsdottir, S., Lundervold, A. J., Vangberg, T., … Waterloo, K. (2010). Invisible expressions evoke core impressions. Emotion, 10(4), 573–586. doi:10.1037/a0018689.

    Article  PubMed  Google Scholar 

  • Laeng, B., Saether, L., Holmlund, T., Wang, C. E. A., Waterloo, K., Eisemann, M., & Halvorsen, M. (2013). Invisible emotional expressions influence social judgments and papillary responses of both depressed and non-depressed individuals. Frontiers in Psychology, 4, 1–7. doi:10.3389/fpsyg.2013.00291.

    Article  Google Scholar 

  • LeDoux, J. (1996). The emotional brain: The mysterious underpinnings of emotional life. New York: Touchstone Press.

    Google Scholar 

  • Leknes, S., Wessberg, J., Ellingsen, D. M., Chelnokova, O., Olausson, H., & Laeng, B. (2013). Oxytocin enhances pupil dilation and sensitivity to ‘hidden’ emotional expressions. Social Cognitive and Affective Neuroscience, 8(7), 741–749. doi:10.1093/scan/nss062.

    Article  PubMed  Google Scholar 

  • Leopold, D. A., O’Toole, A. J., Vetter, T., & Blanz, V. (2001). Prototype-referenced shape encoding revealed by high-level aftereffects. Nature Neuroscience, 4(1), 89–94.

    Article  PubMed  Google Scholar 

  • Liddell, B. J., Brown, K. J., Kemp, A. H., Barton, M. J., Das, P., Peduto, A., & Williams, L. M. (2005). A direct brainstem–amygdala–cortical ‘alarm’ system for subliminal signals of fear. Neuroimage, 24(1), 235–243.

    Article  PubMed  Google Scholar 

  • Livingstone, M., & Hubel, D. (1988). Segregation of form, color, movement, and depth: Anatomy, physiology, and perception. Science, 240, 740–749.

    Article  PubMed  Google Scholar 

  • Lundqvist, D., Flykt, A., & Öhman, A. (1998). The Karolinska directed emotional faces (KDEF). Stockholm: Department of Neurosciences Karolinska Hospital.

    Google Scholar 

  • Mather, G., Pavan, A., Campana, G., & Casco, C. (2008). The motion after effect reloadad. Trends in Cognitive Science, 12, 481–487. doi:10.1016/j.tics.2008.09.002.

    Article  Google Scholar 

  • Moradi, F., Koch, C., & Shimojo, S. (2005). Face adaptation depends on seeing the face. Neuron, 45(1), 169–175. doi:10.1016/j.neuron.2004.12.018.

    Article  PubMed  Google Scholar 

  • Morris, J. S., Öhman, A., & Dolan, R. J. (1999). A subcortical pathway to the right amygdala mediating “unseen” fear. Proceedings of the National Academy of Sciences, 96(4), 1680–1685. doi:10.1073/pnas.96.4.1680.

    Article  Google Scholar 

  • Moutoussis, K. (2015). The physiology and psychophysics of the color-form relationship: A review. Frontiers in Psychology, 6, 1407.

    PubMed  PubMed Central  Google Scholar 

  • Murphy, S. T., & Zajonc, R. B. (1993). Affect, cognition, and awareness: affective priming with optimal and suboptimal stimulus exposures. Journal of Personality and Social Psychology, 64(5), 723.

  • Nasanen, R. (1999). The spatial frequency bandwidth used in the recognition of facial images. Vision Research, 39, 3824–3833.

    Article  PubMed  Google Scholar 

  • Oldfield, R. C. (1971). The assessment and analysis of handedness: The Edinburgh Inventory. Neuropsychologia, 9, 97–114.

    Article  PubMed  Google Scholar 

  • Palumbo, R., Laeng, B., & Tommasi, L. (2013). Gender-specific aftereffects following adaptation to silhouettes of human bodies. Visual Cognition, 21(1), 1–12.

    Article  Google Scholar 

  • Pasley, B. N., Mayes, L. C., & Schultz, R. T. (2004). Subcortical discrimination of unperceived objects during binocular rivalry. Neuron, 42(1), 163–172.

    Article  PubMed  Google Scholar 

  • Pessoa, L., & Adolphs, R. (2010). Emotion processing and the amygdala: From a ‘low road’ to ‘many roads’ of evaluating biological significance. Nature Review Neuroscience, 11(11), 773–783. doi:10.1038/nrn2920.

    Article  Google Scholar 

  • Pessoa, L., McKenna, M., Gutierrez, E., & Ungerleider, L. G. (2002). Neural processing of emotional faces requires attention. Proceedings of the National Academy of Sciences, 99(17), 11458–11463.

    Article  Google Scholar 

  • Prete, G., Capotosto, P., Zappasodi, F., Laeng, B., & Tommasi, L. (2015a). The cerebral correlates of subliminal emotions: An eleoencephalographic study with emotional hybrid faces. European Journal of Neuroscience, 42(11), 2952–2962. doi:10.1111/ejn.13078.

    Article  PubMed  Google Scholar 

  • Prete, G., D’Ascenzo, S., Laeng, B., Fabri, M., Foschi, N., & Tommasi, L. (2015b). Conscious and unconscious processing of facial expressions: Evidence from two split-brain patients. Journal of Neuropsychology, 9, 45–63. doi:10.1111/jnp.12034.

    Article  PubMed  Google Scholar 

  • Prete, G., Laeng, B., Fabri, M., Foschi, N., & Tommasi, L. (2015c). Right hemisphere or valence hypothesis, or both? The processing of hybrid faces in the intact and callosotomized brain. Neuropsychologia, 68, 94–106. doi:10.1016/j.neuropsychologia.2015.01.002.

    Article  PubMed  Google Scholar 

  • Prete, G., Laeng, B., & Tommasi, T. (2014). Lateralized hybrid faces: Evidence of a valence-specific bias in the processing of implicit emotions. Laterality, 19(4), 439–454. doi:10.1080/1357650X.2013.862255.

    Article  PubMed  Google Scholar 

  • Rhodes, G., Jeffery, L., Watson, T. L., Jaquet, E., Winkler, C., & Clifford, C. W. G. (2004). Orientation-contingent face aftereffects and implications for face-coding mechanisms. Current Biology, 14, 2119–2123.

    Article  PubMed  Google Scholar 

  • Rotshtein, P., Vuilleumier, P., Winston, J., Driver, J., & Dolan, R. (2007). Distinct and convergent visual processing of high and low spatial frequency information in faces. Cerebral Cortex, 17(11), 2713–2724.

    Article  PubMed  PubMed Central  Google Scholar 

  • Schiller, P. H., & Malpeli, J. G. (1977). Properties and tectal projections of monkey retinal ganglion cells. Journal of Neurophysiology, 40, 428–445.

    Article  PubMed  Google Scholar 

  • Schyns, P. G., & Oliva, A. (1994). From blobs to boundary edges: Evidence for time-and spatial-scale-dependent scene recognition. Psychological Science, 5(4), 195–200.

    Article  Google Scholar 

  • Skinner, A. L., & Benton, C. P. (2010). Anti-expression aftereffects reveal prototype-referenced coding of facial expressions. Psychological Science, 21(9), 1248–1253. doi:10.1177/0956797610380702.

    Article  PubMed  Google Scholar 

  • Sperandio, I., Lak, A., & Goodale, M. A. (2012). Afterimage size is modulated by size-contrast illusions. Journal of Vision, 12(2), 18.

    Article  PubMed  Google Scholar 

  • Suslow, T., Kugel, H., Ohrmann, P., Stuhrmann, A., Grotegerd, D., Redlich, R., & Dannlowski, U. (2013). Neural correlates of affective priming effects based on masked facial emotion: An fMRI study. Psychiatry Research: Neuroimaging, 211(3), 239–245. doi:10.1016/j.pscychresns.2012.09.008.

    Article  PubMed  Google Scholar 

  • Tamietto, M., & De Gelder, B. (2010). Neural bases of the non-conscious perception of emotional signals. Nature Review Neuroscience, 11(10), 697–709. doi:10.1038/nrn2889.

    Article  Google Scholar 

  • Taylor, S. E. (1991). Asymmetrical effects of positive and negative events: The mobilization-minimization hypothesis. Psychological Bulletin, 110(1), 67.

    Article  PubMed  Google Scholar 

  • Varga, E. T., Elif, K., Antal, A., Zimmer, M., Harza, I., Paulus, W., & Gyula, K. (2007). Cathodal transcranial direct current stimulation over the parietal cortex modifies facial gender adaptation. Ideggyogy Sz, 60(11–12), 474–479.

    PubMed  Google Scholar 

  • Vuilleumier, P., Armony, J. L., Driver, J., & Dolan, R. J. (2003). Distinct spatial frequency sensitivities for processing faces and emotional expressions. Nature Neuroscience, 6, 624–631. doi:10.1038/nn1057.

    Article  PubMed  Google Scholar 

  • Wang, S., Eccleston, C., & Keogh, E. (2015). The role of spatial frequency information in the recognition of facial expressions of pain. Pain, 156(9), 1670–1682. doi:10.1097/j.pain.0000000000000226.

    Article  PubMed  Google Scholar 

  • Williams, M. A., Morris, A. P., McGlone, F., Abbott, D. F., & Mattingley, J. B. (2004). Amygdala responses to fearful and happy facial expressions under conditions of binocular suppression. The Journal of Neuroscience, 24(12), 2898–2904.

    Article  PubMed  Google Scholar 

  • Wincenciak, J., Dzhelyova, M., Perrett, D. I., & Barraclough, N. E. (2013). Adaptation to facial trustworthiness is different in female and male observers. Vision Research, 87, 30–34.

    Article  PubMed  PubMed Central  Google Scholar 

  • Yamashita, J. A., Hardy, J. L., De Valois, K. K., & Webster, M. A. (2005). Stimulus selectivity of figural aftereffects for faces. Journal of Experimental Psychology: Human Perception and Performance, 31(3), 420.

    PubMed  Google Scholar 

  • Yang, E., Hong, S. W., & Blake, R. (2010). Adaptation aftereffects to facial expressions suppressed from visual awareness. Journal of Vision, 10(12), 24.

    Article  PubMed  PubMed Central  Google Scholar 

  • Yip, A. W., & Sinha, P. (2002). Contribution of color to face recognition. Perception, 31, 995–1003.

    Article  PubMed  Google Scholar 

  • Zaidi, Q., Ennis, R., Cao, D., & Lee, B. (2012). Neural locus of color afterimages. Current Biology, 22, 220–224. doi:10.1016/j.cub.2011.12.021.

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank Imma Servillo and Gianluca Durante, who helped us in recruiting and testing participants.

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Correspondence to Giulia Prete.

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Giulia Prete, Bruno Laeng, and Luca Tommasi declare that they have no conflict of interest.

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All procedures performed in the four studies described were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments.

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Since the present study did not involve patients, children or animals, as well as drugs, genetic samples or invasive techniques, verbal informed consent was obtained from all individual participants included in the study.

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Prete, G., Laeng, B. & Tommasi, L. Modulating adaptation to emotional faces by spatial frequency filtering. Psychological Research 82, 310–323 (2018). https://doi.org/10.1007/s00426-016-0830-x

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