Abstract
Involuntary microsaccades and voluntary saccades reflect human brain activities during attention and cognitive tasks. Our eye movements can also betray our emotional state. However, the effects of attention to emotion on microsaccadic activity remain unknown. The present study was conducted in healthy volunteers to investigate the effects of devoting attention to exogenous emotional stimuli on microsaccadic response, with change in pupil size as an index of sympathetic nervous system activity. Event-related responses to unpleasant images significantly inhibited the rate of microsaccade appearance and altered pupil size (Experiment 1). Additionally, microsaccadic responses to covert orienting of attention to emotional stimuli appeared significantly in the anti-direction to a target, with a fast reaction time (Experiment 2). Therefore, we concluded that attentional shifts induced by exogenous emotional stimuli can modulate microsaccadic activities. Future studies of the interaction between miniature eye movements and emotion may be beneficial in the assessment of pathophysiological responses in mental disorders.
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Amrhein, C., Muhlberger, A., Pauli, P., & Wiedemann, G. (2004). Modulation of event-related brain potentials during affective picture processing: A complement to startle reflex and skin conductance response? International Journal of Psychophysiology, 54(3), 231–240.
Awh, E., & Jonides, J. (2001). Overlapping mechanisms of attention and spatial working memory. Trends in Cognitive Sciences, 5(3), 119–126.
Bannerman, R. L., Milders, M., & Sahraie, A. (2009). Processing emotional stimuli: Comparison of saccadic and manual choice-reaction times. Cognition and Emotion, 23(5), 930–954.
Bernat, E., Patrick, C. J., Benning, S. D., & Tellegen, A. (2006). Effects of picture content and intensity on affective physiological response. Psychophysiology, 43(1), 93–103.
Betta, E., Galfano, G., & Turatto, M. (2007). Microsaccadic response during inhibition of return in a target–target paradigm. Vision Research, 47(3), 428–436.
Betta, E., & Turatto, M. (2006). Are you ready? I can tell by looking at your microsaccades. NeuroReport, 17(10), 1001–1004.
Blair, K. S., Smith, B. W., Mitchell, D. G., Morton, J., Vythilingam, M., Pessoa, L., et al. (2007). Modulation of emotion by cognition and cognition by emotion. Neuroimage, 35(1), 430–440.
Bradley, M. M., Miccoli, L., Escrig, M. A., & Lang, P. J. (2008). The pupil as a measure of emotional arousal and autonomic activation. Psychophysiology, 45(4), 602–607.
Bradley, M. M., Moulder, B., & Lang, P. J. (2005). When good things go bad: the reflex physiology of defense. Psychological Science, 16(6), 468–473.
Brosch, T., Sander, D., Pourtois, G., & Scherer, K. R. (2008). Beyond fear: Rapid spatial orienting toward positive emotional stimuli. Psychological Science, 19(4), 362–370.
Calvo, M. G., & Lang, P. J. (2005). Parafoveal semantic processing of emotional visual scenes. Journal of Experimental Psychology: Human Perception and Performance, 31(3), 502–519.
Corbetta, M., Miezin, F. M., Shulman, G. L., & Petersen, S. E. (1993). A PET study of visuospatial attention. The Journal of Neuroscience, 13(3), 1202–1226.
Coull, J. T., Frith, C. D., Büchel, C., & Nobre, A. C. (2000). Orienting attention in time: Behavioural and neuroanatomical distinction between exogenous and endogenous shifts. Neuropsychologia, 38, 808–819.
Cui, J., Wilke, M., Logothetis, N. K., Leopold, D. A., & Liang, H. (2009). Visibility states modulate microsaccade rate and direction. Vision Research, 49(2), 228–236.
Engbert, R. (2006). Microsaccades: A microcosm for research on oculomotor control, attention, and visual perception. Progress in Brain Research, 154, 177–192.
Engbert, R., & Kliegl, R. (2003). Microsaccades uncover the orientation of covert attention. Vision Research, 43(9), 1035–1045.
Fox, E., Russo, R., Bowles, R., & Dutton, K. (2001). Do threatening stimuli draw or hold visual attention in subclinical anxiety? Journal of Experimental Psychology: General, 130(4), 681–700.
Galfano, G., Betta, E., & Turatto, M. (2004). Inhibition of return in microsaccades. Experimental Brain Research, 159(3), 400–404.
Gaymard, B., Ploner, C. J., Rivaud, S., Vermersch, A. I., & Pierrot-Deseilligny, C. (1998). Cortical control of saccades. Experimental Brain Research, 123(1–2), 159–163.
Goldberg, M. C., Lasker, A. G., Zee, D. S., Garth, E., Tien, A., & Landa, R. J. (2002). Deficits in the initiation of eye movements in the absence of a visual target in adolescents with high functioning autism. Neuropsychologia, 40(12), 2039–2049.
Guitton, D., Buchtel, H. A., & Douglas, R. M. (1985). Frontal lobe lesions in man cause difficulties in suppressing reflexive glances and in generating goal-directed saccades. Experimental Brain Research, 58(3), 455–472.
Hafed, Z. M., & Clark, J. J. (2002). Microsaccades as an overt measure of covert attention shifts. Vision Research, 42, 2533–2545.
Hafed, Z. M., Goffart, L., & Krauzlis, R. J. (2009). A neural mechanism for microsaccade generation in the primate superior colliculus. Science, 323(5916), 940–943.
Hafed, Z. M., & Krauzlis, R. J. (2010). Microsaccadic suppression of visual bursts in the primate superior colliculus. The Journal of Neuroscience, 30(28), 9542–9547.
Hartikainen, K. M., Ogawa, K. H., & Knight, R. T. (2000). Transient interference of right hemispheric function due to automatic emotional processing. Neuropsychologia, 38(12), 1576–1580.
Jonides, J., & Irwin, D. E. (1981). Capturing attention. Cognition, 10(1–3), 145–150.
Kissler, J., & Keil, A. (2008). Look-don’t look! How emotional pictures affect pro- and anti-saccades. Experimental Brain Research, 188(2), 215–222.
Ko, H. K., Poletti, M., & Rucci, M. (2010). Microsaccades precisely relocate gaze in a high visual acuity task. Nature Neuroscience, 13(12), 1549–1553.
Lang, P. J., Bradley, M. M., & Cuthbert, B. N. (2005). International Affective Picture System (IAPS): Affective ratings of pictures and instruction manual (Technical Report A–6). Gainesville: University of Florida.
Lang, P. J., Bradley, M. M., & Cuthbert, B. N. (2008). International affective picture system (IAPS): Affective ratings of pictures and instruction manual (Technical Report A-8). Gainesville: University of Florida.
Lang, P. J., & Davis, M. (2006). Emotion, motivation, and the brain: Reflex foundations in animal and human research. Progress in Brain Research, 156, 3–29.
Laubrock, J., Engbert, R., & Kliegl, R. (2005). Microsaccade dynamics during covert attention. Vision Research, 45, 721–730.
Laubrock, J., Engbert, R., & Kliegl, R. (2008). Fixational eye movements predict the perceived direction of ambiguous apparent motion. Journal of Vision, 8(14), 1–17.
Martinez-Conde, S., Macknik, S. L., & Hubel, D. H. (2004). The role of fixational eye movements in visual perception. Nature Reviews Neuroscience, 5(3), 229–240.
Martinez-Conde, S., Macknik, S. L., Troncoso, X. G., & Hubel, D. H. (2009). Microsaccades: A neurophysiological analysis. Trends in Neurosciences, 32(9), 463–475.
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 of the United States of America, 96(4), 1680–1685.
Mulckhuyse, M., & Theeuwes, J. (2010). Unconscious attentional orienting to exogenous cues: A review of the literature. Acta Psychologica, 134(3), 299–309.
Nummenmaa, L., Hyönä, J., & Calvo, M. G. (2006). Eye movement assessment of selective attentional capture by emotional pictures. Emotion, 6(2), 257–268.
Nummenmaa, L., Hyönä, J., & Calvo, M. G. (2009). Emotional scene content drives the saccade generation system reflexively. Journal of Experimental Psychology: Human Perception and Performance, 35(2), 305–323.
Öhman, A., Carlsson, K., Lundqvist, D., & Ingvar, M. (2007). On the unconscious subcortical origin of human fear. Physiology & Behavior, 92(1–2), 180–185.
Otero-Millan, J., Troncoso, X. G., Macknik, S. L., Serrano-Pedraza, I., & Martinez-Conde, S. (2008). Saccades and microsaccades during visual fixation, exploration and search: Foundations for a common saccadic generator. Journal of Vision, 8(14), 1–18.
Partala, T., & Surakka, V. (2003). Pupil size variation as an indication of affective processing. International Journal of Human-Computer Studies, 59(1–2), 185–198.
Pollatos, O., Herbert, B. M., Matthias, E., & Schandry, R. (2007). Heart rate response after emotional picture presentation is modulated by interoceptive awareness. International Journal of Psychophysiology, 63(1), 117–124.
Posner, M. I. (1980). Orienting of attention. The Quarterly Journal of Experimental Psychology, 32(1), 3–25.
Posner, M. I., Walker, J. A., Friedrich, F. J., & Rafal, R. D. (1984). Effects of parietal injury on covert orienting of attention. The Journal of Neuroscience, 4, 1863–1874.
Pourtois, G., Grandjean, D., Sander, D., & Vuilleumier, P. (2004). Electrophysiological correlates of rapid spatial orienting towards fearful faces. Cerebral Cortex, 14(6), 619–633.
Rolfs, M., Engbert, R., & Kliegl, R. (2005). Crossmodal coupling of oculomotor control and spatial attention in vision and audition. Experimental Brain Research, 166(3–4), 427–439.
Rolfs, M., Kliegl, R., & Engbert, R. (2008). Toward a model of microsaccade generation: The case of microsaccadic inhibition. Journal of Vision, 8(11), 1–23.
Rösler, A., Ulrich, C., Billino, J., Sterzer, P., Weidauer, S., Bernhardt, T., et al. (2005). Effects of arousing emotional scenes on the distribution of visuospatial attention: Changes with aging and early subcortical vascular dementia. Journal of the Neurological Sciences, 229–230, 109–116.
Schneps, M., Rose, L. T., Martinez-Conde, S., & Pomplun, M. (2009). Covert orienting reflex: Involuntary pupil response predicts microsaccade production. Journal of Vision, 9(8), 399.
Schutter, D. J., & van Honk, J. (2009). The cerebellum in emotion regulation: A repetitive transcranial magnetic stimulation study. Cerebellum, 8, 28–34.
Turatto, M., Valsecchi, M., Tamè, L., & Betta, E. (2007). Microsaccades distinguish between global and local visual processing. NeuroReport, 18(10), 1015–1018.
Valsecchi, M., Betta, E., & Turatto, M. (2007a). Visual oddballs induce prolonged microsaccadic inhibition. Experimental Brain Research, 177(2), 196–208.
Valsecchi, M., & Turatto, M. (2007b). Microsaccadic response to visual events that are invisible to the Superior Colliculus. Behavioral Neuroscience, 121, 786–793.
Valsecchi, M., Dimigen, O., Kliegl, R., Sommer, W., & Turatto, M. (2009a). Microsaccadic inhibition and P300 enhancement in a visual oddball task. Psychophysiology, 46(3), 635–644.
Valsecchi, M., & Turatto, M. (2009b). Microsaccadic responses in a bimodal oddball task. Psychological Research, 73(1), 23–33.
van Reekum, C. M., Johnstone, T., Urry, H. L., Thurow, M. E., Schaefer, H. S., Alexander, A. L., et al. (2007). Gaze fixations predict brain activation during the voluntary regulation of picture-induced negative affect. Neuroimage, 36(3), 1041–1055.
Yee, R. D., Baloh, R. W., Marder, S. R., Levy, D. L., Sakala, S. M., & Honrubia, V. (1987). Eye movements in schizophrenia. Investigative Ophthalmology & Visual Science, 28(2), 366–374.
Yiend, J., & Mathews, A. (2001). Anxiety and attention to threatening pictures. The Quarterly Journal of Experimental Psychology A: Human Experimental Psychology, 54(3), 665–681.
Zhao, Z., & Davis, M. (2004). Fear-potentiated startle in rats is mediated by neurons in the deep layers of the superior colliculus/deep mesencephalic nucleus of the rostral midbrain through the glutamate non-NMDA receptors. The Journal of Neuroscience, 24(46), 10326–10334.
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This study was partially funded by a Grant-in-Aid for Young Scientists (B) from the Ministry of Education, Culture, Sports, Science and Technology of Japan (KAKENHI, 22700466).
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Appendix
Appendix
IAPS numbers for emotional stimuli. Neutral pictures: 2190, 2480, 2514, 5020, 5030, 5120, 5200, 5520, 5534, 5711, 5720, 5725, 5726, 6150, 7000, 7002, 7003, 7004, 7006, 7009, 7010, 7012, 7017, 7020, 7025, 7026, 7030, 7031, 7034, 7035, 7040, 7050, 7056, 7060, 7080, 7090, 7096, 7100, 7110, 7130, 7140, 7150, 7160, 7170, 7175, 7185, 7187, 7190, 7205, 7207, 7217, 7224, 7233, 7234, 7235, 7490, 7491, 7500, 7550, 7950. Pleasant pictures: 1410, 1440, 1460, 1540, 1590, 1595, 1600, 1601, 1603, 1710, 1750, 1920, 1999, 2000, 2040, 2045, 2050, 2057, 2058, 2070, 2071, 2080, 2150, 2165, 2250, 2311, 2340, 2341, 2347, 5010, 5600, 5830, 7200, 7230, 7280, 7282, 7283, 7325, 7330, 7340, 7350, 7352, 7430, 7405, 7461, 7475, 7476, 7482, 7487, 7488, 8030, 8041, 8080, 8162, 8200, 8350, 8370, 8380, 8467, 8470. Unpleasant pictures: 1090, 1110, 1120, 1220, 1301, 2120, 2691, 2900, 3000, 3010, 3030, 3051, 3060, 3064, 3071, 3080, 3120, 3130, 3170, 3280, 3400, 3500, 3530, 6210, 6212, 6231, 6242, 6243, 6312, 6313, 6314, 6370, 6510, 6540, 6550, 6560, 6571, 6821, 8480, 9040, 9041, 9042, 9250, 9400, 9405, 9410, 9433, 9440, 9490, 9570, 9571, 9600, 9611, 9620, 9621, 9622, 9910, 9911, 9920, 9921.
Factorial one-way ANOVA (three levels: neutral, pleasant, and unpleasant images) followed by multiple comparisons (the Holm method) was performed in the previous rating scores of valence, arousal, and dominance corresponding to the above IAPS numbers (Lang et al., 2008). In the cases of two rating scores on the same IAPS number, those values were averaged. Statistical results are summarized in Table 2.
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Kashihara, K., Okanoya, K. & Kawai, N. Emotional attention modulates microsaccadic rate and direction. Psychological Research 78, 166–179 (2014). https://doi.org/10.1007/s00426-013-0490-z
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DOI: https://doi.org/10.1007/s00426-013-0490-z