Potential threat attracts attention and interferes with voluntary saccades.

Several studies have shown that threatening stimuli are prioritized by the visual system. In the present study we investigated whether a stimulus associated with a threat of electrical shock attracts attention and accordingly interferes with the execution of voluntary eye movements to other locations. In 2 experiments, we showed that when a fear-conditioned and a neutral stimulus were presented simultaneously, voluntary saccades were initiated faster toward fear-conditioned compared with neutral stimuli. Moreover, saccades often erroneously went to the location of threat even when a saccade to a different location was required. This implies an automatic shift of attention to a fear-conditioned stimulus that interferes with saccade execution. The same pattern of results was found for a neutral stimulus that was always presented together with the fear-conditioned stimulus and consequently itself became associated with threat. The current results indicate that threatening stimuli attract visual attention and subsequently bias saccade target selection in a reflexive fashion.

[1]  C. Spielberger,et al.  Manual for the State-Trait Anxiety Inventory , 1970 .

[2]  G. Rizzolatti,et al.  Reorienting attention across the horizontal and vertical meridians: Evidence in favor of a premotor theory of attention , 1987, Neuropsychologia.

[3]  M. Fanselow,et al.  Differential second-order aversive conditioning using contextual stimuli , 1989 .

[4]  M. Fanselow Factors governing one-trial contextual conditioning , 1990 .

[5]  J. Theeuwes Exogenous and endogenous control of attention: The effect of visual onsets and offsets , 1991, Perception & psychophysics.

[6]  Joseph E LeDoux,et al.  Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. , 1992, Behavioral neuroscience.

[7]  J. Theeuwes Perceptual selectivity for color and form , 1992, Perception & psychophysics.

[8]  A. Maher A face in the crowd. , 1992, Orthopedic nursing.

[9]  M. Masson,et al.  Using confidence intervals in within-subject designs , 1994, Psychonomic bulletin & review.

[10]  K. Hugdahl,et al.  Peripheral cuing of covert spatial attention before and after emotional conditioning of the cue. , 1996, The International journal of neuroscience.

[11]  Joseph E LeDoux The emotional brain , 1996 .

[12]  On the Continuity of Perceptual Experience: Implications for Perception and Attention , 1996 .

[13]  S. Yantis,et al.  Visual attention: control, representation, and time course. , 1997, Annual review of psychology.

[14]  K. Mogg,et al.  A cognitive-motivational analysis of anxiety. , 1998, Behaviour research and therapy.

[15]  D. E. Irwin,et al.  Our Eyes do Not Always Go Where we Want Them to Go: Capture of the Eyes by New Objects , 1998 .

[16]  Kenneth Hugdahl,et al.  Emotional modulation of attention orienting: A classical conditioning study , 1999 .

[17]  David E. Irwin,et al.  Influence of attentional capture on oculomotor control. , 1999, Journal of experimental psychology. Human perception and performance.

[18]  E. Fox,et al.  Facial Expressions of Emotion: Are Angry Faces Detected More Efficiently? , 2000, Cognition & emotion.

[19]  A. Ohman,et al.  The face in the crowd revisited: a threat advantage with schematic stimuli. , 2001, Journal of personality and social psychology.

[20]  E. Fox,et al.  Do threatening stimuli draw or hold visual attention in subclinical anxiety? , 2001, Journal of experimental psychology. General.

[21]  A. Ohman,et al.  Emotion drives attention: detecting the snake in the grass. , 2001, Journal of experimental psychology. General.

[22]  J. Theeuwes,et al.  Programming of endogenous and exogenous saccades: evidence for a competitive integration model. , 2002, Journal of experimental psychology. Human perception and performance.

[23]  R. Dolan,et al.  Modulation of spatial attention by fear-conditioned stimuli: an event-related fMRI study , 2002, Neuropsychologia.

[24]  J. Grafman,et al.  The Human Amygdala: An Evolved System for Relevance Detection , 2003, Reviews in the neurosciences.

[25]  W. Roth,et al.  Selective attention in anxiety: Distraction and enhancement in visual search , 2003, Depression and anxiety.

[26]  J. O'Doherty,et al.  Encoding Predictive Reward Value in Human Amygdala and Orbitofrontal Cortex , 2003, Science.

[27]  O. Lipp,et al.  Snakes and cats in the flower bed: fast detection is not specific to pictures of fear-relevant animals. , 2004, Emotion.

[28]  Thomas Weiss,et al.  Eye movements and behavioral responses to threatening and nonthreatening stimuli during visual search in phobic and nonphobic subjects. , 2004, Emotion.

[29]  G. Crombez,et al.  Does imminent threat capture and hold attention? , 2004, Emotion.

[30]  J. W. Rudy,et al.  Understanding contextual fear conditioning: insights from a two-process model , 2004, Neuroscience & Biobehavioral Reviews.

[31]  Karin Mogg,et al.  BRIEF REPORT Time course of attentional bias for threat scenes: Testing the vigilance‐avoidance hypothesis , 2004 .

[32]  Paul Pauli,et al.  Binocular rivalry between emotional and neutral stimuli: a validation using fear conditioning and EEG. , 2005, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[33]  A. Reinecke,et al.  Speeded detection and increased distraction in fear of spiders: evidence from eye movements. , 2005, Journal of abnormal psychology.

[34]  P. Vuilleumier,et al.  How brains beware: neural mechanisms of emotional attention , 2005, Trends in Cognitive Sciences.

[35]  J. Hyönä,et al.  Eye movement assessment of selective attentional capture by emotional pictures. , 2006, Emotion.

[36]  M. Kindt,et al.  Contextual control of human fear associations in a renewal paradigm. , 2007, Behaviour research and therapy.

[37]  O. Lipp,et al.  When danger lurks in the background: attentional capture by animal fear-relevant distractors is specific and selectively enhanced by animal fear. , 2007, Emotion.

[38]  A. Kingstone,et al.  The effect of emotional faces on eye movements and attention , 2007 .

[39]  M. Adamek,et al.  Depression and anxiety. , 2013, The Medical journal of Australia.

[40]  Andreas Keil,et al.  Look–don’t look! How emotional pictures affect pro- and anti-saccades , 2008, Experimental Brain Research.

[41]  O. A. Andreassen,et al.  The human amygdala is involved in general behavioral relevance detection: Evidence from an event-related functional magnetic resonance imaging Go-NoGo task , 2008, Neuroscience.

[42]  Geert Crombez,et al.  Attentional bias to threat: a perceptual accuracy approach. , 2008, Emotion.

[43]  B. de Gelder,et al.  Orienting to threat: faster localization of fearful facial expressions and body postures revealed by saccadic eye movements , 2009, Proceedings of the Royal Society B: Biological Sciences.

[44]  D. Neumann,et al.  The development of an attentional bias for angry faces following Pavlovian fear conditioning. , 2009, Behaviour research and therapy.

[45]  J. Hyönä,et al.  Emotional scene content drives the saccade generation system reflexively. , 2009, Journal of experimental psychology. Human perception and performance.

[46]  A. Ohman,et al.  Some animal specific fears are more specific than others: Evidence from attention and emotion measures. , 2009, Behaviour research and therapy.

[47]  S. Damme,et al.  Signals of threat do not capture , but prioritize attention : a classical conditioning approach , 2010 .

[48]  J. Theeuwes Top-down and bottom-up control of visual selection. , 2010, Acta psychologica.

[49]  Tad T. Brunyé,et al.  Keeping Your Eyes on the Prize , 2010, Psychological science.

[50]  M. Milders,et al.  Attentional bias to brief threat-related faces revealed by saccadic eye movements. , 2010, Emotion.

[51]  P. I. Pavlov Conditioned reflexes: An investigation of the physiological activity of the cerebral cortex. , 1929, Annals of Neurosciences.

[52]  L. Pessoa,et al.  Emotion processing and the amygdala: from a 'low road' to 'many roads' of evaluating biological significance , 2010, Nature Reviews Neuroscience.

[53]  M. Trimble,et al.  The Human Amygdala , 2010 .

[54]  J. Theeuwes,et al.  Signals of threat do not capture, but prioritize, attention: a conditioning approach. , 2011, Emotion.

[55]  Marco Tamietto,et al.  Emotion in the brain: of low roads, high roads and roads less travelled , 2011, Nature Reviews Neuroscience.

[56]  Steven Yantis,et al.  Learned Value Magnifies Salience-Based Attentional Capture , 2011, PloS one.

[57]  Chad R. Mortensen,et al.  The face in the crowd effect unconfounded: Happy faces, not angry faces, are more efficiently detected in the visual search task , 2011 .

[58]  Chad R. Mortensen,et al.  Journal of Experimental Psychology: General Single-and Multiple-target Visual Search Tasks , 2022 .

[59]  James E Witnauer,et al.  The role of within-compound associations in learning about absent cues , 2011, Learning & behavior.

[60]  J. Theeuwes,et al.  Angry faces hold the eyes , 2011 .

[61]  J. Theeuwes,et al.  The presence of threat affects saccade trajectories , 2012 .

[62]  J. Theeuwes,et al.  Updating the premotor theory: the allocation of attention is not always accompanied by saccade preparation. , 2012, Journal of experimental psychology. Human perception and performance.

[63]  J. Theeuwes,et al.  Reward grabs the eye: Oculomotor capture by rewarding stimuli , 2012, Vision Research.

[64]  G. Crombez,et al.  Conditioned fear modulates visual selection. , 2013, Emotion.

[65]  Jan Theeuwes,et al.  Exogenous visual orienting by reward. , 2014, Journal of vision.

[66]  Jan Theeuwes,et al.  Attentional capture by signals of threat , 2014 .

[67]  G. Urcelay,et al.  The functions of contexts in associative learning , 2014, Behavioural Processes.