Effects of emotional and non-emotional cues on visual search in neglect patients: Evidence for distinct sources of attentional guidance

In normal observers, visual search is facilitated for targets with salient attributes. We compared how two different types of cue (expression and colour) may influence search for face targets, in healthy subjects (n=27) and right brain-damaged patients with left spatial neglect (n=13). The target faces were defined by their identity (singleton among a crowd of neutral faces) but could either be neutral (like other faces), or have a different emotional expression (fearful or happy), or a different colour (red-tinted). Healthy subjects were the fastest for detecting the colour-cued targets, but also showed a significant facilitation for emotionally cued targets, relative to neutral faces differing from other distracter faces by identity only. Healthy subjects were also faster overall for target faces located on the left, as compared to the right side of the display. In contrast, neglect patients were slower to detect targets on the left (contralesional) relative to the right (ipsilesional) side. However, they showed the same pattern of cueing effects as healthy subjects on both sides of space; while their best performance was also found for faces cued by colour, they showed a significant advantage for faces cued by expression, relative to the neutral condition. These results indicate that despite impaired attention towards the left hemispace, neglect patients may still show an intact influence of both low-level colour cues and emotional expression cues on attention, suggesting that neural mechanisms responsible for these effects are partly separate from fronto-parietal brain systems controlling spatial attention during search.

[1]  Ken Nakayama,et al.  Attentional requirements in a ‘preattentive’ feature search task , 1997, Nature.

[2]  M. Behrmann,et al.  Parietal cortex and attention , 2004, Current Opinion in Neurobiology.

[3]  S. Rauch,et al.  Masked Presentations of Emotional Facial Expressions Modulate Amygdala Activity without Explicit Knowledge , 1998, The Journal of Neuroscience.

[4]  J. Eastwood,et al.  Negative facial expression captures attention and disrupts performance , 2003, Perception & psychophysics.

[5]  Clara D. Martin,et al.  Controlling for interstimulus perceptual variance abolishes N170 face selectivity , 2007, Nature Neuroscience.

[6]  Bruno Rossion,et al.  Controlling interstimulus perceptual variance does not abolish N170 face sensitivity , 2007, Nature Neuroscience.

[7]  Gilles Pourtois,et al.  Neural systems for orienting attention to the location of threat signals: An event-related fMRI study , 2006, NeuroImage.

[8]  Leslie G. Ungerleider,et al.  Attentional control of the processing of neural and emotional stimuli. , 2002, Brain research. Cognitive brain research.

[9]  Evian Gordon,et al.  A Direct Brainstem–amygdala–cortical Dalarmt System for Subliminal Signals of Fear , 2004 .

[10]  Patrik Vuilleumier,et al.  Impaired Perceptual Memory of Locations across Gaze-shifts in Patients with Unilateral Spatial Neglect , 2007, Journal of Cognitive Neuroscience.

[11]  K. Scherer,et al.  Appraisal processes in emotion: Theory, methods, research. , 2001 .

[12]  Chris Rorden,et al.  The anatomy of spatial neglect based on voxelwise statistical analysis: a study of 140 patients. , 2004, Cerebral cortex.

[13]  S. Dehaene,et al.  Nonconscious semantic processing of emotional words modulates conscious access. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[14]  M. Carrasco,et al.  PSYCHOLOGICAL SCIENCE Research Article Emotion Facilitates Perception and Potentiates the Perceptual Benefits of Attention , 2022 .

[15]  P. Cavanagh,et al.  FACIAL ORGANIZATION BLOCKS ACCESS TO LOW-LEVEL FEATURES: AN OBJECT INFERIORITY EFFECT , 1995 .

[16]  J. Mattingley,et al.  Unconscious perception of non-threatening facial emotion in parietal extinction , 2003, Experimental Brain Research.

[17]  Daniel Lundqvist,et al.  Looking for foes and friends: perceptual and emotional factors when finding a face in the crowd. , 2005, Emotion.

[18]  E. Phelps,et al.  The human amygdala. , 2009 .

[19]  R. Dolan,et al.  Distant influences of amygdala lesion on visual cortical activation during emotional face processing , 2004, Nature Neuroscience.

[20]  R. Dolan,et al.  Distinct spatial frequency sensitivities for processing faces and emotional expressions , 2003, Nature Neuroscience.

[21]  D. Maurer,et al.  The many faces of configural processing , 2002, Trends in Cognitive Sciences.

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

[23]  P Bartolomeo,et al.  [Presenting a battery for assessing spatial neglect. Norms and effects of age, educational level, sex, hand and laterality]. , 2001, Revue neurologique.

[24]  W. Milberg,et al.  Preattentive and attentive visual search in individuals with hemispatial neglect. , 2000, Neuropsychology.

[25]  B. Gelder Towards the neurobiology of emotional body language , 2006, Nature Reviews Neuroscience.

[26]  P Vuilleumier,et al.  Neural response to emotional faces with and without awareness: event-related fMRI in a parietal patient with visual extinction and spatial neglect , 2002, Neuropsychologia.

[27]  Peter J. Lang,et al.  Parallel amygdala and inferotemporal activation reflect emotional intensity and fear relevance , 2005, NeuroImage.

[28]  Jon Driver,et al.  Revisiting Previously Searched Locations in Visual Neglect: Role of Right Parietal and Frontal Lesions in Misjudging Old Locations as New , 2005, Journal of Cognitive Neuroscience.

[29]  A. Ohman,et al.  Emotional conditioning to masked stimuli: expectancies for aversive outcomes following nonrecognized fear-relevant stimuli. , 1998, Journal of experimental psychology. General.

[30]  M. Corbetta,et al.  Influence of Stimulus Salience and Attentional Demands on Visual Search Patterns in Hemispatial Neglect , 1997, Brain and Cognition.

[31]  J-M Beis,et al.  Sensitivity of clinical and behavioural tests of spatial neglect after right hemisphere stroke , 2002, Journal of neurology, neurosurgery, and psychiatry.

[32]  E. Fox Processing emotional facial expressions: The role of anxiety and awareness , 2002, Cognitive, affective & behavioral neuroscience.

[33]  Leslie G. Ungerleider,et al.  The neural basis of biased competition in human visual cortex , 2001, Neuropsychologia.

[34]  D. Grandjean,et al.  Electrophysiological correlates of rapid spatial orienting towards fearful faces. , 2004, Cerebral cortex.

[35]  L Weiskrantz,et al.  Non-conscious recognition of affect in the absence of striate cortex. , 1999, Neuroreport.

[36]  Patrik Vuilleumier,et al.  Effects of emotional prosody on auditory extinction for voices in patients with spatial neglect , 2008, Neuropsychologia.

[37]  K. Scherer Appraisal considered as a process of multilevel sequential checking. , 2001 .

[38]  A. Kertesz Localization in neuropsychology , 1983 .

[39]  S. Zeki,et al.  The architecture of the colour centre in the human visual brain: new results and a review * , 2000, The European journal of neuroscience.

[40]  D. Amaral,et al.  Topographic organization of projections from the amygdala to the visual cortex in the macaque monkey , 2003, Neuroscience.

[41]  Patrik Vuilleumier,et al.  Emotional facial expressions capture attention , 2001, Neurology.

[42]  J. Driver,et al.  Perceptual awareness and its loss in unilateral neglect and extinction , 2001, Cognition.

[43]  R. Henson,et al.  Multiple levels of visual object constancy revealed by event-related fMRI of repetition priming , 2002, Nature Neuroscience.

[44]  Luiz Pessoa,et al.  Target visibility and visual awareness modulate amygdala responses to fearful faces. , 2006, Cerebral cortex.

[45]  K M Heilman,et al.  Selective attention in hemispatial neglect. , 1989, Archives of neurology.

[46]  Shaul Hochstein,et al.  Searching with Unilateral Neglect , 2002, Journal of Cognitive Neuroscience.

[47]  Glyn W. Humphreys,et al.  Perceptual and Action Systems in Unilateral Visual Neglect , 1987 .

[48]  Gilles Pourtois,et al.  Time Course of Brain Activity during Change Blindness and Change Awareness: Performance is Predicted by Neural Events before Change Onset , 2006, Journal of Cognitive Neuroscience.

[49]  A. Treisman,et al.  A feature-integration theory of attention , 1980, Cognitive Psychology.

[50]  Leslie G. Ungerleider,et al.  Visual awareness and the detection of fearful faces. , 2005, Emotion.

[51]  C. Cavada,et al.  The anatomical connections of the macaque monkey orbitofrontal cortex. A review. , 2000, Cerebral cortex.

[52]  R. Zahn,et al.  Asymmetries of visual attention after circumscribed subcortical vascular lesions , 2001, Journal of neurology, neurosurgery, and psychiatry.

[53]  J. Bogousslavsky,et al.  The Behavioral and Cognitive Neurology of Stroke: Index , 2007 .

[54]  J. Duncan,et al.  Visual search and stimulus similarity. , 1989, Psychological review.

[55]  J. Mattingley,et al.  Look at me, I'm smiling: Visual search for threatening and nonthreatening facial expressions , 2005 .

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

[57]  G. Vallar Extrapersonal Visual Unilateral Spatial Neglect and Its Neuroanatomy , 2001, NeuroImage.

[58]  Leslie G. Ungerleider,et al.  Repetition suppression of faces is modulated by emotion. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[59]  D. Amaral,et al.  The amygdala: is it an essential component of the neural network for social cognition? , 2003, Neuropsychologia.

[60]  Asaid Khateb,et al.  Discriminating emotional faces without primary visual cortices involves the right amygdala , 2005, Nature Neuroscience.

[61]  Karl J. Friston,et al.  Incorporating Prior Knowledge into Image Registration , 1997, NeuroImage.

[62]  M Mennemeier,et al.  Disorganized search on cancellation is not a consequence of neglect , 2004, Neurology.

[63]  N. Lavie,et al.  Changing Faces: A Detection Advantage in the Flicker Paradigm , 2001, Psychological science.

[64]  C. Kennard,et al.  The anatomy of visual neglect. , 2003, Brain : a journal of neurology.

[65]  C. Rorden,et al.  Stereotaxic display of brain lesions. , 2000, Behavioural neurology.

[66]  M. Jeannerod Neurophysiological and neuropsychological aspects of spatial neglect. , 1987 .

[67]  L. F. Barrett,et al.  The role of the amygdala in visual awareness , 2007, Trends in Cognitive Sciences.

[68]  D. Perani,et al.  The anatomy of unilateral neglect after right-hemisphere stroke lesions. A clinical/CT-scan correlation study in man , 1986, Neuropsychologia.

[69]  Giuseppe Vallar,et al.  The Cognitive and Neural Bases of Spatial Neglect , 2002 .

[70]  R. Rafal,et al.  Neural fate of seen and unseen faces in visuospatial neglect: A combined event-related functional MRI and event-related potential study , 2001, Proceedings of the National Academy of Sciences of the United States of America.

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

[72]  Adam P. Morris,et al.  Amygdala Responses to Fearful and Happy Facial Expressions under Conditions of Binocular Suppression , 2004, The Journal of Neuroscience.

[73]  M. Posner,et al.  How do the parietal lobes direct covert attention? , 1987, Neuropsychologia.

[74]  Daniel Lundqvist,et al.  Emotion regulates attention: The relation between facial configurations, facial emotion, and visual attention , 2005 .

[75]  Marlene Behrmann,et al.  Hemispatial Neglect and Visual Search: A Large Scale Analysis , 2004, Cortex.

[76]  T. Landis,et al.  Opposite cerebral hemispheric superiorities for visual associative processing of emotional facial expressions and objects , 1979, Nature.

[77]  R. Dolan,et al.  Conscious and unconscious emotional learning in the human amygdala , 1998, Nature.

[78]  Wilhelm Küker,et al.  The cortical substrate of visual extinction , 2003, Neuroreport.

[79]  Patrik Vuilleumier,et al.  Beware and be aware: Capture of spatial attention by fear-related stimuli in neglect , 2001, Neuroreport.

[80]  B. Wilson,et al.  Development of a behavioral test of visuospatial neglect. , 1987, Archives of physical medicine and rehabilitation.

[81]  A. Mack,et al.  What we see: Inattention and the capture of attention by meaning , 2002, Consciousness and Cognition.

[82]  R. Dolan,et al.  Effects of Attention and Emotion on Face Processing in the Human Brain An Event-Related fMRI Study , 2001, Neuron.

[83]  M. Fenske,et al.  Modulation of focused attention by faces expressing emotion: evidence from flanker tasks. , 2003, Emotion.

[84]  R. J Dolan,et al.  Common and distinct neural responses during direct and incidental processing of multiple facial emotions , 2003, NeuroImage.

[85]  Theodor Landis,et al.  Explicit and implicit perception of illusory contours in unilateral spatial neglect: behavioural and anatomical correlates of preattentive grouping mechanisms , 2001, Neuropsychologia.

[86]  Anna Berti,et al.  Unconscious processing in neglect , 2002 .

[87]  G. McCarthy,et al.  Dissociable prefrontal brain systems for attention and emotion , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[88]  C. Kennard,et al.  Distractor-dependent frontal neglect , 1997, Neuropsychologia.

[89]  Robert D McIntosh,et al.  The neurological basis of visual neglect , 2005, Current opinion in neurology.

[90]  J. Haxby,et al.  Human neural systems for face recognition and social communication , 2002, Biological Psychiatry.

[91]  Curt A. Carlson,et al.  Aging and visual search: automatic and controlled attentional bias to threat faces. , 2006, Acta psychologica.

[92]  Karl J. Friston,et al.  A neuromodulatory role for the human amygdala in processing emotional facial expressions. , 1998, Brain : a journal of neurology.

[93]  R. Cubelli,et al.  Neglect Without Extinction , 1999, Cortex.

[94]  Tobias Brosch,et al.  That baby caught my eye... attention capture by infant faces. , 2007, Emotion.

[95]  L. Gauthier,et al.  The Bells Test: A quantitative and qualitative test for visual neglect. , 1989 .

[96]  J. Wolfe,et al.  What attributes guide the deployment of visual attention and how do they do it? , 2004, Nature Reviews Neuroscience.

[97]  J Driver,et al.  Group study of an “undercover” test for visuospatial neglect: invisible cancellation can reveal more neglect than standard cancellation , 2004, Journal of Neurology, Neurosurgery & Psychiatry.

[98]  E. Fox,et al.  Anxiety modulates the degree of attentive resources required to process emotional faces , 2005, Cognitive, affective & behavioral neuroscience.

[99]  J. Ashburner,et al.  Multimodal Image Coregistration and Partitioning—A Unified Framework , 1997, NeuroImage.

[100]  A. Mack Inattentional Blindness , 2003 .

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

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

[103]  Leif Johannsen,et al.  Normalized perfusion MRI to identify common areas of dysfunction: patients with basal ganglia neglect. , 2005, Brain : a journal of neurology.

[104]  L. Weiskrantz,et al.  Differential extrageniculostriate and amygdala responses to presentation of emotional faces in a cortically blind field. , 2001, Brain : a journal of neurology.

[105]  K. Mogg,et al.  Some methodological issues in assessing attentional biases for threatening faces in anxiety: a replication study using a modified version of the probe detection task. , 1999, Behaviour research and therapy.