Lack of automatic attentional orienting by gaze cues following a bilateral loss of visual cortex

In social interactions, the location of relevant stimuli is often indicated by the orientation of gaze. It has been proposed that the direction of gaze might produce an automatic cueing of attention, similar to what is observed with exogenous cues. However, several reports have challenged this claim by demonstrating that the behavioral gain that arises with gaze cueing could be explained by shifts of attention, which are intentional and not automatic. We reasoned that if cueing by gaze was truly automatic, it should occur without awareness and should be sustained by subcortical circuits, including the amygdalae, independently of the main geniculo-striate visual pathway. We presented a cross-modal version of the Posner cueing paradigm to a patient (TN) with bilateral lesions of occipital cortex (Burra et al., 2013; Pegna, Khateb, Lazeyras, & Seghier, 2005). TN was asked to localize a sound using a key press. The location of the sound was congruent or incongruent with the direction of gaze of a face-cue. In groups of healthy young and age-matched participants, we observed significantly longer response times for incongruent than congruent sounds, suggesting that gaze direction interfered with processing of localized sounds. By contrast, TN׳s performance was not affected by sound-gaze congruence. The results suggest that the processing of gaze orientation cannot occur in the absence of geniculo-striate processing, suggesting that it is not automatic.

[1]  Matthew Rizzo,et al.  Eye gaze does not produce reflexive shifts of attention: Evidence from frontal-lobe damage , 2006, Neuropsychologia.

[2]  P. Garthwaite,et al.  Investigation of the single case in neuropsychology: confidence limits on the abnormality of test scores and test score differences , 2002, Neuropsychologia.

[3]  S. Tipper,et al.  Orienting attention via observed gaze shift evokes longer term inhibitory effects: implications for social interactions, attention, and memory. , 2004, Journal of experimental psychology. General.

[4]  Alexis Hervais-Adelman,et al.  Amygdala Activation for Eye Contact Despite Complete Cortical Blindness , 2013, The Journal of Neuroscience.

[5]  Béatrice de Gelder,et al.  Dissociation between Goal-directed and Discrete Response Localization in a Patient with Bilateral Cortical Blindness , 2013, Journal of Cognitive Neuroscience.

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

[7]  S. Tipper,et al.  Gaze cueing of attention: visual attention, social cognition, and individual differences. , 2007, Psychological bulletin.

[8]  Luca Passamonti,et al.  Connectivity Analysis Reveals a Cortical Network for Eye Gaze Perception , 2009, Cerebral cortex.

[9]  A Cohen,et al.  Extrageniculate vision in hemianopic humans: saccade inhibition by signals in the blind field. , 1990, Science.

[10]  Jon Driver,et al.  Covert Spatial Orienting in Audition: Exogenous and Endogenous Mechanisms , 1994 .

[11]  A. Cowey The blindsight saga , 2009, Experimental Brain Research.

[12]  David A Leopold,et al.  Primary visual cortex: awareness and blindsight. , 2012, Annual review of neuroscience.

[13]  Andrew P Bayliss,et al.  Gaze and arrow cueing of attention reveals individual differences along the autism spectrum as a function of target context. , 2005, British journal of psychology.

[14]  Asaid Khateb,et al.  Electrophysiological evidence for early non-conscious processing of fearful facial expressions. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[15]  岡田 俊 Involvement of medial temporal structures in reflexive attentional shift by gaze , 2009 .

[16]  Su-Ling Yeh,et al.  Look into my eyes and I will see you: Unconscious processing of human gaze , 2012, Consciousness and Cognition.

[17]  J. Haxby,et al.  Distinct representations of eye gaze and identity in the distributed human neural system for face perception , 2000, Nature Neuroscience.

[18]  J. Jonides Voluntary versus automatic control over the mind's eye's movement , 1981 .

[19]  L Weiskrantz,et al.  Visual capacity in the hemianopic field following a restricted occipital ablation. , 1974, Brain : a journal of neurology.

[20]  S. Baron-Cohen,et al.  Gaze Perception Triggers Reflexive Visuospatial Orienting , 1999 .

[21]  O. Landry,et al.  A meta-analysis of visual orienting in autism , 2013, Front. Hum. Neurosci..

[22]  J. Hietanen,et al.  Does facial expression affect attention orienting by gaze direction cues? , 2003, Journal of experimental psychology. Human perception and performance.

[23]  The importance of context information for the spatial specificity of gaze cueing , 2013, Attention, perception & psychophysics.

[24]  N. Logothetis,et al.  Activity changes in early visual cortex reflect monkeys' percepts during binocular rivalry , 1996, Nature.

[25]  Alan Kingstone,et al.  Abrupt onsets and gaze direction cues trigger independent reflexive attentional effects , 2003, Cognition.

[26]  K. Nakamura,et al.  The human amygdala plays an important role in gaze monitoring. A PET study. , 1999, Brain : a journal of neurology.

[27]  M. Posner,et al.  Components of visual orienting , 1984 .

[28]  Bernard M. C. Stienen,et al.  Intact navigation skills after bilateral loss of striate cortex , 2008, Current Biology.

[29]  Christopher J. Aura,et al.  Divergence of fMRI and neural signals in V1 during perceptual suppression in the awake monkey , 2008, Nature Neuroscience.

[30]  Melvyn A. Goodale,et al.  Grasping the non-conscious: Preserved grip scaling to unseen objects for immediate but not delayed grasping following a unilateral lesion to primary visual cortex , 2011, Vision Research.

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

[32]  Patrik Vuilleumier,et al.  Processing social aspects of human gaze: A combined fMRI-DTI study , 2011, NeuroImage.

[33]  M. Posner,et al.  Orienting of Attention* , 1980, The Quarterly journal of experimental psychology.

[34]  M. Posner,et al.  Orienting of visual attention in progressive supranuclear palsy. , 1988, Brain : a journal of neurology.

[35]  J. Bargh The four horsemen of automaticity: Awareness, intention, efficiency, and control in social cognition. , 1994 .

[36]  Wataru Sato,et al.  Attentional shift by gaze is triggered without awareness , 2007, Experimental Brain Research.

[37]  J. Hietanen Does your gaze direction and head orientation shift my visual attention? , 1999, Neuroreport.

[38]  M. Tamietto,et al.  Neural bases of the non-conscious perception of emotional signals , 2010, Nature Reviews Neuroscience.

[39]  Paul B Hibbard,et al.  Consciousness of the first order in blindsight , 2010, Proceedings of the National Academy of Sciences.

[40]  A. Kingstone,et al.  The eyes have it! Reflexive orienting is triggered by nonpredictive gaze , 1998 .

[41]  P Vuilleumier,et al.  Perceived gaze direction in faces and spatial attention: a study in patients with parietal damage and unilateral neglect , 2002, Neuropsychologia.