Automatic attention orienting by social and symbolic cues activates different neural networks: An fMRI study

Visual attention can be automatically re-oriented by another person's non-predictive gaze as well as by symbolic arrow cues. We investigated whether the shifts of attention triggered by biologically relevant gaze cues and biologically non-relevant arrow cues rely on the same neural systems by comparing the effects of gaze-cued and arrow-cued orienting on blood oxygenation level-dependent (BOLD) signal in humans. Participants detected laterally presented reaction signals preceded by centrally presented non-predictive gaze and arrow cues. Directional gaze cues and arrow cues were presented in separate blocks. Furthermore, two separate control blocks were run in which non-directional cues (straight gaze or segment of a line) were used. The BOLD signals during the control blocks were subtracted from those during the respective blocks with directional cues. Behavioral data showed that, for both cue types, reaction times were shorter on congruent than incongruent trials. Imaging data revealed three foci of activation for gaze-cued orienting: in the left inferior occipital gyrus and right medial and inferior occipital gyri. For arrow-cued orienting, a much more extensive network was activated. There were large postcentral activations bilaterally including areas in the medial/inferior occipital gyri and medial temporal gyri and in the left intraparietal area. Interestingly, arrow cuing also activated the right frontal eye field and supplementary eye field. The results suggest that attention orienting by gaze cues and attention orienting by arrow cues are not supported by the same cortical network and that attention orienting by symbolic arrow cues relies on mechanisms associated with voluntary shifts of attention.

[1]  Susanne Quadflieg,et al.  The owl and the pussycat: Gaze cues and visuospatial orienting , 2004, Psychonomic bulletin & review.

[2]  M. Corbetta,et al.  Neural Systems for Visual Orienting and Their Relationships to Spatial Working Memory , 2002, Journal of Cognitive Neuroscience.

[3]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[4]  Alan Kingstone,et al.  Attentional effects of counterpredictive gaze and arrow cues. , 2004, Journal of experimental psychology. Human perception and performance.

[5]  Alan Kingstone,et al.  Does gaze direction really trigger a reflexive shift of spatial attention? , 2005, Brain and Cognition.

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

[7]  J. Pratt,et al.  Symbolic Control of Visual Attention , 2001, Psychological science.

[8]  B. Bergum,et al.  Attention and performance IX , 1982 .

[9]  S. Yantis,et al.  Transient neural activity in human parietal cortex during spatial attention shifts , 2002, Nature Neuroscience.

[10]  M. Corbetta,et al.  An Event-Related Functional Magnetic Resonance Imaging Study of Voluntary and Stimulus-Driven Orienting of Attention , 2005, The Journal of Neuroscience.

[11]  Stephen M. Rao,et al.  Neural Basis of Endogenous and Exogenous Spatial Orienting: A Functional MRI Study , 1999, Journal of Cognitive Neuroscience.

[12]  Terry M. Peters,et al.  3D statistical neuroanatomical models from 305 MRI volumes , 1993, 1993 IEEE Conference Record Nuclear Science Symposium and Medical Imaging Conference.

[13]  V. Bruce,et al.  Reflexive visual orienting in response to the social attention of others , 1999 .

[14]  Jon Driver,et al.  Seen Gaze-Direction Modulates Fusiform Activity and Its Coupling with Other Brain Areas during Face Processing , 2001, NeuroImage.

[15]  E. DeYoe,et al.  A physiological correlate of the 'spotlight' of visual attention , 1999, Nature Neuroscience.

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

[17]  H. Kashima,et al.  A deficit in discriminating gaze direction in a case with right superior temporal gyrus lesion , 2006, Neuropsychologia.

[18]  Leslie G. Ungerleider,et al.  Mechanisms of directed attention in the human extrastriate cortex as revealed by functional MRI. , 1998, Science.

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

[20]  A. Nobre,et al.  The Large-Scale Neural Network for Spatial Attention Displays Multifunctional Overlap But Differential Asymmetry , 1999, NeuroImage.

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

[22]  Joel R. Meyer,et al.  A large-scale distributed network for covert spatial attention: further anatomical delineation based on stringent behavioural and cognitive controls. , 1999, Brain : a journal of neurology.

[23]  Petra Vlamings,et al.  Atypical Visual Orienting to Gaze- and Arrow-Cues in Adults with High Functioning Autism , 2005, Journal of autism and developmental disorders.

[24]  Andrew R. Mayer,et al.  Neural networks underlying endogenous and exogenous visual–spatial orienting , 2004, NeuroImage.

[25]  G. McCarthy,et al.  When Strangers Pass , 2004, Psychological science.

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

[27]  A. Kingstone,et al.  Are eyes special? It depends on how you look at it , 2002, Psychonomic bulletin & review.

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

[29]  Jason Tipples,et al.  Orienting to eye gaze and face processing. , 2005, Journal of experimental psychology. Human perception and performance.

[30]  J. Tipples Eye gaze is not unique: Automatic orienting in response to uninformative arrows , 2002, Psychonomic bulletin & review.

[31]  Richard S. J. Frackowiak,et al.  Functional localization of the system for visuospatial attention using positron emission tomography. , 1997, Brain : a journal of neurology.

[32]  Michael J. Brammer,et al.  An Event Related Functional Magnetic Resonance Imaging Study of Facial Emotion Processing in Asperger Syndrome , 2007, Biological Psychiatry.

[33]  T. Allison,et al.  Social perception from visual cues: role of the STS region , 2000, Trends in Cognitive Sciences.

[34]  J. Haxby,et al.  The distributed human neural system for face perception , 2000, Trends in Cognitive Sciences.

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

[36]  Leslie G. Ungerleider,et al.  Mechanisms of visual attention in the human cortex. , 2000, Annual review of neuroscience.

[37]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

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

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

[40]  J. Hietanen,et al.  Social attention orienting integrates visual information from head and body orientation , 2002, Psychological research.

[41]  M. Gazzaniga,et al.  Reflexive Joint Attention Depends on Lateralized Cortical Connections , 2000, Psychological science.

[42]  M. Mesulam A cortical network for directed attention and unilateral neglect , 1981, Annals of neurology.

[43]  Alan Kingstone,et al.  The eyes have it!: An fMRI investigation , 2004, Brain and Cognition.

[44]  M. Rushworth,et al.  Attention Systems and the Organization of the Human Parietal Cortex , 2001, The Journal of Neuroscience.

[45]  K. Paller,et al.  Brain networks for analyzing eye gaze. , 2003, Brain research. Cognitive brain research.

[46]  Richard B Buxton,et al.  Putting spatial attention on the map: timing and localization of stimulus selection processes in striate and extrastriate visual areas , 2001, Vision Research.

[47]  G. Mangun,et al.  The neural mechanisms of top-down attentional control , 2000, Nature Neuroscience.

[48]  T. Paus,et al.  Cortical regions involved in eye movements, shifts of attention, and gaze perception , 2005, Human brain mapping.

[49]  M Dieterich,et al.  Brain activation studies on visual-vestibular and ocular motor interaction. , 2000, Current opinion in neurology.