The influence of directed covert attention on emotional face processing

Activation of the amygdala and the fusiform face area (FFA) are consistent findings in imaging studies on emotional face processing. There is evidence that these activations occur even when emotional faces are unattended; however, it was also shown that amygdala and FFA activation were modulated by the attentional resources allocated to these stimuli. Attentional resources might thereby not only depend on task demands but also on varying degrees of covert attention processes induced by the task. To address this issue we examined the isolated effect of covert shifts of spatial attention on emotional face processing using functional magnetic resonance imaging during a modified spatial cueing paradigm. Directional spatial and neutral cues were presented superimposed on neutral, happy, sad and fearful faces. Subjects performed a target detection task, while fixation was controlled by simultaneous eye tracking. Reaction times showed a strong cue validity effect across all emotions (i.e., faster responses for directional cues). Comparing directed to nondirected attention revealed a significantly reduced signal in the FFA irrespective of the emotional expression. This effect was also seen in bilateral amygdala, but only in trials including fearful faces. Our findings suggest that covert shifts of attention toward a specific location result in reduced face processing independent from task demands. Furthermore, our data show a task-irrelevant amygdala response specific to fearful faces under a wide attentional focus. Attentional disengagement from the faces led to a suppression of this amygdala response and thus provides further evidence that amygdala activation depends on the focus of attention.

[1]  P. Verghese Visual Search and Attention A Signal Detection Theory Approach , 2001, Neuron.

[2]  N. Lavie Perceptual load as a necessary condition for selective attention. , 1995, Journal of experimental psychology. Human perception and performance.

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

[4]  Katsumi Aoki,et al.  Recent development of flow visualization , 2004, J. Vis..

[5]  M. Carrasco Covert attention increases contrast sensitivity: Psychophysical, neurophysiological and neuroimaging studies. , 2006, Progress in brain research.

[6]  M. Posner,et al.  Attention and the detection of signals. , 1980, Journal of experimental psychology.

[7]  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.

[8]  Takashi R Sato,et al.  Neuronal Basis of Covert Spatial Attention in the Frontal Eye Field , 2005, The Journal of Neuroscience.

[9]  A. von Leupoldt,et al.  Specificity of cognitive biases in patients with current depression and remitted depression and in patients with asthma , 2009, Psychological Medicine.

[10]  Christian Büchel,et al.  Elevated responses to constant facial emotions in different faces in the human amygdala: an fMRI study of facial identity and expression , 2004, BMC Neuroscience.

[11]  Carsten Nicolas Boehler,et al.  Mandatory Processing of Irrelevant Fearful Face Features in Visual Search , 2010, Journal of Cognitive Neuroscience.

[12]  Gereon R Fink,et al.  Cerebral correlates of alerting, orienting and reorienting of visuospatial attention: an event-related fMRI study , 2004, NeuroImage.

[13]  Marisa Carrasco,et al.  Covert attention effects on spatial resolution. , 2009, Progress in brain research.

[14]  N. Lavie Distracted and confused?: Selective attention under load , 2005, Trends in Cognitive Sciences.

[15]  F. McGlone,et al.  The role of spatial attention in the processing of facial expression: An ERP study of rapid brain responses to six basic emotions , 2003, Cognitive, affective & behavioral neuroscience.

[16]  Rob Jenkins,et al.  Neural processing of fearful faces: effects of anxiety are gated by perceptual capacity limitations. , 2007, Cerebral cortex.

[17]  Matthew Garner,et al.  Biases in visual orienting to negative and positive scenes in dysphoria: An eye movement study. , 2007, Journal of abnormal psychology.

[18]  Bradley J Wolfgang,et al.  Spatial uncertainty explains exogenous and endogenous attentional cuing effects in visual signal detection. , 2007, Journal of vision.

[19]  Ralph Adolphs,et al.  Fear, faces, and the human amygdala , 2008, Current Opinion in Neurobiology.

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

[21]  Michael Angstadt,et al.  Beyond threat: Amygdala reactivity across multiple expressions of facial affect , 2006, NeuroImage.

[22]  Leslie G. Ungerleider,et al.  Neural processing of emotional faces requires attention , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[23]  M. Eimer,et al.  The processing of emotional facial expression is gated by spatial attention: evidence from event-related brain potentials. , 2003, Brain research. Cognitive brain research.

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

[25]  Thomas M. Moerland,et al.  Fate of unattended fearful faces in the amygdala is determined by both attentional resources and cognitive modulation , 2005, NeuroImage.

[26]  Gereon R. Fink,et al.  Cue validity modulates the neural correlates of covert endogenous orienting of attention in parietal and frontal cortex , 2006, NeuroImage.

[27]  Martin Ingvar,et al.  On the unconscious subcortical origin of human fear , 2007, Physiology & Behavior.

[28]  Jan Gläscher,et al.  Visualization of Group Inference Data in Functional Neuroimaging , 2009, Neuroinformatics.

[29]  Jacob Nachmias,et al.  Contrast discrimination with and without spatial uncertainty , 2002, Vision Research.

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

[31]  Bertram Gawronski,et al.  Cognitive vulnerability to anxiety: A review and an integrative model. , 2009, Clinical psychology review.

[32]  N. Kanwisher,et al.  The fusiform face area: a cortical region specialized for the perception of faces , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[33]  A. Anderson,et al.  Neural Correlates of the Automatic Processing of Threat Facial Signals , 2022 .

[34]  Katherine M. Armstrong,et al.  Visuomotor Origins of Covert Spatial Attention , 2003, Neuron.

[35]  S. R. Schmidt,et al.  The emotional memory effect: Differential processing or item distinctiveness? , 2007, Memory & cognition.

[36]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[37]  L. Leyman,et al.  The Karolinska Directed Emotional Faces: A validation study , 2008 .

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

[39]  S. Bishop,et al.  Neural Mechanisms Underlying Selective Attention to Threat , 2008, Annals of the New York Academy of Sciences.