Mapping the impairment in decoding static facial expressions of emotion in prosopagnosia

Abstract Acquired prosopagnosia is characterized by a deficit in face recognition due to diverse brain lesions, but interestingly most prosopagnosic patients suffering from posterior lesions use the mouth instead of the eyes for face identification. Whether this bias is present for the recognition of facial expressions of emotion has not yet been addressed. We tested PS, a pure case of acquired prosopagnosia with bilateral occipitotemporal lesions anatomically sparing the regions dedicated for facial expression recognition. PS used mostly the mouth to recognize facial expressions even when the eye area was the most diagnostic. Moreover, PS directed most of her fixations towards the mouth. Her impairment was still largely present when she was instructed to look at the eyes, or when she was forced to look at them. Control participants showed a performance comparable to PS when only the lower part of the face was available. These observations suggest that the deficits observed in PS with static images are not solely attentional, but are rooted at the level of facial information use. This study corroborates neuroimaging findings suggesting that the Occipital Face Area might play a critical role in extracting facial features that are integrated for both face identification and facial expression recognition in static images.

[1]  B. Gillam,et al.  Stereoscopic discrimination of the layout of ground surfaces. , 2009, Journal of vision.

[2]  Robin A A Ince,et al.  Eye coding mechanisms in early human face event-related potentials. , 2014, Journal of vision.

[3]  Glyn W. Humphreys,et al.  Expression is computed separately from facial identity, and it is computed separately for moving and static faces: Neuropsychological evidence , 1993, Neuropsychologia.

[4]  Giuseppe Iaria,et al.  Perceptual and anatomic patterns of selective deficits in facial identity and expression processing , 2011, Neuropsychologia.

[5]  A. Watson,et al.  Quest: A Bayesian adaptive psychometric method , 1983, Perception & psychophysics.

[6]  Philippe G Schyns,et al.  Accurate statistical tests for smooth classification images. , 2005, Journal of vision.

[7]  D. Perrett,et al.  Facial expression megamix: Tests of dimensional and category accounts of emotion recognition , 1997, Cognition.

[8]  M. Seghier,et al.  A network of occipito-temporal face-sensitive areas besides the right middle fusiform gyrus is necessary for normal face processing. , 2003, Brain : a journal of neurology.

[9]  Cindy M. Bukach,et al.  Preservation of mouth region processing in two cases of prosopagnosia. , 2008, Journal of neuropsychology.

[10]  D. Fiset,et al.  Efficient visual information for unfamiliar face matching despite viewpoint variations: It’s not in the eyes! , 2016, Vision Research.

[11]  Galia Avidan,et al.  A detailed investigation of facial expression processing in congenital prosopagnosia as compared to acquired prosopagnosia , 2006, Experimental Brain Research.

[12]  P. Schyns,et al.  A mechanism for impaired fear recognition after amygdala damage , 2005, Nature.

[13]  Caroline Blais,et al.  Recognizing famous people , 2010, Attention, perception & psychophysics.

[14]  D. Fiset,et al.  The dual nature of the human face: there is a little Jekyll and a little Hyde in all of us , 2014, Front. Psychol..

[15]  Katie L McMahon,et al.  The locus of taboo context effects in picture naming , 2017, Quarterly journal of experimental psychology.

[16]  Bruno Rossion,et al.  Acquired prosopagnosia as a face-specific disorder: Ruling out the general visual similarity account , 2010, Neuropsychologia.

[17]  P. Bennett,et al.  Inversion Leads to Quantitative, Not Qualitative, Changes in Face Processing , 2004, Current Biology.

[18]  P. Ekman Pictures of Facial Affect , 1976 .

[19]  J. Vroomen,et al.  Covert Processing of Faces in Prosopagnosia Is Restricted to Facial Expressions: Evidence from Cross-Modal Bias , 2000, Brain and Cognition.

[20]  Raika Pancaroglu,et al.  Seeing the eyes in acquired prosopagnosia , 2016, Cortex.

[21]  Garrison W. Cottrell,et al.  Transmitting and decoding facial expressions of emotion , 2004 .

[22]  D. Fiset,et al.  The eyes are not the window to basic emotions , 2012, Neuropsychologia.

[23]  B. Cumming,et al.  All Pulfrich-like illusions can be explained without joint encoding of motion and disparity. , 2005, Journal of vision.

[24]  Caroline Blais,et al.  Visual information extraction for static and dynamic facial expression of emotions: an eye-tracking experiment , 2010 .

[25]  Bruno Rossion,et al.  Understanding face perception by means of prosopagnosia and neuroimaging. , 2014, Frontiers in bioscience.

[26]  Bruno Rossion,et al.  Does Prosopagnosia Take the Eyes Out of Face Representations? Evidence for a Defect in Representing Diagnostic Facial Information following Brain Damage , 2005, Journal of Cognitive Neuroscience.

[27]  Giuseppe di Pellegrino,et al.  Prosopagnosia and Alexia Without Object Agnosia , 1998, Cortex.

[28]  Bruno Rossion,et al.  Reduced fixation on the upper area of personally familiar faces following acquired prosopagnosia. , 2008, Journal of neuropsychology.

[29]  D. C. Howell,et al.  Comparing an Individual's Test Score Against Norms Derived from Small Samples , 1998 .

[30]  Justin Duncan,et al.  When less is more: Impact of face processing ability on recognition of visually degraded faces. , 2015, Journal of experimental psychology. Human perception and performance.

[31]  Vincent Walsh,et al.  Combined TMS and fMRI Reveal Dissociable Cortical Pathways for Dynamic and Static Face Perception , 2014, Current Biology.

[32]  Elias B. Issa,et al.  Precedence of the Eye Region in Neural Processing of Faces , 2012, The Journal of Neuroscience.

[33]  J. Grafman,et al.  A Case of Prosopagnosia Following Moderate Closed Head Injury with Left Hemisphere Focal Lesion , 2000, Cortex.

[34]  Theodor Landis,et al.  Are Unilateral Right Posterior Cerebral Lesions Sufficient to Cause Prosopagnosia? Clinical and Radiological Findings in Six Additional Patients , 1986, Cortex.

[35]  Oliver G. B. Garrod,et al.  Reconstructing dynamic mental models of facial expressions in prosopagnosia reveals distinct representations for identity and expression , 2015, Cortex.

[36]  David Pitcher,et al.  Facial Expression Recognition Takes Longer in the Posterior Superior Temporal Sulcus than in the Occipital Face Area , 2014, The Journal of Neuroscience.

[37]  Garrison W. Cottrell,et al.  Transmitting and Decoding Facial Expressions , 2005, Psychological science.

[38]  N. Dupuis-Roy,et al.  Uncovering gender discrimination cues in a realistic setting. , 2009, Journal of vision.

[39]  Heather J. Ferguson,et al.  Perceptual and Memorial Contributions to Developmental Prosopagnosia , 2017, Quarterly journal of experimental psychology.

[40]  R. Adolphs,et al.  Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala , 1994, Nature.

[41]  Martin Eimer,et al.  Facial identity and facial expression are initially integrated at visual perceptual stages of face processing , 2016, Neuropsychologia.

[42]  Marie L. Smith,et al.  How task shapes the use of information during facial expression categorizations. , 2014, Emotion.

[43]  A. Damasio,et al.  Face agnosia and the neural substrates of memory. , 1990, Annual review of neuroscience.

[44]  Alexander Todorov,et al.  Reverse Correlating Social Face Perception , 2012 .

[45]  Galit Yovel,et al.  A Revised Neural Framework for Face Processing. , 2015, Annual review of vision science.

[46]  Rachael E. Jack,et al.  Cultural Confusions Show that Facial Expressions Are Not Universal , 2009, Current Biology.

[47]  K. Heilman,et al.  Processing of faces by patients with unilateral hemisphere lesions I. Dissociation between judgments of facial affect and facial identity , 1985, Brain and Cognition.

[48]  Katherine B. Martin,et al.  Facial Action Coding System , 2015 .

[49]  Frédéric Gosselin,et al.  Bubbles: a technique to reveal the use of information in recognition tasks , 2001, Vision Research.

[50]  Lesley K. Fellows,et al.  Eye spy: The predictive value of fixation patterns in detecting subtle and extreme emotions from faces , 2014, Cognition.