Deficits in Long-Term Recognition Memory Reveal Dissociated Subtypes in Congenital Prosopagnosia

The study investigates long-term recognition memory in congenital prosopagnosia (CP), a lifelong impairment in face identification that is present from birth. Previous investigations of processing deficits in CP have mostly relied on short-term recognition tests to estimate the scope and severity of individual deficits. We firstly report on a controlled test of long-term (one year) recognition memory for faces and objects conducted with a large group of participants with CP. Long-term recognition memory is significantly impaired in eight CP participants (CPs). In all but one case, this deficit was selective to faces and didn't extend to intra-class recognition of object stimuli. In a test of famous face recognition, long-term recognition deficits were less pronounced, even after accounting for differences in media consumption between controls and CPs. Secondly, we combined test results on long-term and short-term recognition of faces and objects, and found a large heterogeneity in severity and scope of individual deficits. Analysis of the observed heterogeneity revealed a dissociation of CP into subtypes with a homogeneous phenotypical profile. Thirdly, we found that among CPs self-assessment of real-life difficulties, based on a standardized questionnaire, and experimentally assessed face recognition deficits are strongly correlated. Our results demonstrate that controlled tests of long-term recognition memory are needed to fully assess face recognition deficits in CP. Based on controlled and comprehensive experimental testing, CP can be dissociated into subtypes with a homogeneous phenotypical profile. The CP subtypes identified align with those found in prosopagnosia caused by cortical lesions; they can be interpreted with respect to a hierarchical neural system for face perception.

[1]  Denise C. Park,et al.  Nature versus Nurture in Ventral Visual Cortex: A Functional Magnetic Resonance Imaging Study of Twins , 2007, The Journal of Neuroscience.

[2]  B. de Gelder,et al.  Configural face processes in acquired and developmental prosopagnosia: evidence for two separate face systems? , 2000, Neuroreport.

[3]  Mariya V. Cherkasova,et al.  Covert recognition in acquired and developmental prosopagnosia , 2001, Neurology.

[4]  A. Mazzucchi,et al.  Is Prosopagnosia More Frequent in Males Than in Females? , 1983, Cortex.

[5]  Michael B. Lewis,et al.  Capgras delusion: a window on face recognition , 2001, Trends in Cognitive Sciences.

[6]  K. Nakayama,et al.  Face detection in normal and prosopagnosic individuals. , 2008, Journal of neuropsychology.

[7]  O. Pascalis,et al.  Recognition memory in 3- to 4-day-old human neonates. , 1994, Neuroreport.

[8]  Mariya V. Cherkasova,et al.  Impaired spatial coding within objects but not between objects in prosopagnosia , 2005, Neurology.

[9]  Anne-Lise Giraud,et al.  Voice recognition and cross-modal responses to familiar speakers' voices in prosopagnosia. , 2006, Cerebral cortex.

[10]  M Coltheart,et al.  MODELS OF FACE RECOGNITION AND DELUSIONAL MISIDENTIFICATION: A CRITICAL REVIEW , 2000, Cognitive neuropsychology.

[11]  Galia Avidan,et al.  Structural imaging reveals anatomical alterations in inferotemporal cortex in congenital prosopagnosia. , 2007, Cerebral cortex.

[12]  K. Nakayama,et al.  The Cambridge Face Memory Test: Results for neurologically intact individuals and an investigation of its validity using inverted face stimuli and prosopagnosic participants , 2006, Neuropsychologia.

[13]  J. Keenan,et al.  Lesions of the fusiform face area impair perception of facial configuration in prosopagnosia , 2002, Neurology.

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

[15]  Ingo Kennerknecht,et al.  Prevalence of hereditary prosopagnosia (HPA) in Hong Kong Chinese population , 2008, American journal of medical genetics. Part A.

[16]  A. Thiel,et al.  Neuropsychological and neural correlates of autobiographical deficits in a mother who killed her children , 2008, Neurocase.

[17]  I. Kennerknecht,et al.  Hereditary prosopagnosia (HPA): the first report outside the Caucasian population , 2006, Journal of Human Genetics.

[18]  H. Markowitsch,et al.  Die Entwicklung des Bielefelder Famous Faces Test , 2001 .

[19]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[20]  Maria A. Bobes,et al.  Covert Matching of Unfamiliar Faces in a Case of Prosopagnosia: an ERP Study , 2003, Cortex.

[21]  Robert Tibshirani,et al.  An Introduction to the Bootstrap CHAPMAN & HALL/CRC , 1993 .

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

[23]  E. D. de Haan,et al.  A familial factor in the development of face recognition deficits. , 1999, Journal of clinical and experimental neuropsychology.

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

[25]  Mark H. Johnson,et al.  Developing a brain specialized for face perception: a converging methods approach. , 2002, Developmental psychobiology.

[26]  Irene Daum,et al.  Developmental Prosopagnosia: A Review , 2003, Behavioural neurology.

[27]  H. Wilbrand Ein Fall von Seelenblindheit und Hemianopsie mit Sectionsbefund , 1892, Deutsche Zeitschrift für Nervenheilkunde.

[28]  Glyn W. Humphreys,et al.  BORB: Birmingham Object Recognition Battery , 2017 .

[29]  F. Simion,et al.  Newborns’ face recognition over changes in viewpoint , 2008, Cognition.

[30]  Hans Spinnler,et al.  Covert Person Recognition: its Fadeout in a Case of Temporal Lobe Degeneration , 2003, Cortex.

[31]  David I. Perrett,et al.  Recognition of individual faces and average face prototypes by 1- and 3-month-old infants , 2001 .

[32]  B. Duchaine,et al.  Developmental prosopagnosia with normal configural processing , 2000, Neuroreport.

[33]  Andrea Weidenfeld,et al.  An evaluation of two commonly used tests of unfamiliar face recognition , 2003, Neuropsychologia.

[34]  Rafael Malach,et al.  Detailed Exploration of Face-related Processing in Congenital Prosopagnosia: 2. Functional Neuroimaging Findings , 2005, Journal of Cognitive Neuroscience.

[35]  G. Schwarzer,et al.  Gaze behaviour in hereditary prosopagnosia , 2007, Psychological research.

[36]  Galia Avidan,et al.  Functional MRI Reveals Compromised Neural Integrity of the Face Processing Network in Congenital Prosopagnosia , 2009, Current Biology.

[37]  Jarrod D. Hadfield,et al.  MCMC methods for multi-response generalized linear mixed models , 2010 .

[38]  A. Young,et al.  SIMULATING FACE RECOGNITION: IMPLICATIONS FOR MODELLING COGNITION , 1999 .

[39]  H. Bülthoff,et al.  Face recognition under varying poses: The role of texture and shape , 1996, Vision Research.

[40]  M. Behrmann,et al.  Congenital prosopagnosia: face-blind from birth , 2005, Trends in Cognitive Sciences.

[41]  K. Nakayama,et al.  Prosopagnosia as an impairment to face-specific mechanisms: Elimination of the alternative hypotheses in a developmental case , 2006, Cognitive neuropsychology.

[42]  J. Keenan,et al.  Perception of global facial geometry in the inversion effect and prosopagnosia , 2003, Neuropsychologia.

[43]  P. Garthwaite,et al.  Comparing patients' predicted test scores from a regression equation with their obtained scores: a significance test and point estimate of abnormality with accompanying confidence limits. , 2006, Neuropsychology.

[44]  Max Coltheart,et al.  Training of familiar face recognition and visual scan paths for faces in a child with congenital prosopagnosia , 2008, Cognitive neuropsychology.

[45]  J. Mattingley,et al.  Abnormal fMRI Adaptation to Unfamiliar Faces in a Case of Developmental Prosopamnesia , 2007, Current Biology.

[46]  Tobias Elze FlashDot — A platform independent experiment generator for visual psychophysics , 2009 .

[47]  H. McConachie,et al.  Developmental Prosopagnosia. A Single Case Report , 1976, Cortex.

[48]  Joachim Bodamer,et al.  Die Prosop-Agnosie , 2004, Archiv für Psychiatrie und Nervenkrankheiten.

[49]  Galia Avidan,et al.  Reduced structural connectivity in ventral visual cortex in congenital prosopagnosia , 2009, Nature Neuroscience.

[50]  M. Kenward,et al.  An Introduction to the Bootstrap , 2007 .

[51]  Ingo Kennerknecht,et al.  First report of prevalence of non‐syndromic hereditary prosopagnosia (HPA) , 2006, American journal of medical genetics. Part A.

[52]  J. Jost,et al.  F ¨ Ur Mathematik in Den Naturwissenschaften Leipzig the Early Time Course of Compensatory Face Processing in Congenital Prosopagnosia the Early Time Course of Compensatory Face Processing in Congenital Prosopagnosia , 2022 .

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

[54]  H. Hécaen,et al.  Agnosia for faces (prosopagnosia). , 1962, Archives of neurology.

[55]  A. Young,et al.  Understanding face recognition. , 1986, British journal of psychology.

[56]  H. Lissauer,et al.  Ein Fall von Seelenblindheit nebst einem Beitrage zur Theorie derselben , 1890, Archiv für Psychiatrie und Nervenkrankheiten.

[57]  M. Tarr,et al.  The Fusiform Face Area is Part of a Network that Processes Faces at the Individual Level , 2000, Journal of Cognitive Neuroscience.

[58]  Andrew W. Young,et al.  Quaglino's 1867 Case of Prosopagnosia , 2003, Cortex.

[59]  E K Warrington,et al.  Prosopagnosia: A Face-Specific Disorder , 1993, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[60]  Beatriz Luna,et al.  Visual category-selectivity for faces, places and objects emerges along different developmental trajectories. , 2007, Developmental science.

[61]  Nikolaus Weiskopf,et al.  Voxel-based morphometry reveals reduced grey matter volume in the temporal cortex of developmental prosopagnosics , 2009, Brain : a journal of neurology.

[62]  Hanna Damasio,et al.  Double Dissociation between Overt and Covert Face Recognition , 1995, Journal of Cognitive Neuroscience.

[63]  Galia Avidan,et al.  Detailed Exploration of Face-related Processing in Congenital Prosopagnosia: 1. Behavioral Findings , 2005, Journal of Cognitive Neuroscience.

[64]  Karl Sperling,et al.  Hereditary Prosopagnosia: the First Case Series , 2007, Cortex.

[65]  Raya Ariel,et al.  Congenital Visual Agnosia and Prosopagnosia in a Child: A Case Report , 1996, Cortex.

[66]  J. Faraway Extending the Linear Model with R: Generalized Linear, Mixed Effects and Nonparametric Regression Models , 2005 .

[67]  E. Renzi,et al.  Apperceptive and Associative Forms of Prosopagnosia , 1991, Cortex.

[68]  R. Bauer,et al.  Autonomic recognition of names and faces in prosopagnosia: A neuropsychological application of the guilty knowledge test , 1984, Neuropsychologia.

[69]  Catherine J. Mondloch,et al.  What aspects of face processing are impaired in developmental prosopagnosia? , 2006, Brain and Cognition.

[70]  R. Baayen,et al.  Mixed-effects modeling with crossed random effects for subjects and items , 2008 .

[71]  Claus-Christian Carbon,et al.  Visual mental imagery in congenital prosopagnosia , 2009, Neuroscience Letters.

[72]  C. Elger,et al.  Congenital prosopagnosia: multistage anatomical and functional deficits in face processing circuitry , 2010, Journal of Neurology.

[73]  L. Rapport,et al.  Validation of the Warrington theory of visual processing and the Visual Object and Space Perception Battery. , 1998, Journal of clinical and experimental neuropsychology.

[74]  Keith R. Laws,et al.  Testing for a deficit in single-case studies: Effects of departures from normality , 2006, Neuropsychologia.

[75]  M. Coltheart,et al.  Cognitive heterogeneity in genetically based prosopagnosia: a family study. , 2008, Journal of neuropsychology.

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

[77]  Michael S. C. Thomas,et al.  Are developmental disorders like cases of adult brain damage? Implications from connectionist modelling , 2002, Behavioral and Brain Sciences.

[78]  D. Maurer,et al.  Developmental changes in face processing skills. , 2003, Journal of experimental child psychology.

[79]  G. Verbeke,et al.  Statistical inference in generalized linear mixed models: a review. , 2006, The British journal of mathematical and statistical psychology.

[80]  Markus Lappe,et al.  Impairments of Biological Motion Perception in Congenital Prosopagnosia , 2009, PloS one.

[81]  Giuseppe Iaria,et al.  Disconnection in prosopagnosia and face processing , 2008, Cortex.

[82]  Brad Duchaine,et al.  Dissociations of Face and Object Recognition in Developmental Prosopagnosia , 2005, Journal of Cognitive Neuroscience.

[83]  M. Tarr,et al.  Can Face Recognition Really be Dissociated from Object Recognition? , 1999, Journal of Cognitive Neuroscience.

[84]  B. Duchaine Comment on prevalence of hereditary prosopagnosia (HPA) in Hong Kong Chinese population , 2008, American journal of medical genetics. Part A.

[85]  I. Kennerknecht,et al.  Congenital prosopagnosia--a common hereditary cognitive dysfunction in humans. , 2008, Frontiers in bioscience : a journal and virtual library.

[86]  Rafael Malach,et al.  Face-selective Activation in a Congenital Prosopagnosic Subject , 2003, Journal of Cognitive Neuroscience.

[87]  I. Gauthier,et al.  Visual object understanding , 2004, Nature Reviews Neuroscience.

[88]  Mariya V. Cherkasova,et al.  Face imagery and its relation to perception and covert recognition in prosopagnosia , 2003, Neurology.

[89]  Jarrod Had MCMC Methods for Multi-Response Generalized Linear Mixed Models: The MCMCglmm R Package , 2010 .

[90]  E. Renzi,et al.  Prosopagnosia can be associated with damage confined to the right hemisphere—An MRI and PET study and a review of the literature , 1994, Neuropsychologia.