Both identity and non-identity face perception tasks predict developmental prosopagnosia and face recognition ability.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
19 Mar 2024
19 Mar 2024
Historique:
received:
18
04
2023
accepted:
14
03
2024
medline:
20
3
2024
pubmed:
20
3
2024
entrez:
20
3
2024
Statut:
epublish
Résumé
Developmental prosopagnosia (DP) is characterised by deficits in face identification. However, there is debate about whether these deficits are primarily perceptual, and whether they extend to other face processing tasks (e.g., identifying emotion, age, and gender; detecting faces in scenes). In this study, 30 participants with DP and 75 controls completed a battery of eight tasks assessing four domains of face perception (identity; emotion; age and gender; face detection). The DP group performed worse than the control group on both identity perception tasks, and one task from each other domain. Both identity perception tests uniquely predicted DP/control group membership, and performance on two measures of face memory. These findings suggest that deficits in DP may arise from issues with face perception. Some non-identity tasks also predicted DP/control group membership and face memory, even when face identity perception was accounted for. Gender perception and speed of face detection consistently predicted unique variance in group membership and face memory; several other tasks were only associated with some measures of face recognition ability. These findings indicate that face perception deficits in DP may extend beyond identity perception. However, the associations between tasks may also reflect subtle aspects of task demands or stimuli.
Identifiants
pubmed: 38503841
doi: 10.1038/s41598-024-57176-x
pii: 10.1038/s41598-024-57176-x
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
6626Informations de copyright
© 2024. The Author(s).
Références
Bate, S. & Tree, J. J. The definition and diagnosis of developmental prosopagnosia. Q. J. Exp. Psychol. 70, 193–200 (2017).
doi: 10.1080/17470218.2016.1195414
Corrow, S. L., Dalrymple, K. A. & Barton, J. J. Prosopagnosia: current perspectives. Eye Brain 8, 165–175 (2016).
pubmed: 28539812
pmcid: 5398751
doi: 10.2147/EB.S92838
Susilo, T. & Duchaine, B. Advances in developmental prosopagnosia research. Curr. Opin. Neurobiol. 23, 423–429 (2013).
pubmed: 23391526
doi: 10.1016/j.conb.2012.12.011
Bowles, D. C. et al. Diagnosing prosopagnosia: Effects of ageing, sex, and participant–stimulus ethnic match on the Cambridge Face Memory Test and Cambridge Face Perception Test. Cognit. Neuropsychol. 26, 423–455 (2009).
doi: 10.1080/02643290903343149
Kennerknecht, I. et al. First report of prevalence of non-syndromic hereditary prosopagnosia (HPA). Am. J. Med. Genet. Part A 140A, 1617–1622 (2006).
doi: 10.1002/ajmg.a.31343
DeGutis, J. et al. What is the prevalence of developmental prosopagnosia? An empirical assessment of different diagnostic cutoffs. Cortex https://doi.org/10.1016/j.cortex.2022.12.014 (2023).
doi: 10.1016/j.cortex.2022.12.014
pubmed: 36905701
Bennetts, R. J., Murray, E., Boyce, T. & Bate, S. Prevalence of face recognition deficits in middle childhood. Q. J. Exp. Psychol. 70, 234–258 (2017).
doi: 10.1080/17470218.2016.1167924
Bennetts, R. J. et al. Face specific inversion effects provide evidence for two subtypes of developmental prosopagnosia. Neuropsychologia 174, 108332 (2022).
pubmed: 35839963
doi: 10.1016/j.neuropsychologia.2022.108332
Biotti, F. et al. Normal composite face effects in developmental prosopagnosia. Cortex 95, 63–76 (2017).
pubmed: 28850918
doi: 10.1016/j.cortex.2017.07.018
DeGutis, J., Cohan, S., Mercado, R. J., Wilmer, J. & Nakayama, K. Holistic processing of the mouth but not the eyes in developmental prosopagnosia. Cognit. Neuropsychol. 29, 419–446 (2012).
doi: 10.1080/02643294.2012.754745
Gerlach, C. & Starrfelt, R. Patterns of perceptual performance in developmental prosopagnosia: An in-depth case series. Cognit. Neuropsychol. 38, 27–49 (2021).
doi: 10.1080/02643294.2020.1869709
Geskin, J. & Behrmann, M. Congenital prosopagnosia without object agnosia? A literature review. Cognit. Neuropsychol. 35, 4–54 (2018).
doi: 10.1080/02643294.2017.1392295
Palermo, R. et al. Impaired holistic coding of facial expression and facial identity in congenital prosopagnosia. Neuropsychologia 49, 1226–1235 (2011).
pubmed: 21333662
pmcid: 3083514
doi: 10.1016/j.neuropsychologia.2011.02.021
Biotti, F., Gray, K. L. H. & Cook, R. Is developmental prosopagnosia best characterised as an apperceptive or mnemonic condition?. Neuropsychologia https://doi.org/10.1016/j.neuropsychologia.2018.11.014 (2018).
Bate, S. et al. Objective patterns of face recognition deficits in 165 adults with self-reported developmental prosopagnosia. Brain Sci. 9, 133 (2019).
pubmed: 31174381
pmcid: 6627939
doi: 10.3390/brainsci9060133
Bate, S. & Bennetts, R. The independence of expression and identity in face-processing: evidence from neuropsychological case studies. Front. Psychol. 6, (2015).
Biotti, F. & Cook, R. Impaired perception of facial emotion in developmental prosopagnosia. Cortex 81, 126–136 (2016).
pubmed: 27208814
doi: 10.1016/j.cortex.2016.04.008
Duchaine, B., Parker, H. & Nakayama, K. Normal recognition of emotion in a prosopagnosic. Perception 32, 827–838 (2003).
pubmed: 12974568
doi: 10.1068/p5067
Duchaine, B., Yovel, G., Butterworth, E. J. & Nakayama, K. Prosopagnosia as an impairment to face-specific mechanisms: Elimination of the alternative hypotheses in a developmental case. Cognit. Neuropsychol. 23, 714–747 (2006).
doi: 10.1080/02643290500441296
Humphreys, K., Avidan, G. & Behrmann, M. A detailed investigation of facial expression processing in congenital prosopagnosia as compared to acquired prosopagnosia. Exp. Brain Res. 176, 356–373 (2007).
pubmed: 16917773
doi: 10.1007/s00221-006-0621-5
Nunn, J. A., Postma, P. & Pearson, R. Developmental Prosopagnosia: Should it be taken at face value?. Neurocase 7, 15–27 (2001).
pubmed: 11239073
doi: 10.1093/neucas/7.1.15
Chatterjee, G. & Nakayama, K. Normal facial age and gender perception in developmental prosopagnosia. Cognit. Neuropsychol. 29, 482–502 (2012).
doi: 10.1080/02643294.2012.756809
Esins, J., Schultz, J., Stemper, C., Kennerknecht, I. & Bülthoff, I. Face perception and test reliabilities in congenital prosopagnosia in seven tests. i-Perception 7, 204166951562579 (2016).
Marsh, J. E., Biotti, F., Cook, R. & Gray, K. L. H. The discrimination of facial sex in developmental prosopagnosia. Sci. Rep. 9, 19079 (2019).
pubmed: 31836836
pmcid: 6910918
doi: 10.1038/s41598-019-55569-x
Garrido, L., Duchaine, B. & Nakayama, K. Face detection in normal and prosopagnosic individuals. J. Neuropsychol. 2, 119–140 (2008).
pubmed: 19334308
doi: 10.1348/174866407X246843
Duchaine, B. & Nakayama, K. The Cambridge face memory test: Results for neurologically intact individuals and an investigation of its validity using inverted face stimuli and prosopagnosic participants. Neuropsychologia 44, 576–585 (2006).
pubmed: 16169565
doi: 10.1016/j.neuropsychologia.2005.07.001
Bruce, V. & Young, A. Understanding face recognition. Br. J. Psychol. 77, 305–327 (1986).
pubmed: 3756376
doi: 10.1111/j.2044-8295.1986.tb02199.x
Duchaine, B. & Yovel, G. A revised neural framework for face processing. Annu. Rev. Vis. Sci. 1, 393–416 (2015).
pubmed: 28532371
doi: 10.1146/annurev-vision-082114-035518
Haxby, J. V., Hoffman, E. A. & Gobbini, M. I. The distributed human neural system for face perception. Trends Cognit. Sci. 4, 223–233 (2000).
doi: 10.1016/S1364-6613(00)01482-0
Dalrymple, K. A., Garrido, L. & Duchaine, B. Dissociation between face perception and face memory in adults, but not children, with developmental prosopagnosia. Dev. Cognit. Neurosci. 10, 10–20 (2014).
doi: 10.1016/j.dcn.2014.07.003
Bate, S., Bennetts, R. J., Tree, J. J., Adams, A. & Murray, E. The domain-specificity of face matching impairments in 40 cases of developmental prosopagnosia. Cognition 192, 104031 (2019).
pubmed: 31351346
doi: 10.1016/j.cognition.2019.104031
Murray, E., Bennetts, R., Tree, J. & Bate, S. An update of the benton facial recognition test. Behav. Res. 54, 2318–2333 (2021).
doi: 10.3758/s13428-021-01727-x
Rossion, B. & Michel, C. Normative accuracy and response time data for the computerized Benton Facial Recognition Test (BFRT-c). Behav. Res. 50, 2442–2460 (2018).
doi: 10.3758/s13428-018-1023-x
Burns, E. J., Gaunt, E., Kidane, B., Hunter, L. & Pulford, J. A new approach to diagnosing and researching developmental prosopagnosia: Excluded cases are impaired too. Behav. Res. https://doi.org/10.3758/s13428-022-02017-w (2022).
doi: 10.3758/s13428-022-02017-w
Duchaine, B., Germine, L. & Nakayama, K. Family resemblance: Ten family members with prosopagnosia and within-class object agnosia. Cognit. Neuropsychol. 24, 419–430 (2007).
doi: 10.1080/02643290701380491
Mishra, M. V. et al. Comparing the sensitivity of face matching assessments to detect face perception impairments. Neuropsychologia 163, 108067 (2021).
pubmed: 34673046
pmcid: 9647662
doi: 10.1016/j.neuropsychologia.2021.108067
Campbell, J. & Burke, D. Evidence that identity-dependent and identity-independent neural populations are recruited in the perception of five basic emotional facial expressions. Vis. Res. 49, 1532–1540 (2009).
pubmed: 19303422
doi: 10.1016/j.visres.2009.03.009
Connolly, H. L., Young, A. W. & Lewis, G. J. Recognition of facial expression and identity in part reflects a common ability, independent of general intelligence and visual short-term memory. Cognit. Emot. 33, 1119–1128 (2019).
doi: 10.1080/02699931.2018.1535425
Connolly, H. L., Lefevre, C. E., Young, A. W. & Lewis, G. J. Emotion recognition ability: Evidence for a supramodal factor and its links to social cognition. Cognition 197, 104166 (2020).
pubmed: 31951857
doi: 10.1016/j.cognition.2019.104166
Lander, K. & Butcher, N. Independence of face identity and expression processing: exploring the role of motion. Front. Psychol. 6, (2015).
DeGutis, J., Chatterjee, G., Mercado, R. J. & Nakayama, K. Face gender recognition in developmental prosopagnosia: Evidence for holistic processing and use of configural information. Vis. Cognit. 20, 1242–1253 (2012).
doi: 10.1080/13506285.2012.744788
Le Grand, R. et al. What aspects of face processing are impaired in developmental prosopagnosia?. Brain Cognit. 61, 139–158 (2006).
doi: 10.1016/j.bandc.2005.11.005
Tsao, D. Y. & Livingstone, M. S. Mechanisms of face perception. Annu. Rev. Neurosci. 31, 411–437 (2008).
pubmed: 18558862
pmcid: 2629401
doi: 10.1146/annurev.neuro.30.051606.094238
Omer, Y., Sapir, R., Hatuka, Y. & Yovel, G. What is a face? Critical features for face detection. Perception 48, 437–446 (2019).
pubmed: 30939991
doi: 10.1177/0301006619838734
Ulrich, P. I. N. et al. Perceptual and memorial contributions to developmental prosopagnosia. Q. J. Exp. Psychol. 70, 298–315 (2017).
doi: 10.1080/17470218.2016.1177101
Baron-Cohen, S., Wheelwright, S., Skinner, R., Martin, J. & Clubley, E. The autism-spectrum quotient (AQ): Evidence from asperger syndrome/high-functioning autism, malesand females, scientists and mathematicians. J. Autism Dev. Dis. 31, 5–17 (2001).
doi: 10.1023/A:1005653411471
Holdnack, H. A. Wechsler test of adult reading: WTAR (The Psychological Corporation, 2001).
Folstein, M. F., Folstein, S. E. & McHugh, P. R. “Mini-mental state”: a practical method for grading the cognitive state of patients for the clinician. J. Psychiatric Res. 12, 189–198 (1975).
doi: 10.1016/0022-3956(75)90026-6
Larner, A. J. Mini-Mental Parkinson (MMP) as a dementia screening test: comparison with the Mini-Mental State Examination (MMSE). Curr. Aging Sci. 5, 136–139 (2012).
pubmed: 21834788
doi: 10.2174/1874609811205020136
Humphreys, G. & Riddoch, M. J. Birmingham Object Recognition Battery (Lawrence Erlbaum Associates, 1993).
Rezlescu, C., Pitcher, D. & Duchaine, B. Acquired prosopagnosia with spared within-class object recognition but impaired recognition of degraded basic-level objects. Cognit. Neuropsychol. 29, 325–347 (2012).
doi: 10.1080/02643294.2012.749223
Bobak, A. K., Bennetts, R. J., Parris, B. A., Jansari, A. & Bate, S. An in-depth cognitive examination of individuals with superior face recognition skills. Cortex 82, 48–62 (2016).
pubmed: 27344238
doi: 10.1016/j.cortex.2016.05.003
Macmillan, N. A. & Creelman, C. D. Detection Theory: A User’s Guide (Lawrence Erlbaum Associates Publishers, 2005).
Young, A., Perrett, D. I., Calder, A., Sprengelmeyer, R. H. & Ekman, P. Facial expressions of emotion: Stimuli and Test (FEEST). (2002).
Baron-Cohen, S., Wheelwright, S., Hill, J., Raste, Y. & Plumb, I. The, “Reading the Mind in the Eyes” Test revised version: a study with normal adults, and adults with Asperger syndrome or high-functioning autism. J. Child Psychol. Psychiatry Allied Discip. 42, 241–251 (2001).
doi: 10.1111/1469-7610.00715
Oakley, B. F. M., Brewer, R., Bird, G. & Catmur, C. Theory of mind is not theory of emotion: A cautionary note on the Reading the Mind in the Eyes Test. J. Abnorm. Psychol. 125, 818–823 (2016).
pubmed: 27505409
pmcid: 4976760
doi: 10.1037/abn0000182
Thomas, A. L., Lawler, K., Olson, I. R. & Aguirre, G. K. The Philadelphia face perception battery. Arch. Clin. Neuropsychol. 23, 175–187 (2008).
pubmed: 18082362
doi: 10.1016/j.acn.2007.10.003
Behrmann, M., Avidan, G., Marotta, J. J. & Kimchi, R. Detailed exploration of face-related processing in congenital prosopagnosia: 1. Behavioral findings. J. Cognit. Neurosci. 17, 1130–1149 (2005).
doi: 10.1162/0898929054475154
O’Toole, A. J., Deffenbacher, K. A., Valentin, D. & Abdi, H. Low-dimensional representation of faces in higher dimensions of the face space. J. Opt. Soc. Am. A 10, 405 (1993).
doi: 10.1364/JOSAA.10.000405
Jones, R. D. & Tranel, D. Severe developmental prosopagnosia in a child with superior intellect. J. Clin. Exp. Neuropsychol. 23, 265–273 (2001).
pubmed: 11404805
doi: 10.1076/jcen.23.3.265.1183
Pond, S. et al. Aftereffects support opponent coding of face gender. J. Vis. 13, 16–16 (2013).
pubmed: 24361588
doi: 10.1167/13.14.16
Rhodes, G. et al. Sex-specific norms code face identity. J. Vis. 11, 1–1 (2011).
pubmed: 21199895
doi: 10.1167/11.1.1
Palermo, R., Rivolta, D., Wilson, C. E. & Jeffery, L. Adaptive face space coding in congenital prosopagnosia: Typical figural aftereffects but abnormal identity aftereffects. Neuropsychologia 49, 3801–3812 (2011).
pubmed: 21986295
doi: 10.1016/j.neuropsychologia.2011.09.039
Crookes, K. et al. How well do computer-generated faces tap face expertise?. PLoS ONE 10, e0141353 (2015).
pubmed: 26535910
pmcid: 4633121
doi: 10.1371/journal.pone.0141353
Miller, E. J., Foo, Y. Z., Mewton, P. & Dawel, A. How do people respond to computer-generated versus human faces? A systematic review and meta-analyses. Comput. Human Behav. Rep. 10, 100283 (2023).
doi: 10.1016/j.chbr.2023.100283