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Congenital Prosopagnosia Without Object Agnosia? a Literature Review

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Congenital Prosopagnosia Without Object Agnosia? a Literature Review Cognitive Neuropsychology ISSN: 0264-3294 (Print) 1464-0627 (Online) Journal homepage: http://www.tandfonline.com/loi/pcgn20 Congenital prosopagnosia without object agnosia? A literature review Jacob Geskin & Marlene Behrmann To cite this article: Jacob Geskin & Marlene Behrmann (2017): Congenital prosopagnosia without object agnosia? A literature review, Cognitive Neuropsychology, DOI: 10.1080/02643294.2017.1392295 To link to this article: https://doi.org/10.1080/02643294.2017.1392295 View supplementary material Published online: 22 Nov 2017. Submit your article to this journal Article views: 7 View related articles View Crossmark data Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=pcgn20 Download by: [Carnegie Mellon University] Date: 28 November 2017, At: 13:35 COGNITIVE NEUROPSYCHOLOGY, 2017 https://doi.org/10.1080/02643294.2017.1392295 Congenital prosopagnosia without object agnosia? A literature review Jacob Geskin and Marlene Behrmann Department of Psychology and Center for the Neural Basis of Cognition, Carnegie Mellon University, Pittsburgh, PA, USA ABSTRACT ARTICLE HISTORY A longstanding controversy concerns the functional organization of high-level vision, and the Received 16 January 2017 extent to which the recognition of different classes of visual stimuli engages a single system or Revised 3 October 2017 multiple independent systems. We examine this in the context of congenital prosopagnosia (CP), Accepted 6 October 2017 a neurodevelopmental disorder in which individuals, without a history of brain damage, are KEYWORDS impaired at face recognition. This paper reviews all CP cases from 1976 to 2016, and explores domain specificity; face the evidence for the association or dissociation of face and object recognition. Of the 238 CP recognition; modularity; cases with data permitting a satisfactory evaluation, 80.3% evinced an association between object recognition; impaired face and object recognition whereas 19.7% evinced a dissociation. We evaluate the prosopagnosia strength of the evidence and correlate the face and object recognition behaviour. We consider the implications for theories of functional organization of the visual system, and offer suggestions for further adjudication of the relationship between face and object recognition. One of the longstanding controversies in the neurop- perhaps interleaved with other subclusters mediating sychology literature concerns the functional organiz- other classes of input, as evident from high-resolution ation of high-level vision, and the extent to which functional imaging studies (e.g., McGugin, Gatenby, the recognition of different classes of visual stimuli Gore, & Gauthier, 2012a). (for example, faces, words, and common objects) This domain-specific versus domain-general con- engages a single domain-general mechanism or mul- troversy has played out in almost all domains of cog- tiple, independent underlying psychological and nitive neuroscience, oftentimes with vigorous debate neural mechanisms. The distributed view of cortical (Gauthier, 2017a; Kanwisher, 2017), and many investi- function suggests that object discrimination depends gations have addressed this issue using neuroimaging on dispersed regions spread across visual cortex, (e.g., Gauthier, Skudlarski, Gore, & Anderson, 2000; Tarr some of which may support the recognition of more & Gauthier, 2000; Yovel & Kanwisher, 2004), electro- than one stimulus class (e.g., Behrmann & Plaut, physiological measures (e.g., Allison, McCarthy, 2015; Haxby et al., 2001;O’Toole, Jiang, Abdi, & Nobre, Puce, & Belger, 1994; Carmel & Bentin, 2002), Haxby, 2005; Robinson, Plaut, & Behrmann, 2017). In imaging studies in non-human primates (e.g., Arcaro contrast, the more modular account proposes that & Livingstone, 2017; Chang & Tsao, 2017; Landi & Frei- Downloaded by [Carnegie Mellon University] at 13:35 28 November 2017 different categories of objects are represented in wald, 2017), and investigations of neuropsychological and processed by functionally distinct cortical cases. Full coverage of this debate is beyond the scope regions (e.g., Kanwisher, 2017; McKone, Crookes, of this review but many comprehensive papers are Jeffery, & Dilks, 2012; McKone & Kanwisher, 2005). Of available (Grill-Spector & Weiner, 2014; Kravitz, course, there are also various alternatives that fall in Saleem, Baker, Ungerleider, & Mishkin, 2013). between these extreme positions—for example, it is With respect to neuropsychological investigations, possible that the organization is one in which subclus- this topic has received especially pointed attention in ters of visual classes are subserved by the same under- discussions of acquired prosopagnosia (AP), an impair- lying mechanism (for example, configural processing) ment of face recognition in premorbidly normal indi- or is one in which inputs from a single visual class are viduals following a brain lesion, with the critical processed by a small cluster of adjacent regions question being whether this disorder is limited to the CONTACT Marlene Behrmann [email protected] © 2017 Informa UK Limited, trading as Taylor & Francis Group 2 J. GESKIN AND M. BEHRMANN recognition of faces or is, instead, more general, affect- damage or any other obvious neurological disorder ing the recognition of other non-face visual classes as (for recent reviews of this disorder, see Barton & well. On the one hand, many investigations of AP Corrow, 2016a; Cook & Biotti, 2016; Grill-Spector, have argued for domain specificity in which the impair- Weiner, Kay, & Gomez, 2017). ment is restricted to the perception of faces (Barton, Some authors use the term “developmental proso- 2008; Busigny & Rossion, 2010; Riddoch, Johnston, Bra- pagnosia” (DP) to refer to these cases but because cewell, Boutsen, & Humphreys, 2008), and 27 cases of some of the reported DP cases do have brain prosopagnosia without an accompanying deficit in damage, we have opted for the term CP instead. object recognition (object agnosia) are listed in the lit- However, we do use DP as an abbreviation in the erature review by Farah (1991). On the other hand, the text or appendices if other authors have used that des- results of many studies favour a more domain-general ignation to refer to their participants. Also, because, in explanation for the prosopagnosia deficit and have the majority of cases, we cannot confirm the heredi- reported an impairment not only for face recognition tary nature of the deficit (which is usually labelled as but for the recognition of other stimuli, as well (e.g., “hereditary prosopagnosia”; HP), we opt for CP rather Bukach, Bub, Gauthier, & Tarr, 2006; Gauthier, Behr- than HP, as CP is agnostic with respect to an explicit mann, & Tarr, 1999; for recent review, see Barton & hereditary component (for papers on heritability of Corrow, 2016b) and 37 cases of prosopagnosia with face perception, see Shakeshaft & Plomin, 2015; an additional recognition deficit are identified in the Wilmer et al., 2010; Zhu et al., 2010). review by Farah (1991). Whereas the former finding of The aim of the current paper, then, is to provide a domain-specificity is more compatible with the brain survey of the existing literature on CP to elucidate being organized into modules, each with a circum- the nature of the relationship between impairments scribed function as proposed by, for example, Fodor in face and non-face object recognition and, in so (1983) or Lenneberg (1967), the latter is more sugges- doing, to characterize the functional architecture of tive of an organization that may be contingent on a visual recognition. In addition to addressing this scien- more general mechanism, such as the sensitivity to cur- tific question, we also evaluate the methodological vature (Nasr, Echavarria, & Tootell, 2014; Ponce, Hart- approach to data collection in such individuals, carry mann, & Livingstone, 2017) or spatial frequency out a meta-analysis of the findings, and offer some (Woodhead, Wise, Sereno, & Leech, 2011) or the suggestions that might allow for a more directed reliance on holistic processing (Richler, Palmeri, & Gau- approach to testing the hypotheses. We start by pro- thier, 2012). Understanding the functional organization viding some context from neuropsychology and iden- of the visual system is critical from a theoretical point of tifying methodological challenges to the survey view but also from a translational perspective in that a approach, before presenting the method and findings precise characterization of the deficits and their under- of our investigation. lying mechanism may be of value in customizing reha- bilitation approaches for those with visuoperceptual The Farah approach Downloaded by [Carnegie Mellon University] at 13:35 28 November 2017 disorders (e.g., Woodhead et al., 2013). In an effort to shed further light on the question of As noted above, neuropsychological investigations structure–function relations in high-level vision, the have explored the association or dissociation current paper examines the visual recognition behav- between the recognition of different classes of visual iour of individuals with congenital prosopagnosia, a stimuli. For example, the relationship between the rec- disorder that, although recognized several decades ognition of faces versus other visual stimuli such as ago (e.g., Temple, 1992), is currently receiving con- objects and words has been assessed in several siderable scientific attention. Congenital prosopagno-
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