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The Cognitive and Neural Basis of Developmental Prosopagnosia

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The Cognitive and Neural Basis of Developmental Prosopagnosia The Quarterly Journal of Experimental Psychology ISSN: 1747-0218 (Print) 1747-0226 (Online) Journal homepage: http://www.tandfonline.com/loi/pqje20 The cognitive and neural basis of developmental prosopagnosia John Towler, Katie Fisher & Martin Eimer To cite this article: John Towler, Katie Fisher & Martin Eimer (2017) The cognitive and neural basis of developmental prosopagnosia, The Quarterly Journal of Experimental Psychology, 70:2, 316-344, DOI: 10.1080/17470218.2016.1165263 To link to this article: http://dx.doi.org/10.1080/17470218.2016.1165263 Accepted author version posted online: 11 Mar 2016. Published online: 27 Apr 2016. Submit your article to this journal Article views: 163 View related articles View Crossmark data Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=pqje20 Download by: [Birkbeck College] Date: 15 November 2016, At: 07:22 THE QUARTERLY JOURNAL OF EXPERIMENTAL PSYCHOLOGY, 2017 VOL. 70, NO. 2, 316–344 http://dx.doi.org/10.1080/17470218.2016.1165263 The cognitive and neural basis of developmental prosopagnosia John Towler, Katie Fisher and Martin Eimer Department of Psychological Sciences, Birkbeck College, University of London, London, UK ABSTRACT ARTICLE HISTORY Developmental prosopagnosia (DP) is a severe impairment of visual face recognition Received 28 July 2015 in the absence of any apparent brain damage. The factors responsible for DP have not Accepted 1 February 2016 yet been fully identified. This article provides a selective review of recent studies First Published Online 27 investigating cognitive and neural processes that may contribute to the face April 2016 fi recognition de cits in DP, focusing primarily on event-related brain potential (ERP) KEYWORDS measures of face perception and recognition. Studies that measured the face- Prosopagnosia; sensitive N170 component as a marker of perceptual face processing have shown Developmental; N170; Event- that the perceptual discrimination between faces and non-face objects is intact in related brain potential; Face DP. Other N170 studies suggest that faces are not represented in the typical recognition; Face perception fashion in DP. Individuals with DP appear to have specific difficulties in processing spatial and contrast deviations from canonical upright visual–perceptual face templates. The rapid detection of emotional facial expressions appears to be unaffected in DP. ERP studies of the activation of visual memory for individual faces and of the explicit identification of particular individuals have revealed differences between DPs and controls in the timing of these processes and in the links between visual face memory and explicit face recognition. These observations suggest that the speed and efficiency of information propagation through the cortical face network is altered in DP. The nature of the perceptual impairments in DP suggests that atypical visual experience with the eye region of faces over development may be an important contributing factor to DP. Prosopagnosia is a severe deficit of visual face recog- typically report first experiencing face recognition pro- nition in the absence of low-level visual problems and blems in childhood or adolescence (for recent reviews, intellectual disability. Individuals who have this con- see: Susilo & Duchaine, 2013; Towler & Eimer, 2012). dition may also experience difficulties in interpreting Individuals with DP often become most acutely other aspects of faces, such as expressions of aware of their face recognition difficulties because of emotion, or may even show more general deficits in the increased social demands during adulthood. Due object recognition, but the core impairment in proso- to the increasing public awareness of DP, they are pagnosia concerns the recognition of individual faces. now able to get in contact with psychologists and Traditionally, prosopagnosia was regarded as a rela- neuroscientists who are investigating the condition. tively rare consequence of acquired head injury or There are currently no officially established diag- stroke (Bodamer, 1947). However, another type of pro- nostic criteria for DP. However, particular standards sopagnosia of a developmental origin that emerges are generally present in the research literature. DPs over the lifespan, and in the absence of any apparent must experience face recognition difficulties on a brain damage, has recently been found to be much regular basis in typical situations where recognition more common than prosopagnosia resulting from is unproblematic for individuals without face proces- brain damage (acquired prosopagnosia; AP). These sing impairments. Face memory in DP is typically individuals with developmental prosopagnosia (DP) measured using a combination of tests involving CONTACT John Towler [email protected] Department of Psychological Sciences, Birkbeck College, University of London, Malet Street, London WC1E 7HX, UK © 2016 The Experimental Psychology Society THE QUARTERLY JOURNAL OF EXPERIMENTAL PSYCHOLOGY 317 unfamiliar face learning and long-term memory for responsible for the persistent face recognition difficul- familiar faces. Typical diagnostic criteria are that ties in DP. DPs must score below two standard deviations In the current article, we present a selective review from the mean on a number of different face recog- of cognitive and neuroscientific research on face pro- nition tests. The majority of published research on cessing in individuals with unimpaired face recog- DP has employed the Cambridge Face Memory nition abilities and in individuals with DP. This Test (CFMT; Duchaine & Nakayama, 2006)asan review is selective because it focuses on recent important diagnostic tool. This test involves learning studies from our own lab that have employed event- six unfamiliar male faces from different images that related brain potential (ERP) markers of different show the same individual face from different view- stages of face processing to investigate specific points, under different lighting conditions, and with impairments of face perception and recognition in varying degrees of visual noise. DPs can have DP. The results from these studies are discussed in trouble with remembering identical images of unfa- the context of other research on the cognitive and miliar faces over short durations and with interleaved neural basis of DP, and are also linked to general items; however, impairments are generally more assumptions about the architecture of the face proces- fi marked when identi cation involves changes in the sing system in the human brain. We start with a brief image between sample and test. DP, as assessed overview of the cognitive and neural architecture of by the CFMT, can therefore be described as an the face processing system in individuals without impairment in learning new face identities across face processing impairments, which is important to transformations in the retinal image from which understand the nature of the face processing deficits they were originally encountered. Because face learn- in DP. In the subsequent sections, we review ERP ing and face recognition both depend on the ability studies of perceptual stages of face processing in to perceptually process face images, performance DPs and unimpaired control participants. These deficits measured with the CFMT could also reflect studies have used the face-sensitive N170 component perceptual face processing impairments. Some DPs to study the neural processes involved in the detec- do indeed perform poorly in tests of face perception tion of faces versus non-face objects, as well as differ- such as simultaneous face matching that are less ent aspects of configural face processing, and the dependent on memory, demonstrating that pro- importance of the eye region in early perceptual blems in perceptual aspects of face processing can face representations. Results show that although the contribute to DP. However, other DPs show no basic ability to detect face images and discriminate such impairments in face perception tests (e.g., faces from other types of objects appears intact in Garrido, Duchaine, & Nakayama, 2008). Estimates of the prevalence of developmental pro- DP, there are systematic differences between DPs fi sopagnosia (DP) range from 1.9% to 2.5% in different and control participants in the perceptual con gural populations (Kennerknecht et al., 2006; Kennerknecht, analysis of faces and the weight given to perceptual Pluempe, & Welling, 2008), and both family and twin representation of the eye region. Next, we provide evi- studies suggest strong genetic heritability for the dence that the rapid detection of emotional facial capacity to recognize faces across the entire distri- expression appears to be unimpaired in DP, which bution of this ability (Duchaine, Germine, & Nakayama, illustrates that there are important dissociations 2007; Lee, Duchaine, Wilson, & Nakayama, 2010; between aspects of face perception that are intact Wilmer et al., 2010; Zhu et al., 2010). DP has only and others that are selectively impaired in DP. In the recently become the focus of systematic research, subsequent section, we review recent ERP evidence and the neurodevelopmental origins of DP are cur- that compared processes that are directly involved rently unknown. Investigations into the cognitive in face recognition (such as the activation of visual and neural mechanisms responsible for face recog- face memories and the explicit recognition of particu- nition impairments in DP have
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