Elsevier

Cortex

Volume 81, August 2016, Pages 126-136
Cortex

Research report
Impaired perception of facial emotion in developmental prosopagnosia

https://doi.org/10.1016/j.cortex.2016.04.008Get rights and content

Abstract

Developmental prosopagnosia (DP) is a neurodevelopmental condition characterised by difficulties recognising faces. Despite severe difficulties recognising facial identity, expression recognition is typically thought to be intact in DP; case studies have described individuals who are able to correctly label photographic displays of facial emotion, and no group differences have been reported. This pattern of deficits suggests a locus of impairment relatively late in the face processing stream, after the divergence of expression and identity analysis pathways. To date, however, there has been little attempt to investigate emotion recognition systematically in a large sample of developmental prosopagnosics using sensitive tests. In the present study, we describe three complementary experiments that examine emotion recognition in a sample of 17 developmental prosopagnosics. In Experiment 1, we investigated observers' ability to make binary classifications of whole-face expression stimuli drawn from morph continua. In Experiment 2, observers judged facial emotion using only the eye-region (the rest of the face was occluded). Analyses of both experiments revealed diminished ability to classify facial expressions in our sample of developmental prosopagnosics, relative to typical observers. Imprecise expression categorisation was particularly evident in those individuals exhibiting apperceptive profiles, associated with problems encoding facial shape accurately. Having split the sample of prosopagnosics into apperceptive and non-apperceptive subgroups, only the apperceptive prosopagnosics were impaired relative to typical observers. In our third experiment, we examined the ability of observers' to classify the emotion present within segments of vocal affect. Despite difficulties judging facial emotion, the prosopagnosics exhibited excellent recognition of vocal affect. Contrary to the prevailing view, our results suggest that many prosopagnosics do experience difficulties classifying expressions, particularly those with apperceptive profiles. These individuals may have difficulties forming view-invariant structural descriptions at an early stage in the face processing stream, before identity and expression pathways diverge.

Introduction

Developmental prosopagnosia1 (DP) is a lifelong neurodevelopmental disorder associated with impaired face recognition, thought to affect as many as one in every 50 people (Kennerknecht et al., 2008, Kennerknecht et al., 2006). Individuals with DP exhibit deficits recognising personally familiar faces as well as problems discriminating unfamiliar faces, despite normal intelligence, typical low-level vision, and an absence of manifest brain injury (Behrmann and Avidan, 2005, Duchaine and Nakayama, 2006a, Duchaine and Nakayama, 2006b, Susilo and Duchaine, 2013). Due to characteristic problems with face recognition, individuals with DP often utilise cues derived from hairstyle, voice, and gait, for person recognition. Nevertheless, recognising familiar people encountered out of context or following changes in external appearance, can prove challenging (Shah, Gaule, Sowden, Bird, & Cook, 2015).

The precise origin of the face recognition deficits seen in DP remains unclear. Cognitive accounts have argued that, relative to typically developing (TD) individuals, DPs exhibit reduced holistic processing of faces – whereby individual features (eyes, nose, mouth) are integrated into a coherent unified whole – compromising the accuracy and efficiency of their face recognition (Avidan et al., 2011, Liu and Behrmann, 2014, Palermo et al., 2011). At the neurological level, differences in cortical structure (Behrmann et al., 2007, Garrido et al., 2009, Garrido et al., 2009), structural (Gomez et al., 2015, Thomas et al., 2009) and functional connectivity (Avidan and Behrmann, 2009, Avidan et al., 2013) have been observed in inferotemporal regions including the fusiform gyrus, a region thought to be crucial for face processing (Kanwisher, 2000). Strikingly, DP often runs in families (Duchaine et al., 2007, Johnen et al., 2014, Lee et al., 2010, Schmalzl et al., 2008), suggestive of a genetic component.

The characteristic deficits of facial identity recognition seen in DP have attracted substantial research attention (Susilo & Duchaine, 2013). However, there has also been considerable interest in the expression recognition abilities of individuals with DP. The facial expressions of others are a rich source of social information, conveying cues to affective and mental states (Adolphs, 2002, Frith, 2009, Parkinson, 2005). The ability to interpret facial expressions correctly is therefore important for fluent social interaction and wider socio-cognitive development. Moreover, the question of emotion recognition in DP also has important implications for neurocognitive accounts of the condition (Bate and Bennetts, 2015, Kress and Daum, 2003a). Where observed together, difficulties recognising facial identity and facial emotion are suggestive of apperceptive prosopagnosia (De Renzi, Faglioni, Grossi, & Nichelli, 1991); difficulties may arise early on in the face processing stream, leaving observers unable to form an accurate, view-invariant description of face shape (Bruce and Young, 1986, Haxby et al., 2000). Alternatively, intact expression recognition despite impaired recognition of facial identity suggests a locus of impairment relatively late in the face processing stream, after the divergence of expression and identity analysis pathways (Bruce and Young, 1986, Duchaine et al., 2003, Haxby et al., 2000).

Presently, difficulties recognising facial expressions are thought to be relatively uncommon in DP. Palermo et al. (2011) examined the performance of twelve DPs on three emotion recognition tests: The Ekman 60 Faces Test, in which participants label 60 greyscale images of prototypical basic emotions (Young, Perrett, Calder, Sprengelmeyer, & Ekman, 2002); The Emotion Hexagon Test, in which participants label expressions drawn from morph continua constructed from the six basic emotions2 (Young et al., 2002); and The Reading the Mind in the Eyes Test, in which participants identify subtle social emotions from cues present around the eye region (Baron-Cohen, Wheelwright, Hill, Raste, & Plumb, 2001). Strikingly, the twelve DPs were unimpaired at both the group and single-case level, relative to aged-matched controls, on all three tasks (Palermo et al., 2011). Dobel, Bölte, Aicher, and Schweinberger (2007) described intact emotion recognition in six DPs, having administered the Tübingen Affect Battery – a 4 alternative-forced-choice (AFC) emotion labelling task. Similar findings were reported by Humphreys, Avidan, and Behrmann (2007), having administered The Emotion Hexagon Test to three DPs,2 and Lee, et al. (2010), having tested three DPs using The Reading the Mind in the Eyes Test and a 3AFC match-to-sample task. Several further studies of single cases have described intact emotion recognition in DP (Bentin et al., 2007, Duchaine et al., 2003, Kress and Daum, 2003b, Nunn et al., 2001). Moreover, a study of four DPs indicated that they made typical judgements of facial trustworthiness (Todorov & Duchaine, 2008), an inference thought to be mediated by subtle emotion cues.

Nevertheless, many DPs report problems recognising facial expressions in their daily lives (e.g., Lee et al., 2010), and case studies have described individuals with DP, who do exhibit deficits of expression recognition (Ariel and Sadeh, 1996, De Haan and Campbell, 1991, Duchaine et al., 2009, Duchaine et al., 2006, Minnebusch et al., 2007, Schmalzl et al., 2008). For example, Duchaine et al. (2006) described a 53-year-old male DP, Edward, who exhibited clear expression recognition impairments on The Reading the Mind in the Eyes Test and on a 3-AFC match-to-sample task. Similarly, De Haan and Campbell (1991) tested AB, the original case of DP first described by McConachie (1976), and found that as an adult she exhibited problems labelling prototypical basic emotions. Importantly, however, these reports are relatively infrequent (regarded as ‘the exception’ rather than ‘the norm’), and no systematic investigation has found evidence for a group difference.

The present study sought to re-examine the expression recognition abilities of individuals with DP. As discussed above, this question offers critical insight into the locus of the perceptual difficulties seen in this condition. In particular, we sought to test systematically a large sample of DPs using sensitive tests. The ability of different tests to detect emotion recognition deficits varies widely. For example, Edward, the DP described by Duchaine et al. (2006), was substantially impaired on The Reading the Mind in the Eyes Test (4.1 standard deviations below the TD mean), but only mildly impaired on The Emotion Hexagon Test (1.4 standard deviations below the TD mean). In Experiment 1, we investigated observers' ability to make binary classifications of whole-face expression stimuli drawn from morph continua. In Experiment 2 observers judged facial emotion using only the eye-region (the rest of the face was occluded). In our third experiment, we examined the ability of observers' to classify the emotion present within segments of vocal affect.

Section snippets

Neuropsychological testing

A group of 17 (11 females) individuals with DP participated in the study (Table 1). DP participants were recruited through www.troublewithfaces.org. All members of the DP sample described lifelong face recognition problems. None of the DPs had a history of brain injury or psychiatric disorder (e.g., Schizophrenia, Autism Spectrum Disorder). Convergent diagnostic evidence for the presence of DP was collected using the Cambridge Face Memory Test (CFMT; Duchaine & Nakayama, 2006a), the Cambridge

Experiment 1

Measuring individual differences in expression recognition ability is not straight-forward. In particular, tasks that require participants to label prototypical emotional expressions (e.g., happy, sadness, fear, disgust, anger, surprise) may lack sensitivity due to ceiling effects or noise introduced by differences in guessing base-rates (Ipser & Cook, 2015). In our first experiment we sought to determine whether DPs are impaired at making binary categorisations of whole-face emotional

Experiment 2

The results of Experiment 1 suggest that relative to TD controls, individuals with DP are less able to categorise whole-face expression stimuli drawn from continua that morph emotional facial expressions. While our analyses suggest a trend for less precise categorisation overall, difficulties were particularly clear when observers were required to detect the subtle physical differences between stimuli drawn from the fear-surprise continuum. At least two accounts may be advanced to explain the

Experiment 3

The results of the first two experiments indicate that DP individuals are less able to categorise ambiguous facial expressions than TD controls. In Experiment 3 we sought to determine whether this affect recognition deficit was specific to faces, or whether these difficulties extend to other domains. Crucially, aberrant limbic functionality may leave observers unable to interpret emotion per se (Calder & Young, 2005). For example, individuals with developmental alexithymia – a

Discussion

Despite severe difficulties recognising facial identity, emotion recognition deficits are thought to be relatively uncommon in DP (Bate and Bennetts, 2015, Humphreys et al., 2007, Palermo et al., 2011). Contrary to this view, however, we find evidence for widespread deficits in this population. In Experiment 1 we tested observers' ability to make binary classifications of whole-face expression stimuli drawn from morph continua. Psychophysical analyses revealed diminished ability to classify

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