What is Overt and what is Covert in Congenital Prosopagnosia? REVIEW

Neuropsychol Rev
DOI 10.1007/s11065-012-9223-0
REVIEW
What is Overt and what is Covert in Congenital Prosopagnosia?
Davide Rivolta & Romina Palermo & Laura Schmalzl
Received: 8 August 2012 / Accepted: 7 November 2012
# Springer Science+Business Media New York 2012
Abstract The term covert recognition refers to recognition
without awareness. In the context of face recognition, it refers
to the fact that some individuals show behavioural, electrophysiological or autonomic indices of recognition in the absence of overt, conscious recognition. Originally described in
cases of people that have lost their ability to overtly recognize
faces (acquired prosopagnosia, AP), covert face recognition
has more recently also been described in cases of congenital
prosopagnosia (CP), who never develop typical overt face
recognition skills. The presence of covert processing in a
developmental disorder such as CP is a particularly intriguing
phenomenon, and its investigation is relevant for a variety of
reasons. From a theoretical point of view, it is useful to help
shed light on the cognitive and neural underpinnings of face
D. Rivolta (*)
Department of Neurophysiology, Max Planck Institute for Brain
Research, Deutschordenstraße 46,
60528 Frankfurt am Main, Germany
e-mail: [email protected]
D. Rivolta
Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation
with Max Planck Society, Frankfurt am Main, Germany
D. Rivolta : L. Schmalzl
Department of Cognitive Science, Macquarie University, Sydney,
Australia
D. Rivolta
Slop, Scuola Lombarda di Psicoterapia Cognitiva Neuropsicologica,
Retorbido, Pavia, Italy
R. Palermo
ARC Centre of Excellence in Cognition and its Disorders, and
School of Psychology, University of Western Australia, Crawley,
WA 6009, Australia
L. Schmalzl
Department of Neuroscience, Karolinska Institute, Stockholm,
Sweden
recognition deficits. From a clinical point of view, it has the
potential to aid the design of rehabilitation protocols aimed at
improving face recognition skills in this population. In the
current review we selectively summarize the recent literature
on covert face recognition in CP, highlight its main findings,
and provide a theoretical interpretation for them.
Keywords Face perception . Prosopagnosia . Congenital
prosopagnosia . Covert face recognition
Introduction
The ability to recognize faces rapidly and accurately is crucial
for distinguishing family members, friends and colleagues from
strangers, and consequently for navigating our social environment with a sense of security (Davis et al. 2011; Yardley et al.
2008). Some people lack the ability to recognize identity from
faces, a condition known as prosopagnosia, which can either be
acquired following a brain injury (acquired prosopagnosia-AP),
or developmental in nature, in which case the individuals have
never developed an ability to adequately recognize faces
(known as congenital prosopagnosia-CP, or developmental
prosopagnosia-DP) (e.g., Barton 2008; Behrmann and Avidan
2005; Bodamer 1947; Della Sala and Young 2003; Duchaine
and Nakayama 2006b).
What are the main features of CP? From the behavioural point of view, in some cases of CP, the recognition
deficit is purely selective to faces, with individuals exhibiting no difficulty in visual processing tasks with other
kinds of visual stimuli including the within category discrimination of objects (Duchaine and Nakayama 2005).
The deficit can even be specific to the processing of facial
identity, with a spared ability to recognize other facial
cues such as emotional expressions (Duchaine et al.
2003; Humphreys et al. 2007; Lee et al. 2010; Palermo
Neuropsychol Rev
et al. 2011). In other cases of CP however, the deficit can
extend beyond the face domain and include object recognition (Duchaine et al. 2007; Wilson et al. 2010), general
configural processing (Behrmann et al. 2005), or even the
perception of biological motion (Dobel et al. 2007). Recently, an increasing number of studies has begun to not
only investigate “overt” face recognition in CP (i.e., the
explicit ability to recognize faces), but also “covert” face
recognition (i.e., implicit processing of familiar faces that
individuals claim to not recognize).
Covert Face Recognition in CP
Covert face recognition in CP can be investigated using
behavioural (Avidan and Behrmann 2008; Bate et al. 2009,
2008; Bentin et al. 1999; De Haan et al. 1991; Rivolta et al.
2012, 2010), electrophysiological (Eimer et al. 2012) and
autonomic measures (Jones and Tranel 2001). We will discuss each type of evidence separately.
Behavioural Techniques
Two recent group studies have been conducted to determine
whether covert recognition is present in CP. Avidan and
Behrmann (2008) used a Matching task, in which participants had to judge whether pairs of faces shown sequentially
were of the same person or not. Like controls, the group of
six CPs was quicker and more accurate when the pairs were
familiar rather than unfamiliar people, suggesting that the
familiar famous faces were covertly processed by the visual
system despite not being overtly recognized. It is important
to note that most CPs can overtly recognize at least some
faces. Thus, for investigations aimed at the characterization
of covert face recognition it is crucial to exclude trials
containing faces that were actually overtly recognized from
the analysis. Without this precaution one could potentially
erroneously conclude that covert recognition is present,
when the effect is in fact merely driven by overtly recognized faces. This study attempted to control for overt recognition, but the covert and overt face recognition
assessments were carried out in different sessions held on
different days (with the overt assessment occurring before
the covert one). A limitation of this procedure is that it is
possible that a face that had not been recognized during the
overt face recognition assessment could actually be recognized a few days later during the covert face recognition
assessment, and consequently enhance covert recognition
performance. This is particularly relevant since the face
images adopted for overt and covert face recognition assessment were different images of the same people, and it is
possible that some images were more prototypical (and thus
easier to recognize) than others.
Rivolta et al. (2012a) tried to overcome this potential
pitfall by performing overt and covert recognition assessment on the same day, and by using the exact same images
in both assessments. They used three different behavioural
tasks with a group of 11 CPs. In a Forced choice familiarity
task, participants were asked to select which one of two
simultaneously presented faces (one famous and one nonfamous) was familiar. The group of CPs performed above
chance, indicating that they were implicitly oriented towards
faces of people who they knew. Moreover, self-rated confidence in their choice was unrelated to performance in this
task, indicative of covert but not overt recognition. In a
Forced choice cued task, participants had to indicate which
one of two simultaneously presented faces best matched a
name cue shown at the same time. Once again, the group of
CPs matched the name to the correct face more often than
chance, despite their inability to identify any of the faces
overtly. However, confidence was related to performance on
this task, suggesting that this may not be a pure measure of
covert recognition (see Rivolta et al. 2012a for further discussion). In a Priming task, participants were presented with
a face followed by a name, and simply had to judge whether
the name was that of an actor or a politician. The name (e.g.,
“Tom Cruise”) could be preceded either by the face of the
same person (Tom Cruise’s face), a face of a person belonging to the other category (e.g., Tony Blair’s face) or a
scrambled face. While controls were faster when the name
and face matched than in the other two conditions, this
pattern was not observed in the group of CPs.
Overall, these studies indicate that covert face recognition in CP can be demonstrated with behavioural tasks.
However, they may suffer from some limitations that future
research should carefully take into consideration. For instance: (i) They were carried out with a relatively small
sample size (or even single cases of CP; see Rivolta et al.
2010 and Bate et al. 2008); (ii) Despite adopting many tasks
and performing many comparisons between groups, they
did not always carefully correct for multiple comparisons,
thus potentially increasing the chance of a type I error
(Wagenmakers et al. 2011; Wetzels et al. 2011); (iii) Behavioural tasks do not enable one to monitor actual face recognition on-line, that is it could be the case that a face that was
recognized during the covert recognition assessment is no
longer recognized a few minutes later in the overt recognition assessment, which can again lead to potentially misleading results. This latter issue has been taken into account
in the context of electrophysiological investigations that are
described below.
Electrophysiological Techniques
A recent study by Eimer and colleagues (2012) investigated
covert recognition in a group of 12 CPs using Event Related
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Potentials (ERPs). The main focus of the analysis was on the
N250, a negative component which is larger for faces that
are familiar than those that are unfamiliar (Gosling and
Eimer 2011). Half of the CPs showed an N250 for familiar
faces even though they could not overtly recognize them,
indicating covert recognition. No covert recognition was
seen at the earlier ERP component, the N170, suggesting
its primarily involvement in the perceptual rather than recognition related aspects of face processing (Bentin et al.
2000; Eimer et al. 2012; Rivolta et al. 2012; Rossion et al.
2011). In control participants with typical face recognition
skills the N250 was followed by a P600f, a component
known to be involved in semantic memory (Osternhout
and Holcomb 1993) and hence likely to underlie the retrieval of semantic information for the recognition of a specific
person (Eimer 2000). Interestingly, this pattern (i.e., the
N250 followed by the P600f) was also observed in CPs,
but only for trials in which the face was actually overtly
recognized. This observation suggests that, when present,
overt recognition in CP is reflected by similar physiological
mechanisms as in controls. Overall, these results suggest
that covert recognition in CP occurs as a result of a disconnection between spared identity-specific visual memory
traces and later semantic face processing stages, which in
turn indicates that the activation of stored visual representations of familiar faces alone is not sufficient for conscious
explicit face recognition.
This study has the unquestionable merit of representing
the first investigation of electrophysiological correlates of
covert face recognition in a relatively large group of CPs. It
would be of interest in future studies to not only investigate
a limited number of face-sensitive peaks of interest on
particular electrodes, but to consider the information from
all channels over the entire time course of the recordings,
such as in a non-parametric analysis based on a permutation
of residual approach (Anderson and ter Braak 2003). This is
particularly true if we consider that it is likely that important
information is not only represented in the peaks, but in the
activity around them (Rousselet and Pernet 2011; Rousselet
et al. 2011). In addition, an analysis at the source level could
have been very informative for shedding additional light on
the neural substrate behind covert face recognition in CP.
Future studies would benefit from considering these issues.
single case study of a 5 year old boy, who showed higher
SCRs for personally familiar than unfamiliar faces (Jones
and Tranel 2001). In sum, there is some initial evidence for
physiological indices of covert face recognition in CP, but
future studies involving more comprehensive assessments
with multiple techniques would be of particular relevance to
further our knowledge on the relation between different
forms of covert recognition.
Heterogeneity of Covert Face Recognition in CP
Covert face recognition is not a unitary phenomenon displaying the same features in all CPs. Furthermore, not all CPs
show indices of covert recognition. Eimer and colleagues
(2012) found that only half of the people with CP demonstrated covert recognition. Similarly, some behavioural case studies have also failed to demonstrate covert recognition (Bentin
et al. 1999; De Haan et al. 1991). The extent of overt recognition deficits could be an important factor in whether covert
recognition is evident. For instance, Barton et al. (2001)
reported that individuals with AP or CP with more severe
overt recognition deficits are less likely to show covert recognition. This observation can be linked to the original distinction between “apperceptive” (perceptual) and “associative”
(disconnection) prosopagnosia (De Renzi et al. 1991). The
assumption here is that covert recognition is less likely to
occur in the context of an apperceptive deficit affecting early
stages of face processing than an associative deficit disrupting
face recognition at a later stage related to person identification.
In support of this hypothesis, Eimer et al. (2012) found that
overt face recognition performance as measured by the Cambridge Face Memory Test (CFMT, Duchaine and Nakayama
2006a) was significantly better in CPs who showed a covert
N250 component compared to CPs who did not. Similarly,
Rivolta and colleagues 2012a found a correlation between
overt recognition on a Famous face recognition task and
covert recognition on a Forced choice familiarity task, indicating that the better the individuals’ overt face recognition
skills were, the more likely the individuals were to show
covert recognition. To conclude, covert face recognition is
present in some but not all CPs, and when present it seems
to be related to overt face recognition skills. We will now
focus on the neural features of covert recognition in CP.
Autonomic Responses
Indices of covert face recognition can also be detected by
monitoring one type of autonomic activity such as the
galvanic skin conductance response (SCR). The use of
SCR enables to measure the sweat production in response
to the perception of a variety of emotional stimuli (Tranel
and Damasio 1994). The only study adopting SCRs for the
investigation of covert face recognition in CP to date is a
Neural Aspects of Covert Face Recognition
How can we explain the presence of covert face recognition in
individuals with CP who have never acquired typical face
recognition skills to begin with? To answer this question, it
is important to note that many CPs with a very severe face
recognition deficit (e.g., they are unable to reliably recognize
Neuropsychol Rev
friends and family members and perform very poorly on
formal tests) are nevertheless able to recognize at least some
faces. For instance, in our work recognition rates are approximately 28 % of famous faces. As proposed by some authors,
it can be assumed that this partially spared recognition ability
allows CPs to acquire representations for faces they have a lot
of exposure to (Avidan and Behrmann 2008; Bate et al. 2009,
2008; Bentin et al. 1999; De Haan et al. 1991; Rivolta et al.
2012a, b, 2010). For most faces however the representations
are possibly “degraded”, being good enough to support general access to familiarity and hence covert recognition, but not
specific access to identity and hence overt recognition. The
reasons behind the origin of degraded face representations are
far from clear. It is possible that this is driven by (i) a reduced
numbers of saccades within the eyes-mouth-nose region
(Schmalzl et al. 2008); (ii) weak holistic processing (Avidan
et al. 2011; Palermo et al. 2011) and/or (iii) poor general visual
recognition. For instance, it has never been fully investigated
whether “pure” prosopagnosia or prosopagnosia with also
difficulties in the recognition of, for instance, objects show
differences in their overt and covert behaviour.
What are the neural substrates of covert face recognition?
Face recognition typically activates a “core” network as well as
an “extended” network of brain regions (Haxby et al. 2000).
The core network includes the Occipital Face Area (OFA,
Gauthier et al. 2000) and Fusiform Face Area (FFA, Kanwisher
et al. 1997), which have been proposed to be involved in
structural encoding and the evaluation face familiarity (Ewbank
et al. 2012; Rossion et al. 2003). The extended network
includes the anterior temporal cortex, which appears to be
primarily involved in the coding of semantic and biographical
information (Tsukiura et al. 2008). There is some evidence
however, that the right anterior temporal lobe may also be
involved in evaluating face familiarity, although at a later point
in time with respect to the core areas (Gainotti 2007a, b). The
core and extended face areas are anatomically connected via the
Inferior Longitudinal Fasciculus (ILF), a white matter bundle
which connects the occipital and temporal lobes (Catani and
Thiebaut de Schotten 2008; Fox et al. 2008) (See Fig. 1 for a
schematic depiction of the structural and functional components
of the human face-processing network). While some studies
have shown that the core network can be largely spared in CP
(Avidan and Behrmann 2009; Avidan et al. 2005), there is
evidence for hypofunctionality in the extended network
(Avidan and Behrmann 2009; Furl et al. 2011), possibly reflecting a poor connectivity between the two systems (Thomas et al.
2009). This observation fits well with some of the
reported patterns of covert face recognition in CP. For
example, some CPs perform above chance on behavioural tasks such as Forced choice familiarity and Matching
tasks (which require only a familiarity judgment and
thus rely upon the core network), but not on a Priming
task (which requires access to semantic information and
Fig. 1 Structural and functional components of the face-processing
system. The figure depicts the anatomical location of the Occipital
Face Area (OFA), the Fusiform Face Area (FFA), the Anterior Temporal cortex (AT), as well as the Inferior Longitudinal Fasciculus (ILF,
represented in green). The ILF is a white-matter bundle that anatomically connects OFA, FFA and AT. Adapted with permission from
Catani and Thiebaut de Schotten (2008)
thus relies upon both the core and extended networks)
(Rivolta et al. 2012a).
Overall, despite being speculative in nature, we can predict
that a CP with hypofunctioning core and extended face processing network will fail to show overt as well as covert
recognition; whereas a CP with a typically functioning core
network, but a hypofunctioning extended face processing
network will fail to show overt recognition, but may show
behavioural (i.e., above chance performance on Forced choice
familiarity and Matching tasks) and ERP (i.e., a familiarity
sensitive N250) indices of covert recognition. When it comes
to SCRs, the only very limited available information on CPs
makes it difficult to make any clear anatomical predictions on
which brain structures underlie the responses. In general terms
however, SCRs may be mediated by the amygdala and orbitofrontal cortex (Breen et al. 2000; Tranel and Damasio 1994).
Since SCRs for familiar faces are supposedly also driven by
the emotional valence these stimuli have for a person, it can be
postulated that a lack of SCRs in CP might be correlated with
either diminished activity of these areas which code valence,
or poor connectivity between these areas and other face processing regions. This hypothesis finds support in the AP
literature. For example, Valdes-Sosa and colleagues (2011)
described a patient with AP with damaged fusiformtemporal pathways who showed face-selective activation in
orbitofrontal areas and increased SCRs for familiar faces but
no recognition on a priming task.
Conclusions
In conclusion, the investigation of covert face recognition in
CP is relevant for a variety of reasons. First, it can represent
a more sensitive tool than the traditional assessment of overt
recognition for pinpointing the exact nature of face
Neuropsychol Rev
recognition deficit in different individuals. Second, it has the
potential to shed further light on the exact role of different
components within the human neural face recognition system. Moreover, it allows one to determine which apparently
inaccessible information is still present within the visual
system. This last aspect might be informative for the design
of rehabilitation protocols aimed at improving face recognition skills. In fact, knowing that some information about
face familiarity is still present, albeit not accessible, calls for
the planning of interventions aimed at retrieving it. We can
speculate that a cognitive rehabilitation protocol based on
covert face recognition may focus on training the participants in discriminating between familiar and unfamiliar
faces by using a vast sample of faces presented at different
orientations (e.g., front and three quarter view). This strategy, based on the findings on the Forced choice familiarity
task, would make CPs more confident in everyday life by
potentially increasing the number of familiar faces they can
recognize.
Acknowledgments DR is supported by the Neuronale Koordination
Forschungsschwerpunkt Frankfurt (NeFF), RP is supported by the
ARC Centre of Excellence Grant CE110001021, and LS is supported
by the European Research Council.
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