Getting lost: Topographic skills in acquired and developmental prosopagnosia
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Getting lost: Topographic skills in acquired and
developmental prosopagnosia
Jeffrey C. Co
ow a,1, She
yse L. Co
ow a,1, Edison Lee a,b,
Raika Pancaroglu a, Ford Burles d, Brad Duchaine c, Giuseppe Iaria d and
Jason J.S. Barton a,*
a Human Vision and Eye Movement Laboratory, Departments of Medicine (Neurology), Ophthalmology and Visual
Science, University of British Columbia, Vancouver, Canada
College of Osteopathic Medicine, University of New England, Biddeford, USA
c Department of Psychology, Dartmouth University, Dartmouth, USA
d NeuroLab, Department of Psychology, Hotchkiss Brain Institute, and Alberta Children's Hospital Research Institute,
University of Calgary, Calgary, Canada
a r t i c l e i n f o
Article history:
Received 9 September 2015
Reviewed 4 November 2015
Revised 9 November 2015
Accepted 6 January 2016
Action editor Stefan Schweinberge
Published online 22 January 2016
Keywords:
Navigation
Face recognition
Landmark
Places
Orientation
* Co
esponding author. Neuro-ophthalmolo
3N9, Canada.
E-mail address: XXXXXXXXXX (J.J
1 These authors contributed equally.
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a b s t r a c t
Previous studies report that acquired prosopagnosia is frequently associated with topo-
graphic disorientation. Whether this is associated with a specific anatomic subtype of
prosopagnosia, how frequently it is seen with the developmental variant, and what specific
topographic function is impaired to account for this problem are not known.
We studied ten subjects with acquired prosopagnosia from either occipitotemporal o
anterior temporal (AT) lesions and seven with developmental prosopagnosia. Subjects
were given a battery of topographic tests, including house and scene recognition, the road
map test, a test of cognitive map formation, and a standardized self-report questionnaire.
House and/or scene recognition were frequently impaired after either occipitotemporal
or AT lesions in acquired prosopagnosia. Subjects with occipitotemporal lesions were also
impaired in cognitive map formation: an overlap analysis identified right fusiform and
parahippocampal gyri as a likely co
elate. Only one subject with acquired prosopagnosia
had mild difficulty with directional orientation on the road map test. Only one subject with
developmental prosopagnosia had difficulty with cognitive map formation, and none were
impaired on the other tests. Scores for house and scene recognition co
elated most
strongly with the results of the questionnaire.
We conclude that topographic disorientation in acquired prosopagnosia reflects
impaired place recognition, with a contribution from poor cognitive map formation when
there is occipitotemporal damage. Topographic impairments are less frequent in devel-
opmental prosopagnosia.
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.S. Barton).
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Navigating through the environment is a complex function
that, like all high-level abilities, involves a number of cogni-
tive skills. This ability is impaired in subjects with topographic
disorientation, a disorder first described 150 years ago
(Ba
ash, 1998), which leads invariably to the complaint that
subjects get lost in su
oundings that should be familiar.
Given the multiplicity of cognitive operations involved, topo-
graphic disorientation is a heterogeneous collection of con-
ditions, with different subjects varying in the reasons for thei
failure to find their way. In recognition of this, several tax-
onomies of the various problems that can lead to topographic
disorientation have been proposed (Agui
e and D'Esposito,
1999; Arnold et al., 2013; De Renzi, XXXXXXXXXXFor example, in
some subjects the main deficit may be failure to recognize
landmarks (McCarthy, Evans, & Hodges, 1996; Takahashi and
Kawamura, 2002), while in others, landmark recognition
may be intact but there is difficulty in learning or recognizing
scenes (Epstein, Deyoe, Press, Rosen, & Kanwisher, 2001;
Mendez and Che
ier, XXXXXXXXXXOthers who can also recognize
landmarks may not accurately represent the spatial relation-
ship between locations (Takahashi, Kawamura, Shiota,
Kasahata, & Hirayama, 1997), or derive the spatial layout of
the environment (De Renzi, Faglioni, & Villa, 1977; Pai, 1997)
and therefore cannot form a cognitive map (Iaria, Bogod, Fox,
& Barton, XXXXXXXXXXThe evaluation of these different abilities is
eflected in the evolving design of test batteries for topo-
graphic skills (Arnold et al., 2013; Liu, Levy, Barton, & Iaria,
2011).
Topographic disorientation has also had a long-known
elationship to prosopagnosia, the inability to recognize
familiar faces. In fact, LL, one of the first cases of proso-
pagnosia described (Quaglino and Borelli, 1867), had impaired
spatial orientation and could not remember the facades of
houses or familiar scenes (Benton, 1990; Della Sala and Young,
2003). Also, the first large series of 22 subjects with acquired
prosopagnosia noted a close association of this conditionwith
“vestibular and directional distu
ances” p. 28 of (Hecaen and
Angelergues, XXXXXXXXXXSince then there have been numerous
anecdotal reports (Barton, Press, Keenan, & O'Connor, 2002;
Bauer, 1984; Clarke, Lindemann, Maeder, Bo
uat, & Assal,
1997; Landis, Cummings, Benson, & Palmer, 1986; Malone,
Mo
is, Kay, & Levin, 1982; Martins and Cunha e Sa, 1999;
Takahashi, Kawamura, Hirayama, Shiota, & Isono, 1995;
Uttner, Bliem, & Danek, 2002) and a recent review of ac-
quired prosopagnosia found explicit mention of topographic
problems in 29% of 147 cases (Schmidt, XXXXXXXXXXA relevant
observation is that, in 31 patients with posterior cere
al
arterial infarction, half of patients with impairments on tests
of face recognition were also impaired on house recognition
(Martinaud et al., XXXXXXXXXXOne potential explanation of this as-
sociation is the anatomic proximity of the parahippocampal
place area, a region activated by viewing scenes (Epstein and
Kanwisher, 1998), to the fusiform face area (Kanwisher,
McDermott, & Chun, 1997), an important component of the
face processing network (Haxby, Hoffman, & Go
ini, 2000).
These observations raise a number of questions. First, the
type of topographic disorientation in these subjects has rarely
een investigated or clarified.WFwas impaired on amaze test
(Henke, Schweinberger, Grigo, Klos, & Sommer, 1998) and VH,
a subject with progressive right temporal atrophy, developed
slight difficulty with a test of famous place identification as
her disorder progressed (Evans, Heggs, Antoun, & Hodges,
1995). Some of the anecdotes reported would suggest that
subjects had trouble recognizing places (Clarke et al., 1997;
Landis et al., XXXXXXXXXXHowever, at this point the nature of
topographic impairment associated with prosopagnosia must
e considered unknown.
Second, it is not clear whether topographic impairments
are linked to a specific type of prosopagnosia, which, being a
complex task like topographic disorientation, is not a single
entity but a family of disorders with different functional and
structural bases (Barton, XXXXXXXXXXAnatomically, face processing
involves a network of regions (Haxby et al., XXXXXXXXXXWhile pro-
sopagnosia is classically associated with bilateral medial
occipitotemporal lesions (Damasio, Damasio, & van Hoessen,
1982; Meadows, 1974), it has since been described with othe
lesions, such as right occipitotemporal and right or bilateral
anterior temporal (AT) lesions (Barton, XXXXXXXXXXThese structural
variants may also co
espond to functional subtypes, with
occipitotemporal lesions causing apperceptive face process-
ing deficits and right AT lesions impairing access to facial
memories (Barton, 2008; Damasio, Tranel, & Damasio, 1990;
Davies-Thompson, Pancaroglu, & Barton, XXXXXXXXXXSince not all
prosopagnosic subjects have topographic disorientation
(Schmidt, 2015), a natural question is whether topographic
impairments co-segregate with certain anatomic variants of
prosopagnosia. Furthermore, a developmental form of pro-
sopagnosia has been described recently (Duchaine and
Nakayama, 2006b; Susilo and Duchaine, XXXXXXXXXXThe nature of
the functional deficits and structural anomalies of the devel-
opmental variant are still being clarified (Avidan and
Behrmann, 2014; Stollhoff, Jost, Elze, & Kennerknecht, 2011).
Whether or how frequently topographic disorientation is
associated with this form is also uncertain.
In this study we evaluated spatial orientation skills in a
large cohort of these rare subjects, both those with acquired
prosopagnosia from a variety of lesions, as well as a second
group with developmental prosopagnosia. Our goals were
two-fold. The first was to determine if topographic impair-
ments were present in all groups or specific to certain types of
prosopagnosia. The second was to evaluate the type of the
topographic impairments present, by using a selected battery
of tests for different navigational skills. These included place
ecognition, directional orientation on map reading, and
cognitive map formation. In one taxonomy of topographic
disorientation (Agui
e and D'Esposito, 1999), these can be
considered approximately as tests for the subtypes of land-
mark agnosia, heading disorientation, and anterograde
disorientation.
1. Methods
1.1. Subjects
1.1.1. Acquired prosopagnosia
This cohort included 10 subjects (5 female, age range 24e70
years, mean 43.4 years, SD 17.1 years). All subjects had a
detailed neuro-ophthalmologic history and examination, with
est-co
ected acuity of 20/60 or better, as well as Goldmann
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perimetry and the Farnsworth-Munsell 100-hue test of colo
discrimination. All complained of impaired face recognition in
daily life and were impaired on both a famous faces test of
ecognition (Barton, Cherkasova, & O'Connor, 2001) and on at
least one of either the Cam
idge Face Memory test (Duchaine
and Nakayama, 2006a) or the faces component of the War-
ington Recognition Memory test (Wa
ington, 1984), while
performing normally on the word component of the latte
(Table 1). None had complaints of mistaking one type of object
for another in daily life, and all were able to recognize objects
or their drawings during the neuro-ophthalmologic exam.
They were also administered a battery of standard neuro-
psychologic tests to exclude more general problems of atten-
tion, memory and vision (Table 2). During the clinical
interview, several acknowledged difficulties with recognizing
places or getting lost in familiar places, while others were not
aware of such problems (Table 3).
1.1.2. Developmental prosopagnosia
This cohort consisted of 7 adult subjects (5 female, age range
35e61 years, mean 44.6 years, SD 9