Visual agnosia Download

Visual Agnosia
I. Biran, MD, and H. B. Coslett, MD
Department of Neurology, University of Pennsylvania School of Medicine, 3400 Spruce Street, Philadelphia, PA 19104, USA.
E-mail: [email protected]
Current Neurology and Neuroscience Reports 2003, 3:508–512
Current Science Inc. ISSN 1528–4042
Copyright © 2003 by Current Science Inc.
The visual agnosias are an intriguing class of clinical phenomena that have important implications for current theories of high-level vision. Visual agnosia is defined as impaired
object recognition that cannot be attributed to visual loss,
language impairment, or a general mental decline. At least
in some instances, agnostic patients generate an adequate
internal representation of the stimulus but fail to recognize
it. In this review, we begin by describing the classic works
related to the visual agnosias, followed by a description of
the major clinical variants and their occurrence in degenerative disorders. In keeping with the theme of this issue, we
then discuss recent contributions to this domain. Finally, we
present evidence from functional imaging studies to support the clinical distinction between the various types of
visual agnosias.
The term “agnosia” was coined by Freud [1] in his discussion of aphasia and related disorders. Like subsequent
investigators, he described a disruption between objects
and their concepts. However, there are earlier descriptions
of similar clinical phenomena. Munk [2] described dogs
with parieto-occipital lesions that were able to avoid
objects in their surroundings but failed to recognize the
objects. He termed this behavior as “Seelenblindheit”
(mind-blindness) [2]. An important early theoretical contribution was made by Lissauer [3], who offered the distinction between two clinical forms of impaired object
recognition: “apperceptive” and “associative” agnosias. On
Lissauer’s account, the former reflects a failure to generate a
fully specified perceptual representation, whereas the latter
is attributable to an inability to link an adequate percept to
stored knowledge indicating its name, function, size, and
so forth [3] (translated into English by Jackson [4]). As
noted by Teuber [5], associative visual agnosia may be
regarded as a “normal percept stripped of its meaning.”
Earlier descriptions of visual agnosia were provided by
Finkelnburg’s account [6] of “asymbolia” and Jackson’s
concept [7] of “imperception.”
Clinical Variants
Visual agnosia can be specific to certain kinds of objects.
Accordingly, there are agnosias for objects, agnosias for
faces or “prosopagnosia,” agnosias for words or “pure
word blindness,” agnosias for colors, and agnosias for
the environment, including landmarks. Finally, the disorder of simultanagnosia—an inability to “see” more
than one object at a time—is often regarded as a type of
visual agnosia.
Agnosia for objects
Inability to recognize familiar objects is the most common of the agnostic syndromes. Patients are impaired in
naming regular objects and are often unable to describe
them or mimic their use. Object agnosias are further
classified as either apperceptive (the percept is not fully
constructed and, therefore, patients are unable to copy
drawings) or associative (the percept is relatively intact
and patients are able to copy drawings). As the following text discusses, the agnosia can be specific to a
semantic category, usually living or animate objects;
agnosias for nonliving or inanimate objects have also
been described [8].
Prosopagnosic patients are unable to recognize the identity of faces (ie, to whom a face belongs), although they
are capable of recognizing that a face is a face and, in
some instances, the gender and age of the person.
Prosopagnosia is usually secondary to temporo-occipital
lesions, affecting the fusiform and lingual gyri. Whether
a bilateral or a right unilateral lesion is sufficient to cause
the deficit has been an issue of debate [9]. There is also
evidence that impaired face recognition could be
encountered with frontal lesions. Rapcsak et al. [10] documented both anterograde and retrograde face memory
impairment in subjects with frontal lesions.
Agnosia for words
This is also known as pure alexia, alexia without agraphia,
or pure word blindness. Although this phenomenon is
usually discussed in the context of language impairments,
it is an agnostic symptom, as subjects who suffer from this
deficit show a language impairment limited to visually presented stimuli (eg, reading), but not to auditorily presented stimuli. Accordingly, this deficit could be regarded
as a failure in the visual recognition of words, and thus as
an agnostic deficit [11].
Visual Agnosia • Biran and Coslett
Color agnosia
In this rare clinical syndrome, patients fail to name colors.
This deficit is not secondary to basic color perception, as
demonstrated by tasks requiring color categorization and
hue perception. The distinction between this syndrome
and color anomia is not clear. Some authors suggest that
the two syndromes could be differentiated by tasks probing color information (ie, matching between known
objects to colors), which is impaired with agnostic subjects
and preserved with anomic subjects [12,13].
Progressive prosopagnosia
This is a degenerative disorder presenting with progressive
impairment in the recognition of faces. This syndrome is
part of the fronto-temporal dementias (FTDs), which may
present as focal atrophy in any combination of the right
and left frontal or temporal cortices. Although in the
semantic dementia variant of the FTDs the atrophy is
prominent in the left temporal lobe, in progressive
prosopagnosia the atrophy is prominent in the right temporal lobe [20–22].
Landmark agnosia
Landmark agnosia is one of the causes for topographic disorientation (the loss of way-finding ability). Patients with
landmark agnosia are unable to use environmental features for orientation. This deficit is usually secondary to
lesions of the medial aspect of the occipital lobes, either
bilaterally or right-sided. Pallis [14] reported a classic case
of this disorder, and the topic has recently been reviewed
by Aguirre [15].
Although not a classic neurodegenerative disorder,
schizophrenia is often associated with visual agnosia. In
a recent study of 41 patients with schizophrenia,
Gabrovska et al. [23] reported a high incidence of visual
processing deficits that were similar to associative agnosia. Schizophrenia patients also demonstrate a specific
impairment to memorizing faces. This deficit is highly
correlated with a reduction in the volume of the fusiform
gyrus [24]. In conjunction with other reports of discrete
cognitive impairments in schizophrenia [25], these contributions help to bridge the gap between schizophrenia
and behavioral neurology.
Simultanagnosia is the inability to perceive simultaneously several items in the visual scene. This piecemeal
perception of the visual environment causes severe disability and patients often behave as blind subjects.
Simultanagnosia can be part of Balint’s syndrome [16],
which also includes an inability to shift gaze (psychic
paralysis of gaze) and difficulties in reaching visualized
objects (optic ataxia). This complex syndrome is associated with bilateral lesion of the posterior parietal and
occipital lobes [17].
The visual agnosias can teach us about the way we allocate
attention to the external world and build an internal mental
representation. In the following section, we focus on recent
work that explores the cognitive deficits underlying visual
agnosia. These reports not only contribute to our understanding of the clinical disorders, but also have implications
for our understanding of perception and cognition.
Visual Agnosia in Degenerative Disorders
The clinical phenomena discussed here were described
mainly through lesion studies. However, the agnosias are
also prevalent in degenerative disorders, often at a stage of
the illness at which general cognitive abilities are at least
relatively preserved. The following syndromes have been
reported in neurodegenerative disorders.
Posterior cortical atrophy
This disorder presents with a progressive decline in complex visual processing and relative sparing of other cognitive abilities [18]. It is associated with occipito-parietal
atrophy and hypometabolism on single photon emission
computed tomography (SPECT) or positron emission
tomography (PET) scans. In most instances, the disorder is
caused by Alzheimer’s disease. However, posterior cortical
atrophy differs from typical Alzheimer’s disease in that the
lesions show predilection to the posterior parietal and
occipital areas. Patients with this syndrome show a high
rate of alexia without oral language difficulty (80%),
Balint’s syndrome (68%), and visual agnosia (44%) that is
primarily apperceptive [19•].
Simultanagnosia can teach us about the way we allocate and
shift attention. According to Posner et al.’s [26] paradigm,
shifting attention from a previous to a novel focus is performed in three steps: 1) disengaging from the previous
focus, 2) moving attention between the foci, and 3) engaging
attention at the new focus. In a recent report, Pavese et al.
[27•] provide compelling evidence that, at least in some
instances, simultanagnosia is associated with a deficit in disengaging visual attention. They studied a patient with simultanagnosia whose ability to report both items in an array was
greatly facilitated by removing the item that he had initially
reported. Performance was not improved by the sudden
onset of a second stimulus, suggesting that once he had
“locked onto” a stimulus, he was unable to disengage attention and shift to a different object or location [27•].
Mental representations
Visual agnosia is generally regarded as a deficit in the processing of information, such that knowledge of the shape,
form, and other stored knowledge of the physical attributes
of an object cannot be accessed. In some instances, there is
strong reason to believe that the mental representations of
that knowledge are preserved. Several investigators have
recently reported data from visual imagery tasks that demonstrate that stored visual knowledge may be at least relatively preserved in patients with severe visual agnosia.
Simultanagnosic patients can be impaired in the allocation of attention not only in the context of a visual scene,
but also in mental imagery. An interesting clinical observation is that of an artist who, following a stroke in the posterior circulation, suffered from simultanagnosia. During her
stroke recovery while painting scenes from memory, her
drawings revealed selective attention to the left lower quadrant, with important aspects of the whole image “clipped,”
as if missing from her internal representation of the scene
[28]. Subjects with prosopagnosia can show impaired overt
recognition of faces with relative preservation of covert recognition of these stimuli (eg, these patients may fail to
match faces, but event-related potentials could demonstrate covert matching) [29]. The covert recognition of
faces suggests that internal representations of faces can be
relatively preserved in prosopagnostic subjects. Barton and
Cherkasova [30] studied nine prosopagnostic patients and
assessed their mental imagery for faces by a questionnaire
composed of 37 questions probing facial features (eg, who
has a bigger moustache—Stalin or Hitler?) and facial shape
(eg, who has a more pear-shaped face—John F. Kennedy or
Nixon?). They demonstrated a dissociation between performance on tasks assessing facial features as compared
with face shape; deficits in the former were associated with
left occipito-temporal damage whereas deficits in the latter
were associated with lesions of the right fusiform face area.
Covert face recognition (assessed by sorting famous faces
by occupation and by pointing out a famous face from two
faces) correlated with feature imagery. Finally, impaired
mental representation in a visual agnostic-like pattern can
also be demonstrated in pure alexic subjects. Bartolomeo et
al. [31] described a patient who was impaired in tasks
assessing mental imagery of letters (judging whether an
upper-case letter has curved lines), but had a faultless performance when he was allowed to trace the contour of the
letters with his finger. This suggests that his impairment
was isolated to the visual representation of the letters, but
not to their relative motor engrams [31].
As briefly noted previously, for some patients the ability to
recognize visually presented stimuli is significantly influenced by the semantic category of the item. Thus, a number of patients have been reported, for example, who are
able to name man-made objects but are severely impaired
in naming naturally occurring items such as animals, fruits,
and vegetables. A number of competing hypotheses try to
explain these category-specific deficits. The modality-specific hypothesis [8], later named the Sensory-Functional
Theory (SFT) [32], postulates that the animate versus inan-
imate dissociation follows from a selective impairment of
the sensory or functional attributes that subserve the processing of either of these two categories. On this account,
the identification of animate objects relies more on sensory attributes and would be disproportionately impaired
by damage to the processing of sensory features associated
with these objects. In contrast, inanimate objects may be
known primarily by virtue of their function and the manner in which they are used or manipulated. As a consequence, a deficit in the recognition of inanimate objects
would be disrupted by loss of information regarding the
function of an object or sensory-motor knowledge regarding the manner in which the object is manipulated. A competing hypothesis is that the semantic knowledge is
organized categorically in the brain [32]. Clearly, teleologic
explanations for this organization can be made. Evolutionary pressures would favor an animal that could easily recognize and distinguish other animals that are potential
predator or prey or plants that are potential sources of
food. Further, developmental data support the idea that
infants as young as 3 months of age can differentiate living
from nonliving things [33].
There have been several recent contributions to this
debate. Borgo and Shallice [34] demonstrated that subjects
with specific impairment to animate objects are also
impaired in the recognition of inanimate materials (eg, liquids) for which sensory-motor knowledge is lacking and
that are distinguished by sensory features such as texture.
They concluded that these data are not consistent with the
proposal that there is a fundamental distinction between
items as a function of semantic category [34].
The following case study provides data consistent with
the categorical hypothesis. We recently studied a 50-yearold patient who suffered a stroke involving the anteromedial aspect of the right occipital lobe (Coslett and Biran,
unpublished data). Following this insult, he suffered from
a marked visual recognition deficit and memory loss. Neuropsychologic tests showed normal attention, concentration, and working memory, and impaired immediate and
long-term memory. The patient performed normally on
the Wisconsin Card Sorting Task. Despite good performance on a variety of tests assessing visual processing, he
performed poorly on the Boston Naming Test and the Benton Facial Recognition Test. He was significantly impaired
naming animate as compared with inanimate items (42%
vs 75%, chi-squared test P value=0.019).
We than evaluated the contribution of various knowledge types (sensory, functional, encyclopedic, and taxonomic) to the naming performance and the differential
animate/inanimate impairment observed with AD. In a
naming to confrontation task, the subject was presented
with color pictures of 194 inanimate objects and 150 animate objects; accuracy and reaction time were recorded.
For each item, 30 control subjects had listed semantic features that were further classified into the following categories: sensory (eg, “a lantern is bright”); function (eg, “ovens
Visual Agnosia • Biran and Coslett
are used for broiling”); and encyclopedic/taxonomic (eg,
“dove is a symbol of peace”) [35]. Using a stepwise discriminant analysis, we evaluated the predictive value of the
various factors such as stimulus frequency, familiarity, animacy, and types of knowledge that defined the object.
This subject named the inanimate objects significantly
better and faster than the animate objects (69% accuracy
for inanimate, 37% accuracy for animate, chi-squared test
P value=0.0001; response time of -4633 ms for inanimate
objects, response time of -7581 ms for animate objects, t=3.416; P=0.008). In a discriminant function analysis, the
only factor contributing to his performance was animacy
versus inanimacy. This suggests that in this case, the animate/inanimate distinction cannot be reduced to different
features, different knowledge types, and other variables
such as frequency or familiarity, and are rather related
directly to the category itself.
trally than peripherally located faces, and that the place
areas responded more to peripherally than centrally
located places. They suggested that objects whose recognition and analysis require fine details (eg, faces) will be
linked to centrally located activation, whereas large objects
(eg, houses) will be linked to peripheral activation.
In reviewing recent contributions to the understanding of
the heterogeneous category of visual agnosias, we have
attempted to highlight not only the clinical phenomenology of these disorders, but also their implications for
accounts of the manner in which visual information articulates with other brain faculties. Although the agnosias have
been investigated for more than 100 years, exploration of
these fascinating disorders continues to offer important
insights into brain function and organization.
Functional Imaging of Object Recognition
In the past few years, functional imaging in healthy subjects has helped to elucidate the anatomy of object recognition. Malach et al. [36] described the lateral occipital cortex
(LOC), which is located at the lateral and ventral aspects of
the occipito-temporal cortex. This area is activated preferentially by objects compared with scrambled objects or textures, regardless of the nature of the object (eg, faces, cars,
common objects, and even unfamiliar abstract objects)
[36,37]. Further processing of the visual stimuli occurs in
specific brain areas according to stimulus category. For
example, faces are processed in the fusiform face area [38]
and in the occipital face area [39]; the former is more selective for faces than the latter. Places and/or spatial layouts
are processed in the parahippocampal place area [40],
whereas objects like animals and tools are processed in
specific loci in the fusiform and the superior and middle
temporal gyri [41]. Orthographic stimuli are processed in
the left inferior occipito-temporal cortex on or near the left
fusiform gyrus [42,43], although this localization is highly
debated [44]. Thus, the specific perceptual categories of
visual stimuli dictate very different ways of their processing
in the brain and might give an anatomic basis for the different agnostic syndromes.
The allocation of the different brain areas to specific
object categories could be explained in part by the eccentricity bias (a preferential response to stimuli based on
their location in the visual field, either in the center or in
the periphery). This is one of the dimensions of organization of the visual cortex, especially the low-level areas. In a
recent study, Levy et al. [45••] demonstrated a relationship
between category specificity and retinal eccentricity. They
scanned subjects while they viewed either faces or houses;
in different trials, both types of stimuli were presented in
either the center or periphery of the visual fields. They
demonstrated that the face areas responded more to cen-
Dr. Biran may be reached at the Agnes Ginges Center for
Human Neurogenetics, Hadassah University Medical Center in Jerusalem.
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Human Brain Damage
Human Brain Damage
(2) Face Recognition
(2) Face Recognition