Agnosia
Agnosia
Agnosia
21 (2003) 501520
Visual agnosia
M. Jane Riddoch, PhD*, Glyn W. Humphreys, PhD
Brain and Behavioural Sciences Centre, School of Psychology,
University of Birmingham, Birmingham B15 2TT, UK
This work was supported by grants from the MRC, Wellcome Foundation, and the Stroke
Association.
* Corresponding author.
E-mail address: m.j.riddoch@bham.ac.uk (M.J. Riddoch).
0733-8619/03/$ - see front matter 2003, Elsevier Inc. All rights reserved.
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the same luminance, wavelength, and area when the only dierence between
them was shape. Over the years, there has been some controversy as to
whether or not decits in form perception, such as that shown by Mr. S., may
be classied as decits of low-level visual processing or whether or not they
form part of the agnosia continuum. In the 1950s, Bay argued that the sensitivity in visual testing was lacking in such patients. He used more detailed
examination techniques than were generally applied clinically, including tests
for local adaption and for sensation time, Bay dened sensation time as the
minimal time required for the appearing of a sensation (p. 516). Stimuli
were presented tachistoscopically in dierent parts of the visual eld. The
time taken to detect the stimuli was raised in areas of decreased function.
Adaption occurred if a constant stimulus was applied to a xed area of the visual eld. Over time, the perception of this stimulus slowly faded. The fading
time was dependent on the objects size and its positioning in the visual eld.
Fading occurred more rapidly in impaired areas of the visual eld and demonstrated disorders of visual functioning that had not been apparent on
standard perimetric testing in a variety of brain-damaged patients, including
a patient with visual agnosia [7]. Bay found that the retina in patients with
apparently normal visual elds showed abnormal fatigue. The abnormality
was greatest in the central retinal region but aected the periphery more (visual stimuli would tend to drop out of awareness). Bay argued that the visual
eld essentially was contracted and therefore would not allow the simultaneous perception of a whole visual stimulus in circumstances in which the visual
angle subtended by the stimulus was greater than the remaining functional
central area. As a result, it would not be possible to gain a holistic view of
the stimulus, but details of it may be seen in succession. These eects must
be contrasted with whose occurring in cases of simultanagnosia. Here also
identication is limited to one object at a time; however, now what denes
the object is critical. Luria [69] described a patient who was able to report
the star of David when shown the stimulus in a single color; however, the
patient only reported the presence of a triangle when the two triangles making up the star of David were shown in dierent colors. Identication here is
not determined by the spatial extent of the stimulus but by how the parts
group together (when in the same color) or segment apart when in dierent
colors. Bays [7] attribution of impaired visual recognition to disturbed
sensory processes resulted in more stringent assessments of many of the
subsequently reported cases of visual agnosia. For example, a detailed
investigation of visual abilities of a patient with visual agnosia, HJA [8],
showed no tunnel vision [9]; however, he was impaired in detecting local elements embedded in more global geometric forms. Thus, whereas he performed at normal levels in detecting a line target embedded in distractor
lines of a dierent orientation, he was unable to perform a similar task when
the target was a square made of four parallel lines (Fig. 1). Similarly, HJA
was abnormally slow in responding to local elements in compound global
letters [10], although he could respond to the global form itself (Fig. 2).
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Fig. 1. Examples of the displays used by Alkhateeb et al [9]. In (A) the elements consist of single
lines; in (B) they consist of groups of lines. (Adapted from Alkhateeb W, Bromley JM,
Humphreys GW, Javadnia A, Riddoch MJ, Ruddock, H. Abnormal responses to multi-element
spatial stimuli in a subject with visual form agnosia. Clinical vision Science 1992; 7;16373; with
permission.)
Alkhateeb et al [9] argue that this pattern of performance in more complex search tasks mirrors HJAs ability to identify correctly local features of
visual scenes, while being unable to link them into a coherent percept (see
later discussion of Perceptual integration of form information). Others
also explored whether or not impaired low level vision (such as the thresholds for detecting and discriminating gratings, color, correlated movement,
reectance, shape from motion or luminance contrast, relative position, texture, and orientation) in separate studies in groups of patients with localized
Fig. 2. A Navon-type stimulus consisting of a global shape (the letter H) made up of smaller
letters (S).
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brain damage can account for recognition disorders. The accumulated data
show that whereas there may be elevated thresholds, there is no correlation
between the pattern or the severity of impairments and the presence or
absence of visual agnosia (for a discussion of these issues, see Cowey [11]).
In the 1980s Campion and coworkers argued that the visual recognition
problem in patients with agnosia resulting from a particular etiology, carbon monoxide poisoning, is the result of multiple small scotoma (resulting
from the multiple lesions caused by the poisoning). They proposed that the
behavioral consequences of such lesions would be that patient viewed the
world through a peppery mask [12,13]. Given that we adapt over natural
holes because of the blind spot, however, and that any masking eect may
be reduced by movement, then the import of this argument is not clear. An
alternative account is that the problem results from impaired grouping processes [14,15] (see later discussion). Recently, Vecera and Gilds [16] attempted
to distinguish between these possibilities in a series of experiments with normal subjects. The basic paradigm required subjects to respond to a spatially
cued target. There were two conditions to the experiment: either subjects
viewed the displays (two rectangular bars) through a peppery mask (masking condition), or the displays were degraded in one of two ways (grouping
condition). In the grouping condition, either the midsections of the rectangles were removed (cues such as co-linearity and closure remained present,
allowing grouping of the parts into an object) or the corners were removed
(making it more dicult to group the parts into objects). The displays were
aligned either horizontally one above and one below the xation cross, or
they were aligned vertically, again one on each side of the xation cross.
A spatial cue appeared at one end of one of the bars. This was either valid
(75% of trials) or an invalid (25% of trials). After the cue, the two bars were
shown empty for 200 ms. On valid trials, the target then appeared in the
cued location. On invalid trials there were three possible locations for the
target: (1) in the same bar as the cue but at the opposite end; (2) in the other
bar in the same relative spatial location as the cue; or (3) in the other bar and
at the opposite end to the relative spatial location of the cue (for examples of
the stimuli, see Fig. 3). In the masking condition, RTs were slowed but the
pattern of results was similar to that obtained from unmasked displays (ie,
there was a valid cuing eect with responses to targets in the cued rectangle
faster than those to target in the in uncued rectangle). In the grouping conditions, there was no eect of degrading when only the corners of the rectangles were present, suggesting that grouping processes nullify this form of
degradation. There was an eect of degrading, however, when only the midsections of the rectangles were present (ie, in the circumstances when grouping could not occur). Vecera and Gilds [16] argue that their results support
the grouping-decit account of visual agnosia (see later discussion of Feature integration).
Warrington [17] also argued the poor recognition in cases such as those of
Efron [6] are conceptualized best as a partial or incomplete visual eld
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Fig. 3. Stimuli similar to those used by Vecera and Gilds [16]: (A) illustrates the sequence of
events: a cue rst appears at the end of one of the rectangles, there is an interstimulus interval,
and the target then appears in one of three possible locations; (B) illustrates the masked
displays; and (C ) shows the stimuli with corners or mid sections only. (From Vecera SP, Gilds
KS. What processing is impaited in apperceptive agnosia? Evidence from normal subjects.
Journal of Cognitive Neuroscience 1998;19: 56880; with permission.)
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particular, they propose that the term apperceptive agnosia be reserved for
disorders reecting damage to those sub-components of object recognition
that implicate the ability to construct, by recourse to stored representations,
an object specic structural description [18]. Tests used to assess whether or
not stored representations can be accessed include identifying overlapping,
familiar objects [19,20], incomplete outline drawings of objects [21], or
unconventional view object photographs [22]. In all these instances, patients
with posterior right hemisphere damage seem to be selectively impaired. One
diculty with this account is that, although right hemisphere patients show
impaired performance on a variety of perceptual tasks, they typically do not
have any diculty recognizing undegraded objects in conventional views;
such a diculty would seem to be central to the concept of visual agnosia.
Whilst acknowledging these arguments, the weight of opinion is that deficits of form processing can occur and that these are independent of early
visual processes that may be reected in poor visual acuity, reduced visual
elds or impairments in color, or movement or depth perception. In addition, some studies report measures of contrast sensitivity, visual evoked
responses, eye movements, and detection of targets dened by luminance,
which can be preserved even though problems in form perception are demonstrated [23].
Apperceptive disorders
Lissauer suggested two ways to assess the integrity of form perception: (1)
shape discrimination and (2) shape copying. He reported the results of these
tests with his patient, GL. With shape discrimination, GL initially was asked
to detect obvious dierences between simple shapes and then minimal dierences between complex shapes. He performed well with simple tests (eg, he
was asked to discriminate between shapes similar to the letter 3; one of the
shapes had an additional curl at the top), but performance slowed with more
complex tests (eg, he was asked to distinguish between two boxes, each of
which contained 12 equally distributed crosses; in one box, the center was
empty, whereas the other was lled with a cross). On the basis of these
observations, Lissauer argued that perceptual abilities might lie on a continuum, with the implication that a simple shape discrimination test is not sufcient to determine whether or not a perceptual decit is present. GLs
diering performance on the discrimination tests suggests that one may distinguish his processing of form (which the authors imply is intact based on
his performance in the easy discrimination test) from his ability to integrate
local and global aspects of form (which may be impaired, given his performance on the dicult discrimination test).
Lissauers patient was able to copy; however, again it is clear that Lissauer
did not regard copying ability as denitive proof of intact perception. He
indicates that the procedure used by the patient was very slow with many
pauses. He also noted that GL found it easier to copy line drawings than real
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objects, because it was dicult to perceive the outline contour when shadows
were present. Recently, the dierences between drawing real objects and
copying line drawings have been explored empirically in a patient with visual
agnosia [24]. The patient, HJA, was asked to copy line drawings or to draw
objects, but in conditions of good lighting, without shadow. There were several conditions: either HJAs head was xed or he was allowed free movement. Also, objects were positioned within or outside reaching range in
order to vary the potential contribution of stereoscopic depth (stereo cues
being stronger within reachable space [25]) (see Fig. 4 for examples of HJAs
performance). This enabled judgment of the role of such cues in HJAs object
identication. All the drawings subsequently were presented to a group of
control subjects who were asked to name the depicted objects. The results
showed no reliable dierence in the identication of line drawings versus real
objects when the objects were close, even when head movements were prevented. When HJAs head was xed, however, and objects were viewed from
a distance, few of his drawings could be identied. In this condition, he typically failed to depict all the parts of the object successfully. The data indicate
that stereo depth cues may play an important part in such patients perceiving
objects, with perception abnormally impaired when stereo depth cues are
reduced, by preventing motion and stereo disparities (with a xed head position and more distant stimuli). In line with Lissauers original observations,
these data also suggest that the ability to copy items varies as a function of
test conditions and that apparently good copying cannot necessarily be taken
as evidence of intact perception. Given this proviso, we review the cases of
several patients in the literature, taking their ability to discriminate shapes
and to copy drawings as a starting point. We show that some patients are
unable to perform even these simple tasks (presumably because of impaired
form perception) and that, whereas others succeed, performance is far from
normal. In these instances, we propose that the decit is described best as a
perceptual decit specically aecting processes of visual integration.
Impaired form perception
Many patients have been described with a profound decit in form perception who are unable to either discriminate between simple shapes or to
copy drawings successfully [6,12,2628]. Interestingly, all these cases suered
carbon monoxide poisoning. Color, brightness, and movement discrimination typically were preserved, whereas the ability to perceive gural properties, such as size, orientation, and shape, was lost [6,28]. For instance,
Efrons patient, Mr. S., was unable to discriminate between a square and
a rectangle that were matched for total ux. Task diculty was manipulated
by varying the ratio of length to the width of the oblong. Mr. S. was barely
above chance, except on the easiest discriminations. In a more extensive
report of patient DF, Milner and colleagues [28] indicate that she performed
at chance on a similar test to that described by Efron [6]; she also was unable
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Fig. 4. Examples of HJAs copies of (A) copies of line drawings; (B) real objects presented at a
distance with the head not xed; (C ) copies of real objects (distant condition, head xed); (From
Chainey H, Humphreys GW. The real-object advantage in agnosia: evidence for a role of
surface and depth information in object recognition. CognitiveNeuropsychology 2001;18:175
91; with permission.)
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Fig. 5. Examples of the stimuli used by Giersch et al [39]: (A) non-overlapping, (B) overlapping
non-occluding, (C ) overlapping, occluding, and (D) overlapping silhouettes. (From Giersch A,
Humphreys GW, Boucart M, Koviaks I. The computation of occluded contours in visual
agnosia: evidence of early computation prior to shape binding and gure-ground coding.
Cognitive Neuropsychology 2000;17:73159; with permission.)
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impaired when more stringent tests are used. One of these, HJA [8], was previously discussed, and his case is discussed in more detail here because it
reects a particular problem in coding complex shapes. Like Lissauers
patient, GL, HJA was able to produce accurate drawings of objects he could
not recognize, although, like GL, he was very slow. He also performed the
Efron [6] shape test well and could make orientation and size-matching
judgments at a normal level [42]. He showed at search functions (ie, no
eect of the number of distractors) on visual search tasks in which the target
diered from the distractors in terms of a single feature (eg, line orientation)
[14,43]. These data suggest that HJA is able to process simple form information in a spatially parallel manner. On other tests, however, he did not do as
well. For instance, he was at chance on an object decision task in which nonobjects were constructed using parts of real objects, although in an alternative version of the task in which silhouettes rather than line drawings were
used, he performed within normal limits. The internal detail in the line drawings seemed to disrupt rather than enhance his performance (nonbrain
damaged subjects nd line drawings easier to discriminate than silhouettes
[44]). Furthermore, as indicated in the previous section on Impaired form
perception, whereas HJA was able to identify the individual items in overlapping gures, he was slow relative to control performance [8]. In addition,
we also have shown that HJAs visual recognition is compromised if time
restraints are imposed. With unlimited exposure, he was able to name
80% of a set of line drawings, selected on the basis of previous successful
performance; however, at 100 ms, he was only able to name 15% of them.
These ndings suggest that HJAs perceptual abilities were impaired (1)
under speeded conditions and (2) when there were multiple segmentation
cues. Riddoch and Humphreys [10] characterized HJAs decit as a failure
to integrate local visual elements into perceptual wholes. This is not to say
that HJA is insensitive to global shape information. As noted, using Navontype stimuli in which large global letters are made up of smaller local
letters [45] (see Fig. 2), HJA responds faster to the global than to the local
letter (as with control subjects). Unlike normal subjects, however, the identity of the local letter had no eect on his responses to the global letter. His
responses to the local letter when presented in isolation were also within the
normal range, but he was slow when he had to identify the local letter in the
context of the global letter. This suggests that there is an abnormal eect of
global context that hinders his accurate perception of local detail. Consistent with this, HJA was impaired at grouping homogeneous distractors in
visual search tasks in order to detect targets eciently [15]. Normally, a
homogeneous context facilitates search by helping distractors form a separate group from the target. The detrimental eect of the distractor context,
for HJA, is indicative of interference from more global groups on the coding
of a target part.
To account for this pattern of performance, Riddoch and Humphreys
proposed that HJA had impaired perceptual integration of shape elements
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(eg, hand postures) or internal structure (eg, gures from Rays Progressive Matrices). Against her good performance on tests of form perception,
Annalisa was impaired on tests of gureground segmentation: these included detecting a fragmented letter superimposed on a noisy background
[47] and a test based on that described by Ghent [48], in which displays of
three to ve overlapping drawings of either meaningful or meaningless items
(in separate conditions) were presented with 10 single drawings of items
from the appropriate condition. The task was to choose which of the single
items were present in the target array.
Similar eects have been reported recently in two further cases (SZ and
AP) [49]. SZ had bilateral lesions implicating the posterior watershed distribution with sparing of the primary visual cortex, and AP had decits aecting bilateral middle and inferior temporo-occipital cortices again sparing
the primary visual cortices. Both patients performed reasonably well when
asked to match a target item (a geometric shape) to one of three items
(80% and 100% correct for SZ and AP, respectively). Performance dropped,
however, when a similar task was performed with items consisting of partially overlapping geometric shapes (31% and 70% correct for SZ and AP,
respectively). Likewise, SB is reported as being able to match identical
shapes, but was at chance when asked to segment overlapping gures [50]
(also see Kartsounis and Warrington [41]). Butter and Trobe [51] reported
another patient, SM, who, like HJA, was not only impaired at overlapping
forms but was also worse with line drawings than with silhouettes. Indeed,
when presented with drawings of single objects, SM sometimes identied
them as two separate items, indicating segmentation of the parts and poor
coding of the whole. We suggest that normally an integrated representation
of the parts is linked to more holistic descriptions based on low spatial frequency components, so that we perceive wholes that are articulated and
identiable. This linkage process is impaired in integrative agnosia. Integrative agnosia represents a form of apperceptive agnosia in which the coding
of single shapes is relatively unimpaired, with the decits revealed under
conditions that stress visual segmentation and grouping.
Associative disorders
In contrast to the above cases, in which forms of perceptual decit are
apparent, many patients have been reported with impaired recognition of
visually presented objects but who perform well on tests of perception
[52,53]; thus, it seems that Lissauer was not correct in his assumption that
some form of perceptual decit underlies the recognition problem in all
patients with visual agnosia. We suggest that there exist relatively pure
forms of associative agnosia, without a concomitant apperceptive decit.
Riddoch and Humphreys [53,54] distinguished two forms of stored knowledge serving object recognition: stored structural descriptions and stored
semantic knowledge. Structural descriptions are stored representations of
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about the perceptual properties of objects, because they assumed that perceptual knowledge was key to identifying living things. In contrast to this,
nonliving things may be distinguished more on the basis of their functional
properties (what they do or how they are used) and, thus, nonliving things
would not be as dependent on access to detailed perceptual knowledge.
Thus, damage to stored knowledge about the functional properties of
objects would disturb nonliving things more than living things (for evidence,
see Warrington and McCarthy [61,62]). Other investigators argued that such
category specic decits can reect the categoric nature of our semantic representations, which may be organized modularly to separate animals from
plant life and other things. At present, there is a good deal of study targeted at distinguishing these and other relevant accounts [60]. For our purposes, the important lesson is that disorders of semantic knowledge can be
described as associative agnosias, and they can arise in patients with no
apparent perceptual problems. A case such as JBs is particularly interesting,
however, because his problem is not in semantic knowledge itself, but in
accessing this knowledge from vision. How could a decit in visual access
also generate an apparent category-specic decit? Humphreys, Riddoch,
and Quinlan [63] demonstrated that category eects are found not only in
patients but also in normal participants (albeit on measures of reaction time
rather than error). They argued that the eects occurred because many living
things have a similar perceptual structure, and this created increased competition for recognition and naming. In a patient such as JB, competition at a
semantic level may be exacerbated if the lesion adds noise to activation
that is transmitted from the structural description system. Living things are
more dicult to identify as a consequence (for a simulation, see Humphreys
et al [64]).
The notion that one cause of category-specic decits for living things
arises in visual access to semantic knowledge also is supported by patients
with relatively milder decits than JB, who present with a naming rather
than a recognition impairment for living things. SRB and DM suered damage to the left medial and inferior occipito-temporal regions and they demonstrated a particular impairment in naming animate items [65,66]. Naming
inanimate items was relatively preserved (71% versus 95% correct for SRB,
and 46% versus 75% correct for DM for animate versus inanimate line drawings, respectively). In both cases there was no eect of name frequency, and
the patients provided specic semantic information about the items they
were unable to name (eg, for kangarooit lives in Australia, it carries its
young in a pouch, it hops). Both patients performed within the normal
range on standardized tests of semantics; however, on other tests, which
stress stored knowledge of the visual features of items, performance was not
as good. Thus, when drawing from memory, their drawings of animate items
received lower ratings from control subjects than their drawings of inanimate items (control subjects were presented with all the drawings and asked
to rate how good a representation of a target object each one was; good
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representations received higher scores). Both patients were impaired somewhat, particularly when they were required to make within-category discriminations of real living objects from nonobjects created by combining
the parts of living things [67]. In addition, when the patients were required
to produce a name in response to denition stressing either the perceptual
properties of objects (eg, the name for an orange or cone-shaped vegetable)
or functional and associative properties (eg, the name of the root vegetable
that is said to help you see in the dark), the patients did well with the functional and associative denitions (92% and 89% correct for SRB and DM,
respectively) but more poorly on the perceptual denitions (51% and 42%
correct for SRB and DM, respectively (the control mean was 93.4% and
74% correct for inanimate and animate items, respectively). The data from
SRB and DM suggest that they have a mild disorder of stored perceptual
knowledge about objects, along with intact semantic knowledge of the functional characteristics of objects. Furthermore, this can produce an apparent
naming problem for living things, wherein patients sometimes seem to be
within a tip-of-the-tongue state. Humphreys, Riddoch, and Price [68] argue
that bottom-up activation of semantic knowledge from vision may be insufcient to invoke a name and that object naming requires recurrent activation of stored perceptual knowledge to dierentiate activation of a target
object from activation of other similar representations. Subtle impairments
of stored perceptual knowledge in cases such as SRB and DM produce naming decits because recurrent activation operates less well. This may be particularly important for the naming of living things, given the perceptual
similarity between their category members.
Summary
As was originally proposed by Lissauer, visual recognition may break
down either at an apperceptive or at an associative level. At an apperceptive
level, ner grain distinctions may be made; the authors distinguished here
between disorders of shape recognition and perceptual integration. It is not
the case, however, that all patients with visual recognition decits have
impaired perception: poor recognition and naming may also result from
damage to stored perceptual knowledge (eg, structural descriptions), from
problems in accessing semantic knowledge, from perceptual knowledge, or
from impairments to semantic knowledge itself. These represent dierent
types of associative decit. In some cases, mild damage to stored perceptual
knowledge also generates problems that are more severe on naming than on
recognition and more severe for some categories of objects than others.
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