Higher Cortical Visual Deficits

Review Article

Address correspondence to Dr Jason J. S. Barton, Beth Israel Deaconess Medical Higher Cortical Visual Center, 4807 Collingwood Street, Vancouver, BC V6S 2B5, [email protected]. Deficits Relationship Disclosure: Dr Barton receives personal Jason J. S. Barton, MD, PhD, FRCPC compensation for serving on the advisory board of Vycor Medical, Inc, and for speaking at the LAUNCH review course ABSTRACT for residents provided by EMD Serono, Inc. Dr Barton Purpose of Review: This article reviews the various types of visual dysfunction that has also provided expert can result from lesions of the cerebral regions beyond the striate cortex. review for several law firms Recent Findings: Patients with dyschromatopsia can exhibit problems with color and receives book royalties from Springer and UpToDate. constancy. The apperceptive form of prosopagnosia is associated with damage to Dr Barton’s laboratory is posterior occipital and fusiform gyri, and an associative/amnestic form is linked to supported by grants from the damage to more anterior temporal regions. Pure alexia can be accompanied by a Canadian Institutes of Health Research and Natural Sciences surface dysgraphia. New word-length effect criteria distinguish pure alexia from and Engineering Research hemianopic dyslexia. Subtler problems with perception of numbers and faces can Council of Canada. be seen in patients with pure alexia as well. Also, a developmental form of Unlabeled Use of topographic disorientation, which is due to problems with forming cognitive maps Products/Investigational Use Disclosure: of the environment, has been discovered. In Balint syndrome, added features of Dr Barton reports no disclosure. decreased flexibility of attention in simultanagnosia include local and global * 2014, American Academy capture. Balint syndrome can affect not just localization in space, but also in time, of Neurology. as manifest in sequence agnosia. Summary: Lesions at intermediate levels of a processing hierarchy can cause difficulty with color perception or motion perception. At a higher level, ventral lesions of the occipitotemporal lobes can lead to a variety of problems with object recognition. Dorsal lesions of the occipitoparietal lobes can cause difficulty with spatial localization and guidance.

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Most lesions of the visual system from the ventral occipitotemporal cortex the retina to the striate cortex charac- affect what has been colloquially teristically cause scotomata, regions of called a ‘‘what’’ stream, involved ulti- the visual field where vision is lost mately in object identification. The surrounded by regions where it is ‘‘intermediate’’ level of this stream is preserved. Lesions of extrastriate cor- involved particularly in color process- tex lead to very different types of ing, and a lesion of this will lead deficits, however. Rather than a gen- to achromatopsia. Higher-level recog- eral loss of vision constrained to a nition deficits can lead to diverse specific location in the visual field, types of general visual agnosia or a they cause a loss of a specific type of number of selective agnosias, includ- visual function that often is neither ing prosopagnosia, pure alexia, and localized nor limited to one part of the topographagnosia. In contrast, lesions field. of the dorsal occipitoparietal cortex Diverse types of visual functions are cause problems with spatial process- affected by extrastriate lesions, which ing, in what some view as a ‘‘where’’ are grouped into two broad families stream1 and others view as a focus on according to anatomic location and preparation for visually guided action.2 functional relationships.1,2 Lesions of The intermediate deficit here is

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Copyright © American Academy of Neurology. Unauthorized reproduction of this article is prohibited. KEY POINT akinetopsia, impaired motion process- find this unpleasant, as if things look dirty. h Cortical visual ing. High-level deficits are the compo- A partial defect is called dyschromatopsia. syndromes can be nents of Balint syndrome, including With dyschromatopsia, some color per- grouped into problems simultanagnosia, optic ataxia, and oc- ception remains, but the ability to with various types of ular motor apraxia, as well as distinguish one color from another is object recognition with astereognosis. reduced. For some patients, the world ventral occipitotemporal The lesions that cause the various takes on a specific tint. Rarely, patients lesions, and problems types of cortical syndromes discussed may report illusory spread of colors, in with spatial analysis and in this article are the usual suspects which an object’s color seeps out of its attention with dorsal for cerebral pathology, eg, stroke, boundaries. occipitoparietal lesions. tumors, and encephalitis. In most Color vision is processed by a cases, the temporal pattern of the network in the occipitotemporal cor- problem is the key to diagnosing the tex. Cerebral dyschromatopsia is asso- cause. For syndromes that are more ciated with bilateral lesions of the likely to emerge after bilateral lesions, lingual gyri5 (Figure 7-3); its severity such as achromatopsia or Balint syn- reflects how much of the cortical color drome, etiologies that can have bilat- network is lost.6 Unilateral lesions may eral effects should be considered. not cause a symptomatic deficit, but Thus, among the different kinds of when tested carefully, patients with stroke, postoperative watershed in- such lesions are shown to have farctions, embolic showers, and vascu- hemiachromatopsia, impaired discrim- litis would be suspects. Other causes ination of colors in the contralateral of bilateral lesions include posterior hemifield. reversible encephalopathy syndrome, An impairment of color perception multiple cerebral metastases, and her- is often associated with superior field pes simplex encephalitis. Patients with defects and other higher-order prob- a slower, progressive course of visual lems of recognition, such as proso- dysfunction may have posterior corti- pagnosia and topographagnosia. cal atrophy or the Heidenhain variant Not all color function is lost in of Creutzfeldt-Jakob disease. At the patients with achromatopsia; special other end of the spectrum from tests can show evidence of retained neurodegeneration, increased recog- red/green and blue/yellow color nition exists that some people are opponency that is based on processing born with a selective visual agnosia, by retinal ganglion cells. This residual as has been described, for example, in ability is likely responsible for the fact congenital prosopagnosia3 and devel- that such patients can perceive bound- opmental topographic disorientation.4 aries between areas of different colors, In some cases the deficit appears to but cannot identify what the respective run in families, suggesting an inherited colors are.7 Clinically, this can lead to genetic defect. the phenomenon in which they cannot read the Ishihara plates up close (at a SYNDROMES OF THE VENTRAL distance where they can see the dots, STREAM and, hence, the visible boundaries are Achromatopsia those between each dot and the white Acquired brain lesions can impair background), but can read the plates if color vision.5 Complete impairment they are far enough away that the dots is called achromatopsia, and patients merge, so that the only visible bound- with this condition see the world in aries are those between red and green grayscale (Case 7-1). Some patients regions.

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Case 7-1 A 41-year-old man awoke one day with a sense of distortion between the right and left halves of his vision, along with nausea and imbalance. A CT scan showed a left occipital infarction and a right vertebral arterial dissection. The next day in the hospital the patient had a right occipital infarction and noted many visual problems, which slowly improved over time. He had trouble recognizing faces, seeing their shapes, and identifying ethnicity and age of faces. Everyone appeared good-looking. He recognized people by their voices, clothing, physical posture, facial moles, or hairstyles. He could not visualize the faces of well-known actors when he heard their names. Initially the world appeared black and white, but later he saw some color tints, although he had trouble distinguishing colors that were similar to each other, such as blue and green. Although the patient was a sports car enthusiast, all cars looked the same to him. He could not recognize different buildings, which all looked like a ‘‘bunch of squares.’’ He had trouble navigating his neighborhood and got lost following a short but twisting route to the supermarket across the street. His memory for daily events was poor, causing problems. On examination, the patient’s visual acuity was normal, but he had bilateral superior altitudinal defects (Figure 7-1). The Farnsworth-Munsell color test showed severe difficulties with color discrimination (Figure 7-2). He recognized 47 of 50 words on the Warrington Recognition Memory Test but only 28 of 50 faces. Only 60% of celebrity faces were familiar, even though he recognized 100% of their names. He also performed poorly on a test of his ability to visualize the shapes and features of famous faces. MRI showed bilateral occipitotemporal ischemic lesions involving the lingual and fusiform gyri (Figure 7-3), and functional MRI confirmed the loss of both right and left fusiform face areas.

FIGURE 7-1 Goldmann perimetry of the patient in Case 7-1 showing bilateral superior altitudinal defects.

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Copyright © American Academy of Neurology. Unauthorized reproduction of this article is prohibited. Continued from page 924 Comment. This man had a typical history and findings due to bilateral occipitotemporal lesions, which caused the constellation of dyschromatopsia, prosopagnosia, topographic disorientation, and bilateral superior quadrantanopia.

FIGURE 7-2 Farnsworth-Munsell color test results of the patient with cerebral dyschromatopsia in Case 7-1. The black lines indicate the magnitude of the patient’s error for color sorting at each hue location. The greater distance away from the center of the disc, the greater the error. The patient has difficulty with all hues, and particularly with green and blue. These findings are consistent with the patient’s own observations from daily life.

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FIGURE 7-3 Axial and coronal T1-weighted MRI from the patient in Case 7-1 showing bilateral lesions of the fusiform and lingual gyri (arrows).

KEY POINT More sophisticated deficits of color defect may still be able to discern the h Cerebral dyschromatopsia perception can also be demonstrated broad categories of red and blue even is best diagnosed by tests in patients with achromatopsia. Color though they are impaired in discern- that require patients to constancy refers to the fact that an ing finer distinctions within those sort colored chips by individual’s perception of an object’s color domains. Also, in color anomia, either their hue or color remains stable even when the impaired naming of colors exists, saturation, rather than by lighting changes. This stability requires although color perception is normal. having patients name the visual system to estimate what the The best tests for achromatopsia colors. illumination must be from the general involve sorting colored chips for coloration of the entire scene and to their hue (redYgreen) or saturation discount that from the wavelengths of (redYpink), such as the Farnsworth- light emanating from the object. Munsell color test (Figure 7-2). ‘‘Discounting the illuminant’’ is a cortical computation that is inaccurate in General Visual Agnosia patients with dyschromatopsia.7 Patients with general visual agnosia Patients with achromatopsia may have trouble recognizing objects.8 still be able to read Ishihara plates, This is often particularly true if the so testing for achromatopsia requires image of an object is impoverished some care. Patients may be unable to (eg, a two-dimensional line drawing) name colors, but those with a partial and less so for real three-dimensional

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Copyright © American Academy of Neurology. Unauthorized reproduction of this article is prohibited. KEY POINT objects, although the latter can also this information to stored knowledge h A taxonomy of general cause patients difficulty. If the object about what objects look like or their visual object agnosia is they cannot name is made to emit a use. Further fractionating distinctions divided into apperceptive sound or given to them to touch, they have been proposed in a taxonomy of and associative variants, 9 will recognize it, showing that the agnosia. each with further problem is limited to vision. A number of types of apperceptive subtypes. Another important diagnostic con- visual agnosia exist. In visual form sideration is that the patient should agnosia, the ability to perceive the have sufficient basic vision (ie, visual shape of objects is impaired8;patients acuity and central visual field) to sup- may have difficulty identifying even port object recognition. Sometimes elementary geometric forms, eg, tri- diffuse visual deficits can mimic object angles and squares. Severity varies: agnosia. some patients see simple shapes but As with many complex functions, not more complex ones. Their difficul- object recognition involves a hierarchy ties likely stem from their inability to of processing stages and a network of see the basic building blocks of shape, occipitotemporal regions. A funda- such as curvature, surface, and volume. mental and traditional distinction lies If asked to copy a drawing of an object, between apperceptive and associative these patients fail miserably. This type forms of agnosia. Patients with apper- of visual agnosia has often been asso- ceptive visual agnosia are unable to ciated with carbon monoxide poison- form accurate visual representations ing, which likely causes a diffuse array of objects in their brain, and without of lesions affecting the occipital cortex, such information they cannot deter- as well as object-processing areas such mine what the objects are. Patients with as the lateral occipital cortex. It is also associative visual agnosia are able to seen with posterior cortical atrophy form fairly accurate visual representa- (Case 7-2 and Figure 7-4) and bilateral tions, but they have difficulty matching occipital ischemia.

Case 7-2 A 71-year-old woman reported that she had noted visual problems for several years. She had great difficulty finding things and tended to misidentify objects. She could recognize that a face was familiar, although she often could not recall the names of people. Reading was difficult for her even with large print, and she had trouble playing dominoes. She got confused while dressing; her husband often had to help her finish. She could walk her dog by herself along well-known paths in her neighborhood, but often did not recognize where she was when being driven in a car. On examination, her visual acuity was 20/20, but attaining this result required showing her one letter at a time. She identified a square and a circle, and said a triangle was a tent. She had more difficulty with three-dimensional shapes such as cubes and pyramids. From line drawings of objects she identified a chair but not a key, hammer, glasses, or glove. With real objects, she stated that a ruler was a thermometer, but when the ruler was placed in her hand, she realized it was a ruler. She knew that the ruler was used to draw straight lines, but did not know what edible product came from maple trees. When she viewed the cookie theft picture, she identified ‘‘a smaller woman on a ladder, the other woman looking out a window.’’ Her brain MRI showed diffuse atrophy of both the occipitotemporal and occipitoparietal cortex consistent with posterior cortical atrophy, a focal neurodegenerative form of dementia (Figure 7-4).

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Continued from page 927 Comment. This patient had an apperceptive problem that was manifest with slightly more complex three-dimensional drawings, and worse for line drawings of objects (eg, she mistook the chair in the cookie theft picture for a ladder). The patient had some deficits in semantic knowledge as well; these couldalsohaveaffected her object recognition.

FIGURE 7-4 MRI from the patient in Case 7-2, with visual agnosia. Axial fluid-attenuated inversion recovery (FLAIR) images show marked atrophy (arrows) of occipitotemporal (A)and occipitoparietal (B) cortex, more pronounced on the right.

Patients with integrative agnosia, on from unusual viewpoints; they may have the other hand, perceive shape reason- difficulty creating or using a mental ably well10; they can match similar representation of the three-dimensional shapes.Theycopydrawingsslowlyand shape of an object. Fortunately for these proceed painstakingly, part by part, but patients, this difficulty may not create can be relatively accurate. Their prob- toomanyproblemsinreallife. lem lies in linking or grouping the parts Among the associative visual agno- of an object to see the whole item, sias, in which knowledge about ob- especially if the object is large and jects is lost or rendered inaccessible, complex. These patients can get interesting distinctions can be made derailed by the intersections of lines in between knowledge of object form drawings with overlapping figures, and and knowledge of object utility. The they may not appreciate the incongru- latter can be probed by tests such as ities in impossible M. C. Escher figures the Pyramid and Palm Trees Test, and false animals created by joining the which requires that patients deter- parts of different beasts together. Like mine which two of three pictured visual agnosia, integrative agnosia can items are related (eg, hammer, screw- occur with posterior cortical atrophy or driver, hockey stick). A patient with bilateral occipital infarctions. associative visual agnosia has trouble Patients with transformation agnosia relating items with pictures, but can fail to recognize objects that are shown do so if told the names of the objects

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Copyright © American Academy of Neurology. Unauthorized reproduction of this article is prohibited. KEY POINT instead. Another interesting distinc- mantic deficit that is usually associated h 13 To diagnose prosopagnosia, tion is that recognition of living or- with anterior temporal lesions, not the examiner must show ganisms can be more affected than just prosopagnosia. that a patient does not that of inanimate objects. Associative To test face recognition, a clinician recognize faces either agnosia is linked to left or bilateral can use a famous faces test to probe for long known or recently lesions of the parahippocampal, fusi- long-term recognition.12 Patients are seen as familiar. The form, and lingual gyri.11 presented with images of celebrities patient should be familiar and anonymous people and asked with or even name the Prosopagnosia to indicate which faces look familiar. A person through other Prosopagnosia is the inability to rec- patient with prosopagnosia has reduced visual or nonvisual cues. ognize faces that were either previ- ability to make this distinction. If ously known to the patient or recently patients can state which faces are learned.12 Patients with prosopagnosia familiar but have trouble providing the learn to recognize people by other names belonging to those faces, the cues (Case 7-1). They can recognize diagnosis is prosopanomia, a much some faces by an unusual feature, rarer condition. such as a distinctive nose or mus- The problem with tests that use tache. They may also use other visual famous faces is that they assume that cues, such as hairstyle (although not the patient knows the celebrities, which entirely reliable because hair is easily maynotbethecaseforarecent changed), or body motion, such as a immigrant or a recluse. The validity of distinctive gait. Almost all patients the test can be verified by also report that they rely heavily on recog- presenting the patient with a list of nizing voices. The ability to glean names that includes the celebrities other sorts of information from faces already used in the famous face test, seems to vary among patients. This and having the patient indicate which information includes the ability to names are famous and which are not.12 perceive emotional expression in An alternate approach is to assess faces, the age or gender of the person, short-term recognition for faces by and attractiveness. showing a patient a series of faces, To diagnose prosopagnosia, the clini- and then, after an interval, presenting cian should first confirm, by administer- these faces again mixed with new faces ing a basic object recognition test, that and asking the patient which ones the patient does not have a general were seen the first time around. This visual agnosia. The Boston Naming Test is the strategy of the Warrington Rec- can be used for this purpose. Next, the ognition Memory Test, which has as a examiner should confirm that the pa- useful contrast a second component tient has preserved knowledge about that involves words rather than faces, people. If culturally appropriate, pa- and the Cambridge Face Memory Test, tients can be asked to give the occupa- which is available online. tions and biographic details of Prosopagnosia is caused by lesions of celebrities. Ideally, a voice recognition the fusiform gyri or anterior temporal test could verify the patients’ assertion lobe12; these are generally right or that they can recognize people by voice, bilateral (Figure 7-3 and Figure 7-5). but a standard test for this has not yet Unilateral left lesions are unusual and been developed. Patients who cannot tend to occur in left-handed patients. recognize voices or faces and have These findings are consistent with reduced semantic knowledge about functional neuroimaging results show- people have a multimodal person se- ing that the face-processing network is

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FIGURE 7-5 Axial MRIs of lesions in three different patients with prosopagnosia. A, T1-weighted MRI of a 58-year-old man who had a carotid dissection causing a right occipitotemporal infarction (arrow) because of a persistent fetal circulation pattern. B, Fluid-attenuated inversion recovery (FLAIR) MRI of a 20-year-old woman who had herpes encephalitis at age 10 and has bilateral fusiform lesions (arrows). C, T1-weighted MRI of a 30-year-old woman who presented with a seizure and confusion because of herpes encephalitis at age 25, which caused right anterior temporal encephalomalacia (arrow).

asymmetric, with greater involvement imagine the faces of two celebrities and of right hemispheric regions. answer a question about the faces, such As with general visual agnosia, sub- as which face is thinner or has the bigger types of prosopagnosia likely exist. An nose.15 Whether anterior temporal le- apperceptive variant is associated with sions cause a recognition impairment fusiform lesions.14 Patients with this that is truly face specific or also affects variant have trouble perceiving the voices has been questioned.13 complex three-dimensional geometry Is prosopagnosia really just about of the face, particularly in the eye faces? Can a lesion cause a perceptual region. This can be assessed with tests deficit that is so specific that it affects that require patients to match anony- only faces? This debate has been ongoing mous faces, particularly across changes for many decades. Some researchers in the point of view or lighting, as with claim to have identified patients who the Benton Facial Recognition Test or appear to be the holy grail of the field: the Cambridge Face Perception Test. By patients with pure prosopagnosia with contrast, patients with the associative/ completely intact recognition of objects amnestic variant have accurate percep- other than faces. This would be consis- tion and score well on those tests. They tent with the claims of some neuroimag- have difficulty matching what they see ing researchers that regions like the to what they know, however, because fusiform face area may be modules their facial memories have either been dedicated only to face processing. Others destroyed or disconnected from per- suggestthatprosopagnosiaismerelythe ceptual processing, which appears to be most dramatic example of the difficulty the case in patients with anterior tem- in seeing the fine and subtle distinctions poral damage. Clinicians can test the between different examples of the same status of facial memories with a face type of object. Thus, a patient with imagery test that requires patients to prosopagnosia may struggle telling not

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Copyright © American Academy of Neurology. Unauthorized reproduction of this article is prohibited. KEY POINT justonefacefromanotherface,butalso notice some improvement in the first h When tested for one car from another car and one dog few months if the problem was of recognition of objects from another dog. sudden onset, as with stroke. However, such as cars, patients Settling this debate is not easy. Given it rarely resolves completely. Ongoing with prosopagnosia the untidy nature of pathologic lesions, research efforts use perceptual learning tend to have difficulty if the trouble that a patient with approaches to try to improve face recog- their performance is prosopagnosia has differentiating vari- nition in patients with prosopagnosia. adjusted for their level ous cars can always be attributed to a of premorbid expertise. lesion that may have affected not just Pure Alexia (Alexia Without face-processing areas but adjacent cor- Agraphia) tex involved in perceiving other objects. Like face recognition, reading is a On the other hand, if a patient with highly developed expert skill in prosopagnosia passes a car recognition humans. The parallel is also anatomic: test, is that enough evidence to prove functional neuroimaging studies show normal perception of all other object that reading activates a network very categories?Inadditiontotheissueof similar to the one activated by face the number of various types of objects perception. The key difference is needed for testing to be confident on that the reading network depends this point, the vexing issue of prior more heavily on the left hemisphere patient expertise remains. The skill of and the face network depends more seeing fine differences between objects heavily on the right hemisphere. Just of the same type may depend on as the right fusiform face area is a experience; differentiating one type of dominant component of the face net- hawk from another by its shape may be work, the left visual word-form area is a trivial for a veteran bird watcher but key region for reading. Whereas lesions challenging for a novice. Adjustment for of the right fusiform gyrus cause premorbid expertise has rarely been prosopagnosia, lesions of the left fusi- done in studies of object recognition in form gyrus cause alexia. prosopagnosia. One study that did use a Alexia is the loss of prior reading skill. test with two phases first tested subjects Assessment of reading in these patients on their verbal knowledge about cars; must take into account their previous the assessment of their car expertise was reading competency. In pure alexia, used to adjust their scores on the second reading is the only verbal skill affected. phase, visual recognition of cars. The These patients can comprehend speech, results showed that most patients with converse with others normally, and can prosopagnosia recognized fewer cars even write. Other names for pure alexia than would be predicted from their include alexia without agraphia and pure verbal knowledge.16 word blindness. As with many things, Patients with prosopagnosia often purity is an ideal not often achieved in have other deficits. Those with fusi- real life. Some patients with alexia have a form lesions often have superior field mild degree of anomia. Detailed testing defects, topographagnosia, and of their writing shows that, while the dyschromatopsia if their lesions are dramatic problems with writing that are bilateral. Those with anterior temporal seen in alexia with agraphia are absent, lesions may have some amnestic de- most patients with pure alexia have what fects, although too mild to account for is known as surface dysgraphia.17 They their failure to recognize people. make spelling mistakes when writing Prosopagnosia is usually a per- irregular words such as yacht and manent deficit, although some patients colonel; these mistakes show that they

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KEY POINTS h Pure alexia may not be are guided by sound-to-spelling corre- mental dictionary but not the spelling entirely without a spondences rather than knowledge of rules. They can read regular or irregular degree of agraphia. the word, as if they had lost a mental words correctly but are unable to guess Patients with pure alexia dictionary in which they could look up how a made-up word they have never tend to make errors words with unusual spelling. seen before would be pronounced, as it when writing irregularly As a complex skill, reading depends does not have a mental dictionary entry. spelled words, indicating on the integrity of a number of other Deep dyslexia is more bizarre, as pa- a surface dysgraphia. processes. Before concluding that a tients make semantic errors when read- h Pure alexia is characterized patient who reports difficulty with reading, for example seeing the word piano by a marked word-length ing has pure alexia, the clinician should and reading it aloud as orchestra.At effect, with reading time evaluate for other conditions. Reading least one patient with alexia with determined by the may be impaired by ocular disorders agraphia from a parietal lesion showed number of letters in a that impair central vision in both eyes, this pattern in his reading.20 word: 160 milliseconds such as macular degeneration and cat- Pure alexia has a range of severity; an per letter is the diagnostic aracts, but these disorders should be extreme case was Monsieur C, a patient criterion separating pure evident by reduced acuity and depres- Dejerine describedwhocouldnotread alexia from hemianopic dyslexia. sion of the central visual field on even single letters. These patients are perimetry. Likewise, hemianopia that classified as having letter dyslexia. Other encroaches upon the central 5 degrees patients have apparently intact letter of vision can cause a hemianopic dys- identification but read slowly. A charac- lexia, particularly if the right hemifield is teristic feature of these patients is the affected.18 Impaired attention in patients high correlation between the time it with simultanagnosia or hemineglect takestoreadawordandthenumberof will disrupt reading. Patients with left letters in the word. In healthy individuals, hemineglect have a characteristic pat- the word-length effect is trivial, around tern of errors involving the left side of several milliseconds per letter. In patients words or the left side of pages, and with hemianopic dyslexia, it does not usually these attentional defects are exceed 160 milliseconds per letter,18 also apparent for other visual stimuli. while in alexic patients, it can be several Eye movements also play a key role in hundred to several thousand millisec- efficient reading. Unstable fixation be- onds per letter. Some patients even read cause of saccadic intrusions or nystagmus aloud each letter of a word before interferes with reading, as do inaccurate identifying the word; another term for saccades caused by cerebellar disease. this disorder is letter-by-letter reading. These ocular motor impairments should Even this strategy fails some patients; be evident on examination. despite having laboriously identified each While pure alexia is generally letter, they still cannot identify the word. regarded as a problem of visual process- Pure alexia is always associated with ing, some alexic syndromes reflect diffi- left occipitotemporal lesions. Previous culty with linguistic processing.19 These notions interpreted alexia as a discon- are most often described in neurode- nection syndrome. Since reading is generative conditions. Patients with dependent on centers in the left hemi- surface alexia have lost a mental lexicon, sphere, visual input to these centers can so they rely on grapheme-to-phoneme be disrupted by a combination of a left rules to read, which works fine if words occipital lesion causing right hemianopia are regular in spelling or even made up, and a callosal lesion disrupting transfer but not if words are irregular in spelling. of information from the intact right Patients with phonologic alexia have the occipital cortex. Indeed, some cases opposite problem. They have their exist in which disconnection seems

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Copyright © American Academy of Neurology. Unauthorized reproduction of this article is prohibited. the only plausible explanation of alexia; selective visual agnosia is an equally however, most patients have extensive plausible explanation (Case 7-3). In damage to the occipitotemporal cortex this view pure alexia is functionally in addition to possible damage to conceptualized as a damaged whole- callosal fibers. This often involves the wordYprocessing mechanism, so pa- fusiform gyrus, site of the visual word tients resort to reading each word form area. Hence, in many patients a serially by its component letters,

Case 7-3 A 41-year-old right-handed man awoke with numbness of the right side of his face and right leg and trouble speaking, all of which recovered over a few days. He had trouble finding the names of objects, but this ability also slowly recovered over months. He was left with a right hemianopia and trouble reading. He read letter by letter and did better with words related to his work and with vertically oriented text. He tried a number of strategies, including scrolling text and tracing letters, without much success. He could identify individual letters and easily distinguish them from other objects, and he could write well. He recognized familiar faces but had trouble retrieving the names of people. He also had difficulty recognizing his work tools until they were placed in his hand. Visual field testing confirmed a complete right hemianopia. He identified single letters quickly. Assessment of his reading of words showed good accuracy, but he was quite slow, taking on average 6.5 seconds to read a word. Testing of his word-length effect showed that he took an extra 1.5 seconds for every additional letter in a word. MRI showed a small left occipital lesion involving the region of the left visual word-form area (Figure 7-6).

FIGURE 7-6 Axial fluid-attenuated inversion recovery (FLAIR) (A), sagittal T1-weighted (B), and coronal T1-weighted (C)MRIof the patient with pure alexia in Case 7-3 showing the stroke in his left fusiform gyrus (arrows).

Comment. This man had pure alexia and right hemianopia. A right hemianopia alone can account for patients taking up to 160 milliseconds more for each additional letter in a word, but this patient’s word-length effect was 10 times that. His disorder was on the milder end of alexia since his ability to read single letters appeared to be preserved. Interestingly, he also had a subtle perceptual problem with other objects, namely his tools. This was consistent with the arguments advanced by some that alexia is not completely specific to words.

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KEY POINT h Getting lost can be the combined with variably damaged pro- imageoftheenvirons,acognitivemapof result of a number of cesses that encode those single let- the relationships of pathways, buildings, different problems, ters, which leads to letter dyslexia in and other landmarks to each other. This including the inability to extreme cases and very prolonged may be derailed if the ability to recognize recognize landmarks, word-length effects in the rest. landmarks is impaired. Landmark agnosia failure to form a As with faces, debate continues as to has been associated with medial cognitive map with whether the alexic defect is specific for occipitotemporal lesions, particularly on these landmarks, or reading. In the past, reports noted that the right, and may account for many cases poor orienting of some patients also had problems reading of topographagnosia that accompany oneself to the musical notation or map symbols. A new prosopagnosia (Case 7-1). Functional environment. review suggests that reading of numbers imaging shows that images of buildings is affected in most patients.21 Also, recent and places activate a region just medial studies show subtle perceptual deficits in to the fusiform face area called the alexic patients,22 even for faces.23 Again, parahippocampal place area. The diffi- it remains uncertain whether these defi- culty with recognizing landmarks fol- cits are related to the mechanism causing lowing lesions in this region can be the alexic defect and therefore inextrica- considered another type of selective bly linked to it, or merely associated visual object agnosia. As with faces, this through damage to neighboring cortex. can be tested by seeing if patients can Alexia is often persistent, but the few recognize images of famous places or, longitudinal studies that exist show that more informally (although perhaps bet- after sudden onset, the deficit can im- ter), with images from their own town. prove substantially. In particular, improve- On the other hand, it is possible for ments can be seen in the word-length patients to recognize landmarks but have effect. A number of rehabilitative ap- trouble encoding the spatial relationships proaches have been tried,24 some em- betweentheminthecognitivemap.This phasizing letter identification, others trying can now be tested with computer simula- to force whole-word recognition instead tions, some of which are available online of the letter-by-letter strategy. These ap- (www.gettinglost.ca). Cognitive map for- proaches can improve reading speed, mation and its use are associated with although with variable transfer to words activity in the hippocampi and retro- that were not part of the training set and splenial cortex. A deficit in form- with variable effects on the word-length ing cognitive maps may account for effect. In general, it appears that training some cases of developmental topographic must continue for 6 months or more for disorientation, a recently described any improvement to ensue. congenital form of selective agnosia.26 One can also navigate without a Topographagnosia mental map by using a sequence of Patients with topographagnosia get lost moves, much like following verbal di- in familiar surroundings. As with all rections after stopping at a gas station complex tasks, multiple cognitive skills (eg, go three blocks and turn right, are involved in orientation and route then left again after one block). Such finding. Furthermore, navigation prob- directions are not as useful as a cogni- lems may be solved in a number of ways. tive map because they are not helpful if Thus, it is not surprising that topographic one deviates from the prescribed path. disorientation encompasses a family of This type of navigation requires a sense disorders with different origins.25 of how one is oriented spatially relative The most flexible and useful means of to the environment; loss of this ability navigation is the formation of a mental is called egocentric disorientation.25

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Copyright © American Academy of Neurology. Unauthorized reproduction of this article is prohibited. It is not known whether it is possible to independent processing networks to improve the navigational deficits of that have in common a spatial analysis patients with topographagnosia through of vision. The fact that these deficits can training. Fortunately, smartphones with occur together indicates that their net- global positioning system capability pro- works are in proximity. The traditional vide these patients with an easy, avail- definition should be expanded to in- able substitute strategy. clude other notable consequences of dorsal lesions, such as astereognosis and smooth pursuit deficits. SYNDROMES OF THE DORSAL Diagnosing Balint syndrome requires STREAM first and foremost careful perimetry to Akinetopsia establish that the patient’s loss of vision Motion perception was one of the first is not responsible for the lack of aware- selective visual functions localized to a ness of objects, misreaching, or failure to specific cortical area, namely the mid- make accurate saccades to objects. This dle temporal area, or visual cortical isnotalwayseasy;itrequiresasetting area 5 (V5). Not long after, there was a free of distraction and an examiner with report of a patient who had impaired patience. A patient with only a keyhole motion perception and bilateral le- of central vision remaining after bilateral sions of the lateral occipitotemporal striate lesions can behave very much like cortex, which presumably destroyed a patient with Balint syndrome. The the human homologues of V5.27 For impact of disturbances of attention, this patient, water poured from a spatial localization, and action guidance pitcherseemedtobefrozenand can be extremely disabling (Case 7-4), as objects appeared to jump rather than is also described in an account of the life move; the patient also had trouble of two patients with Balint syndrome.29 judging the approach of oncoming cars. A second patient with similar Simultanagnosia symptoms and similar lesions was later Simultanagnosia is a deficit of spatial found. No other patients have since attention.30 Primarily it is a limitation in surfaced, however, underscoring the capacity; it is classically defined as a extreme rarity of this condition in its failure of the ability to pay attention to full-blown bilateral variant. Patients more than one object at a time. When a with unilateral lesions have been de- display contains two items, the patient scribed28 but are usually asymptomatic, with simultanagnosia may be aware of requiring specialized computerized only one, even if both are located in the motion tests to demonstrate their same place. If the examiner holds up a impairments, which are localized to pen placed on top of a finger, the patient the contralateral hemifield. may be aware of the pen but not the finger. The lack of awareness in this Balint Syndrome condition can be as disabling as blind- The classic formulation of Balint syn- ness: patients bump into things when drome is the triad of simultanagnosia, walking, struggle with reading, and cer- optic ataxia, and ocular motor apraxia tainly should not drive. Their limitation caused by bilateral occipitoparietal le- makes searching for objects difficult. sions. However, these components are Patients also have trouble sustaining only loosely associated. Each can be attention over large displays with many found in patients without the others, items. A classic test is the starry night indicating that they result from damage display, where small bright dots appear

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Case 7-4 A 49-year-old woman was referred because of visual difficulties. Three months earlier she had experienced simultaneous bilateral strokes (Figure 7-7) due to primary cerebral angiitis. Visual field testing during her hospitalization showed a left inferior quadrantanopia. After discharge from the hospital she had trouble seeing multiple objects in photographs on pages of books, and both arms were initially very clumsy in reaching for items in the right or left hemispace. The clumsiness of her right arm improved within several weeks, but she still felt her left arm was not functioning quite right when she tried to use utensils. She had so much trouble stumbling into things while walking that she had to use a wheelchair. On examination, her visual fields were normal. She had trouble relating the items of the cookie theft picture to one another. In line drawings she could identify a key, a glove, a chair, and a cactus. When shown a picture of a baby face, she reported seeing only the eyes. She was able to recognize famous faces. She read short sentences of small words well, but with longer sentences had trouble maintaining the words in their correct sequence. She read the word phantom correctly, but when asked to read its letters, she omitted the a and the n. When shown Navon letters (Figure 7-8) she often did not see the global letter, although she always reported the small local letters. When shown Arcimboldo pictures, she knew that the images depicted faces but did not realize that the faces were made up of other objects, such as fruits or vegetables. Her reaching for objects was erratic, and she did not align her grasp to the orientation of the object. Comment. This patient displayed classic problems with reaching to visual objects, seeing multiple objects simultaneously and relating those objects to each other correctly in space, as demonstrated in her reading. She also showed both local and global capture.

FIGURE 7-7 Axial fluid-attenuated inversion recovery (FLAIR) MRI of the patient with Balint syndrome in Case 7-4 showing bilateral lesions in lateral occipital and parietal cortex.

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FIGURE 7-8 Examples of stimuli with global and local elements. A, a Navon letter with sparsely distributed Ws that at the global level form an F. A patient with Balint syndrome sees only the Ws. B, an Arcimboldo painting of a face composed of vegetables. The patient with Balint syndrome reports the face but not the vegetables.

or disappear in random locations; pa- capture.32 When the global form is tients with simultanagnosia struggle to strong, as with the faces that are detect these occurrences.31 composed of vegetables or other items The reduction in attentional capacity in Arcimboldo pictures (Figure 7-8), of patients with simultanagnosia is patients may report seeing only the accompanied by a lack of flexibility in faces, but not the vegetables, which is an shifting attention. This is reflected in example of global capture.32 Healthy the phenomena of local and global individuals have no difficulty moving capture. Some stimuli have both local between the local and global frames to and global structures. A typical example see the forms present in both, but is the Navon letter, in which small local patients with simultanagnosia tend to letters are grouped so that they make have difficulty at one or the other level. up a large global letter (Figure 7-8). To diagnose simultanagnosia, the cli- When the global form is weak because nician simply needs displays that have the local letters are few and far be- multiple elements and to ask patients to tween, patients with simultanagnosia report what they see. The cookie theft report seeing the small local letters picture from the Boston Diagnostic Apha- only, which is an example of local sia Examination is commonly employed

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KEY POINTS h Attention in (but probably could use updating). Other spatial coding that may be simultanagnosia is Simultanagnosia is linked to lesions of defective includes the assessment of characterized both by the medial occipitoparietal junction, the orientation of objects in space and reduced capacity, cuneus, and intraparietal sulcus, as well in relation to oneself. If asked to grasp causing failure to detect as a number of white matter tracts linking an object with a dominant long axis, multiple stimuli, and a visual attention network.33 such as a pen, patients with optic lack of flexibility, ataxia may fail to orient their grasp to causing difficulty seeing Optic Ataxia match the axis of the object. both the trees and the Optic ataxia refers to inaccurate reaching Poor spatial coding may not be the forest simultaneously. to targets under visual guidance. Unlike only localization problem in these h Balint syndrome may patients with cerebellar ataxia, patients patients. One study showed that local- include problems not withopticataxiashouldbeabletoreach izing events in time can also be only localizing objects to targets whose spatial coordinates are affected. For example, a patient was in space, but also derived from other senses, eg, reaching shown a square, a triangle, and another localizing them in time. parts of their own bodies. This is not triangle in sequence and could not tell always the case, however; in some whether the square had been the first, patients reaching can be inaccurate to second, or third in the sequence, even somatosensory targets such as parts of though the patient could report how theirownbody.Thisisnotsurprising many squares and triangles had been given that the parietal cortex contains shown. It was proposed that the regions that perform multimodal spatial patient had trouble assigning the cor- computations. Optic ataxia is likely the rect temporal ‘‘location’’ or epoch to result of degraded analyses of the posi- each stimulus, which was called se- tion of objects in space. Patients with quence agnosia.35 Balint syndrome therefore also have The occipitoparietal lesions that trouble judging how far apart objects cause optic ataxia likely involve the are from each other. Functional neuro- junction between the inferior parietal imaging provides evidence that these lobule and the superior occipital cor- computations involve the inferior parie- tex.36 Similar deficits have been tal lobule. Misreaching with either limb reported with lesions of the premotor results from bilateral lesions, but a cortex and occipital-frontal white mat- unilateral lesion may cause misreaching ter connections, however. with only the contralateral arm or only for visual targets in the contralateral Acquired Ocular Motor Apraxia hemifield. Tests for optic ataxia should Bilateral lesions can also cause a therefore assess accurate pointing to defect in the initiation and guidance objects to the right or left of center and of saccades to visual targets. When with the right and the left hand. In severely affected with acquired ocular particular, reaching may be more im- motor apraxia, patients may have paired for targets seen in the peripheral difficulty generating any saccades to a rather than the central visual field.34 visual stimulus on command, although Having the patient reach without on occasion saccades can be facilitated by looking directly at the object may be a blink; this difficulty is sometimes called a more sensitive, although less natural, psychic paralysis of gaze. A target that test for optic ataxia. The deficit is also suddenly and unexpectedly appears may more specific to rapid reaching for still trigger a reflexive saccade. If the objects and may not be apparent if defect is less severe, the patient may the patient is allowed to delay reaching merely take longer than expected to for a few seconds. make a saccade to a target. This delay

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Copyright © American Academy of Neurology. Unauthorized reproduction of this article is prohibited. KEY POINT can be accentuated if the object at which These pursuit defects are asymptomatic h The ocular motor the patient was initially looking when the and detected only by close observation deficits with target appeared remains visible. Some or ocular motor recordings. occipitoparietal lesions 37 refer to this as spasm of fixation. In the include difficulty with mildest of cases, prolonged saccadic Astereognosis initiating saccades, latencies may be apparent only with accurate targeting of Perception of the position of objects formal ocular motor recordings. saccades, and accurate in depth is another type of spatial com- In addition to problems with initia- matching of eye to putation. The most well-known pro- tion, the saccades of patients with target speed during cess that is involved in depth percep- acquired ocular motor apraxia may be smooth pursuit. tion is stereopsis. Two objects located inaccurate, reflecting, as with optic at different distances from the observer ataxia, a deficit in obtaining the correct have a different relationship to each coordinates of visual objects in space. other in the retinal image of the right In severe cases, the eyes may appear to versus the left eye. The power of this wander until they stumble upon the depth cue can be appreciated by trying object; even then they may fail to stay to thread a needle with one eye closed with the object, demonstrating an and then with both eyes open. Loss of impersistence of gaze. As a result, these stereopsis can occur with bilateral patients have chaotic eye movements occipitoparietal lesions,39 and can be when searching for objects.37 demonstrated with common tests of Ocular motor apraxia is associated stereovision used in eye clinics, such with bilateral lesions of the parietal eye as the Titmus stereo fly test or Randot fields, the frontal eye fields, or both.38 A Stereo Test, which require the patient severe inability to make any saccades to wear polarized glasses and present can improve with time, particularly if the slightly different images to each eye. lesions do not involve both the frontal Stereopsis is not the only cue to and the parietal regions. Unilateral pari- depth relationships, to which any one- etal lesions are unlikely to cause symp- eyed person or painter can attest. tomatic deficits, but ocular motor Relative size and saturation are strong recordings can show similar deficits in pictorial cues to distance; moving one’s a patient’s planning and guidance of head can give depth cues from optic saccades in the direction contralateral to flow patterns and motion parallax. It is the lesion. not known whether the cerebral lesions Although saccades dominate the dis- that cause astereopsis also affect the cussion about ocular motor apraxia, ability of a patient to derive depth from smooth pursuit is often also defective these monocular cues. in these patients because cortical areas involved in generating smooth pursuit are adjacent to the parietal and frontal CONCLUSION eye fields. These regions occupy the Deficits of cortical visual function are medial superior temporal sulcus and unusual but varied and intriguing. the fundus of the arcuate sulcus in They are important because they offer monkeys. Unilateral lesions of these opportunities to study how the brain structures in humans can lead to re- makes sense of the visual world. This duced pursuit of targets moving toward review provides a framework for under- the side of the lesion, and sometimes standing and categorizing these different even excessive pursuit (ie, the eye types of deficit, as well as for understand- moving faster than the target) for ing and utilizing the diagnostic measures targets moving in the other direction. and insights gained in recent years.

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