Neuropsychologic assessment of visual disorders

Neurol Clin N Am 21 (2003) 387–416 Neuropsychologic assessment of visual disorders Margaret Lanca, PhDa,*, Beth A. Jerskey, MAb, Margaret G. O’Connor, PhDc a Department of Psychiatry, Harvard Medical School, Boston, MA; Department of Psychiatry, The Cambridge Hospital, Cambridge, MA, USA b Center for Clinical Biopsychology, Boston University, Boston, MA, USA c Department of Neurology, Harvard Medical School, Boston, MA; Division of Behavioral Neurology, Beth Israel Deaconess Medical Center, Boston, MA, USA In this article, the authors focus on the neuropsychologic assessment of patients who present with visual difficulties in the clinical setting. This type of evaluation often is requested to assist with differential diagnosis and to obtain information regarding the functional implications of a patient’s visual problem. Several neurologic conditions affect brain structures that mediate higher-order visual processes. Some cases of visual difficulties occur in the context of diffuse brain damage, whereas others are the result of focal insult or injury. Information regarding the nature and severity of the visual problem may help establish a diagnosis of dementia, the prototype of diffuse injury. Deficits in the analysis or construction of visual stimuli may emerge early in the course of dementia, in which case they are associated with other cognitive deficits and diffuse neuropathology. A detailed neuropsychologic assessment may distinguish between forms of dementia. Visuospatial abilities may be disproportionately affected in patients with Lewy body disease, whereas visual abilities may be relatively preserved early in Alzheimer’s disease (AD) [1]. Aside from dementia, other neurologic disorders, such as cerebrovascular accidents, may have circumscribed damage to occipital and temporal brain regions that result in focal visual disturbances. In these disorders, investigation of the cognitive and perceptual characteristics of the visual problem may elucidate the locus of the brain lesion. In addition to * Corresponding author. The Cambridge Hospital, Department of Psychiatry, Macht Building, 1493 Cambridge Street, Cambridge, MA 02139. E-mail address: margaret_lanca@hms.harvard.edu (M. Lanca). 0733-8619/03/$ - see front matter Ó 2003, Elsevier Inc. All rights reserved. doi:10.1016/S0733-8619(02)00109-3 388 M. Lanca et al / Neurol Clin N Am 21 (2003) 387–416 providing information regarding the neural substrates of a visual problem, careful assessment of the patient’s visual abilities provides valuable information about the patient’s functional status, capacity for independence, and rehabilitative potential. Formal neuropsychologic testing begins with a survey of a broad spectrum of cognitive and perceptual domains. Assessment of intelligence, attention, memory, and language skills allows the examiner to understand the significance of the visual problem relative to other abilities. A profile of strengths and weaknesses emerges that is of diagnostic value and serves as a guide for remediation. The clinical assessment of visual problems is embedded in this comprehensive examination geared toward identifying the critical components of the visual deficit and probing associated deficits, some of which may exacerbate the visual problem. One of the primary goals of the evaluation is to obtain a detailed description of how the patient experiences the visual problem in everyday life. This description subsequently influences the tests that are chosen in the evaluation. During the interview portion of the assessment, the medical history is reviewed and data from previous evaluations are considered. Of particular relevance is information from ophthalmologic examinations regarding fundamental aspects of visual processing (eg, stereopsis, color perception, form perception, movement detection, and so forth). This information provides the backdrop for further assessment of problems that affect more complex attributes of visual representations. Neuroanatomic studies with humans and nonhuman primates suggest that different neural systems subserve object recognition, object location capacity, and constructional skills [2]. In light of these investigations, neuropsychologists have classified visual tasks according to the extent of perceptual, spatial, or constructional processes involved in task performance [3]. The authors use this framework in reviewing the tests used in the clinical setting. As per the Benton and Tranel classification schema, visuoperceptual tests selected for review focus on the analysis, synthesis, and identification of visual stimuli. Visuospatial tests concentrate on spatial location, perception of direction and distance, and visual neglect. Visuoconstructive tests focus on the ability to draw or assemble visual stimuli in accordance with a specific design or mental image. Finally, tests of visual attention and visual memory are discussed. In this article, a small sample of tests used for clinical assessment is reviewed. Table 1 lists the measures reviewed and the visual domain under which they fall. Case examples are presented under each major domain. In some cases, the use of a qualitative, process approach to scoring is more helpful in forming a diagnostic impression and detecting localization [4]. Examples of this approach are highlighted in subsequent sections. The effects of visuoperceptual disorders on reading are not addressed in this article. The interested reader should consider the following reading tests that often are included in neuropsychologic evaluations: subtests from the M. Lanca et al / Neurol Clin N Am 21 (2003) 387–416 389 Table 1 Sample of tests used for clinical assessment Tests of visuoperception Tests of visuospatial abilities Benton Visual Form Discrimination Test Line Bisection Test Hooper Visual Organization Test Mesulam’s Cancellation Test Embedded Figures Test Bell’s Test or Visual Neglect Test Visual Object and Space Perception Battery Benton Judgment of Line Orientation Test Benton Facial Recognition Test Visual Object and Space Perception Battery The Eyes Test Tests of visuoconstruction Tests of visual attention and memory Bender Visuonator Gestalt Test Spatial Span Test Clock Drawing Test Visual Reproduction Test Rey-Osterrieth Complex Figure Test Ruff Figural Fluency Test Block Design Test Spatial Working Memory Test Object Assembly Test Object Working Memory Test Biber Figure Learning Test Warrington Recognition Memory Test Boston Diagnostic Aphasia Examination [5], which provide information regarding single letter reading, word reading, and paragraph comprehension, and the Woodcock Johnson Reading Test [6] and Wide Range Achievement Test [7], which are valuable tools for assessment of reading strategies with single words and longer passages. Reading comprehension and reading speed are assessed with many tests including the Nelson-Denny Test [8]. Many of these measures are multifactorial and may not test a single component of visual functioning. One caveat to this is that no single test score, in isolation of the patient’s history or other test scores, should be used to make a clinical impression. Assessment procedures Visuoperceptual tests of object recognition Deficits in visual analysis and synthesis for object recognition occur for several reasons. Causes may include diminished visual acuity secondary to peripheral factors and perceptual problems that are the result of damage to cortical structures that mediate vision. If the patient has difficulty analyzing the perceptual features of a given stimulus, he or she is at a deficit in many other parts of the visual examination. There are some neurologic conditions, such as Balint’s syndrome, where perception of parts of stimuli is intact but the individual has difficulty integrating the visual details. In other conditions, such as visual agnosia and prosopagnosia (see articles elsewhere in this issue and later discussion in this article of case studies DM and KT), analysis and synthesis may be intact but the recognition of particular items (such as objects or faces) may be impaired as a result of the patient’s inability to access previous representations. 390 M. Lanca et al / Neurol Clin N Am 21 (2003) 387–416 Some of the tests presented in this section focus on the perception of single features of a stimulus, whereas others focus on the integration of perceptual elements for the purposes of identification or recognition. In some tests, the individual is asked to identify a stimulus; other tasks require the individual to associate the perceived stimulus with a previously stored memory. In light of research findings indicating that different brain regions mediate the perception of objects versus faces, these types of stimuli are examined separately. Benton Visual Form Discrimination Test The Benton Visual Form Discrimination Test focuses on the visual analysis of 2-D line drawings. The patient is asked to match 16 geometric figures to identical figures embedded in four foil stimuli [9]. Distracter stimuli differ from the target by small variations of displacement, rotation, or distortion. Normative studies indicated that the majority of control subjects obtain high scores on this test. One study found that in an older population (ages 55 to 97), age and education but not gender were significantly associated with test performance in subjects without neurologic concerns [10]. Because test performance is dependent on intact perception, visual scanning, and object recognition, poor performance may be indicative of lesions in many regions of the brain, including parietal and temporal lesions; patients with bilateral-diffuse brain damage also demonstrate increased deficits on this task [11]. Hooper Visual Organization Test An exemplary illustration of the multifactoral nature of some neuropsychologic tests is provided by the Hooper Visual Organization Test [12]. This test not only requires visuoperceptual differentiation and conceptual reorganization of object pieces, but also the correct naming of the integrated object. Administration consists of 30 drawings of common items that have been broken into two or more parts (Fig. 1). The patient is required to reconstruct the object mentally and then name it. Scoring is simply the total number of correctly identified objects, although some items receive half credit for partially correct responses. Test-retest reliability is moderate [13]. Construct validity studies have found high correlations between performance on the Hooper and perceptual organization subtests of the Weschler Adult Intelligence Scale–Revised (WAIS-R [14]) and object naming ability [15]. Patients with various brain lesions can perform poorly on this test partly as a result of the multiplicity of task demands (eg, focus on features, contour, hemiattentional space, and overt verbal response). Therefore, it is important to examine the types of errors patients make. For example, patients with right-hemisphere damage are prone to part and nonintegrated errors. A prototypic response of someone with a visual neglect is that the first image in Fig. 1 is ‘‘a flying duck’’ based on the fact that the tail of the fish (the correct identification) in the upper right side of the figure resembles M. Lanca et al / Neurol Clin N Am 21 (2003) 387–416 391 Fig. 1. Three items from the Hooper Visual Organization Test. (From Hooper HE. The Hooper Visual Organization Test. Beverly Hills (CA): Western Psychological Services; 1958; with permission.) a head of a duck, whereas the head of the fish is in the left hemiattentional field [4]. Patients with left-hemisphere damage make more language-based errors. Schultheis and colleagues found that anomic subjects achieved a significantly greater number of correct responses on a multiple-choice version of the Hooper as opposed to the standard administration and that overall performance was greatly improved when the object naming demand was reduced [16]. Embedded Figures Test Also known as the Hidden Figures Test and Figure-Ground Test, the Embedded Figures Test (Fig. 2) is used to examine visual identification of figures presented in a complex background. The primary version of this test consists of 16 figures that are presented on the left half of a page [17]. On the right half of the page are complex designs in which the target figure is embedded. Patients are asked to search for and trace the target figure. Timing and accuracy are measured. Normative studies reveal that healthy adults are adept at performing this task and there are no effects of gender on task performance [17]. Lesion analytic studies show that patients with righthemisphere damage perform more poorly than patients with left-hemisphere damage on this task [18]. Other studies indicate that patients with anterior lesions perform better than patients with posterior lesions when there is no time constraint [19]. Patients with diffuse damage, such as AD, also may have difficulty with this test underscoring that this test, like others, is dependent on several cognitive abilities (eg, attention) and object identification [20]. Visual Object and Space Perception Battery The Visual Object and Space Perception Battery [21] comprises nine subtests, four of which focus on the perception and identification of letters and visual line drawings. Each of these four tests assesses a particular 392 M. Lanca et al / Neurol Clin N Am 21 (2003) 387–416 Fig. 2. Sample items from the Embedded Figures Test. (From Spreen O, Benton AL. Embedded Figures Test. Victoria (BC): Neuropsychological Laboratory, University of Victoria; 1969; with permission.) dimension of visual perception while minimizing the involvement of other cognitive skills. Hence, these tests can be used with patients who have aphasic difficulties or other problems that sometimes intrude on test performance. The Incomplete Letters Test examines perception of degraded letters. Validity studies show that patients with right posterior lesions have particular difficulties with regard to this type of task [21]. The Silhouettes Test focuses on the ability to recognize common objects (ie, animals and objects) that are presented in unusual, noncanonical views. Studies of this test reveal that patients with right-hemisphere lesions have greater difficulty identifying objects and animals than do patients with left-cerebral lesions or nonlesion control participants [21]. The Object Decision Test requires the patient to identify objects that are presented in a 2-D, silhouette fashion. The Progressive Silhouettes is similar to the previous tasks in that it requires the patient to recognize a common object that is presented from an unusual 90-degree angle and with few distinctive features. The distinctive features of the object emerge over sequential images until the patient is able to M. Lanca et al / Neurol Clin N Am 21 (2003) 387–416 393 recognize the object. The tenth and final image is presented from a lateral perspective that is easily recognized. Studies show that patients with rightcerebral brain damage perform more poorly on this task than do patients with left brain damage [21]. Benton Facial Recognition Test The Benton Facial Recognition Test examines a patient’s ability to discriminate facial features by requiring a patient to match target faces with faces in which clothing and hair have been shaded out. The original test consists of 22 stimulus cards and requires 54 matches (Fig. 3). The patient is asked to match a front-view face with either an identical front-view face, a three-quarter front-view face, or a front-view face with different lighting Fig. 3. Three items from the Benton Facial Recognition Test. (From Benton AL, Hamsher K, Varney NR, Spreen O. Contributions to neuropsychological assessment. New York: Oxford University Press; 1983; with permission.) 394 M. Lanca et al / Neurol Clin N Am 21 (2003) 387–416 conditions. The first six items require only single responses, and the subsequent 16 items require three matches to each stimulus face. Normative studies show that increased age and lower educational status have adverse effects on test performance. Hemineglect related to parietal lesions may have an adverse effect on recognition and may negatively affect a patient’s score on this test. Temporal lobe regions, however, are more commonly implicated in performance on this task. Imaging studies show the importance of right inferior occipitotemporal region for face recognition [22]. This test in conjunction with the Warrington Test (addressed later), which measures facial memory, can give rich information about the patient’s ability to recognize and recall facial features. The Eyes Test There are several tests that focus on visual perception of emotion. One of these, the Eyes Test, requires the individual to perceive and determine the emotional expression of facial features that have been abstracted from larger photographs [23,24]. A series of 25 photographs of the eye region of a human face is presented. Each photograph has a different expression (eg, pensive, playful, or indecisive,) and the patient is asked to choose one of four words that best describes what the person in the photograph is thinking or feeling (Fig. 4). Normative research has shown that gender affects performance: women perform better on this task than do men. Adults with highfunctioning autism or Asperger’s syndrome have difficulty on this task. A functional MRI (fMRI) study revealed amygdala activity during task performance in nonimpaired control participants, whereas amydgala activity was not observed in autistic participants [25]. Case study: patient DM DM presented with visual processing problems in the context of a right occipital hemorrhage in November 1999. Evacuation of the hematoma revealed evidence of tumor, which subsequently was treated with radiation Fig. 4. An item from the Eyes Test. (From Baron-Cohen S, Wheelwright S, Hill J, et al. The ‘‘Reading the Mind in the Eyes’’ Test revised version: a study with normal adults, and adults with Asperger syndrome or high-functioning autism. J Child Psychol Psychiatry 2001;42(2): 241–51.) M. Lanca et al / Neurol Clin N Am 21 (2003) 387–416 395 and chemotherapy. Residual symptoms included a left hemianopia, which undermined spatial navigation and reading. He was unable to recognize people and buildings, even those with which he had been familiar in the past. Imaging studies (Fig. 5) showed an extensive medial occipital lesion extending towards the posterior temporal lobe with some white matter changes. Lesions also were noted in lingual and fusiform gyri, which may have accounted for his prosopagnosia. Evaluation findings revealed that DM was of high average to superior intelligence. His verbal intelligence quotient (VIQ) was 111. In contrast, nonverbal perceptual abilities were impaired leading to a performance intelligence quotient (PIQ) that was below average (PIQ = 70). The magnitude of the discrepancy between his VIQ and PIQ is consistent with right-hemisphere brain disease. Performance on tasks of visuoperceptual abilities revealed salient deficits. Assessment with Goldman perimetry confirmed evidence of a left hemianopia. There was no evidence of visual neglect on a letter cancellation task (discussed later), but DM needed to frequently readjust his field of vision in order to see all of the targets. Face perception and line orientation detection were impaired on the Benton tasks (face perception: 32/54, <percentile; detection of line orientation: 13/30, <1.5th percentile). DM had a great deal of difficulty with tasks from the Visual Object and Space Perception Battery (see later discussion). Consistent with a right medial temporal lesion, there was evidence of a material specific memory problem. His recognition of words was superior (49/50), whereas facial recognition was almost at chance (30/50; <percentile). Recall of orally presented short stories was superior (99th Fig. 5. Brain imaging study of patient DM. 396 M. Lanca et al / Neurol Clin N Am 21 (2003) 387–416 percentile), but recall of visually displayed stimuli fell in the borderline impaired range (fifth percentile). Visuospatial and hemineglect tests Previous studies have shown that object location is mediated by different neural systems from those involved in object recognition [2]. In this section, tests that focus on components of spatial analysis are presented. The first few tests are concerned with the phenomenon of hemispatial neglect, a problem that typically emerges in the context of right cerebral damage. Subsequently, tests focusing on the detection of spatial location, direction, and distance are reviewed. Patients with left-hemisphere damage may demonstrate difficulties with spatial analysis; however, damage to right cerebral structures is considered more problematic in this aspect of visual processing [26,27]. Another aspect of space perception, topographic orientation, may also decline in the wake of damage to right cerebral brain regions. A review of the literature did not find specific clinical tests that measure topographic orientation in real space. Consequently, tests that focus on this aspect of visual perception are not reviewed in this article. Line Bisection Test The Line Bisection Test is used to assess visual neglect by requiring patients to bisect lines of varying lengths (Fig. 6) [28]. Performance is evaluated by measuring the extent to which the patient’s bisection deviates from the actual midpoint of the line. Short lines are less likely to elicit a deviation from the center than long lines [29]. Patients with visual field defects and neglect make the greatest errors, usually by underestimating the side of the line opposite to the defective field [30]. Barton and Black found that hemianopic patients without neglect bisect the line biased in the Fig. 6. The Line Bisection Test. (From Schenkenberg T, Bradford DC, Ajax ET. Line bisection and unilateral visual neglect in patients with neurologic impairment. Neurol 1980;30:509–17.) M. Lanca et al / Neurol Clin N Am 21 (2003) 387–416 397 direction opposite to that seen in neglect [31]. Although this test is useful for assessing visual neglect, for many patients with right-hemisphere lesions, multiple trials of the test are important because neglect does not necessarily appear on every trial. One recent study by Ferber and Karnath found that the line bisection test missed 40% of their neglect patients, while the Letter Cancellation Test and Bell’s Test (see later discussion) missed identifying only 6% [32]. Test-retest correlations for this test version are high [33]. Mesulam’s Cancellation Test Developed by Mesulam [34], this test is used to assess visual neglect and visual scanning abilities by requiring patients to pick out target stimuli in a visual array. There are four conditions, two of which focus on scanning for shapes and two of which focus on scanning for letters. Items are arranged either in organized columns and rows or they are displayed in a random fashion. Patients’ performances are analyzed with respect to the number and distribution of items identified in the four quadrants of the page. Mesulam recommended that the patient be given a different colored pencil after every 10 targets in order to document search strategy. A study by Uttl and Pilkenton-Taylor investigated various letter cancellation tasks in a sample of healthy adults between the ages of 18 and 91 years [35]. The results of this research showed that there was a large age-related decline in the speed of the letter cancellation performance and no age-related differences in the spatial distribution of cancellation errors. Mesulam [34] demonstrated that patients with right-sided lesions tended to begin on the right side of the page or in the center of the page and used a more random search strategy. Patients with left-hemisphere lesions typically start on the left side, systematically scan, and, even in the presence of right visual field cut, still cancel target items on the right side. These patients also tend to be more accurate and faster at detecting geometric figures than letters. Additional support for the predominant role of the right hemisphere in visual scanning has been demonstrated in neuroimaging studies [36]. More specifically, neocortical activation was observed in the right anterior cingulated gyrus, in the intraparietal sulcus of the right posterior parietal cortex, and in mesial and lateral premotor cortices. Bell’s Test or Visual Neglect Test As with the previous two tests, the purpose of Bell’s Test [37] is to assess visual scanning by asking the patient to identify target stimuli on a page with multiple stimuli. The test consists of a sheet of paper with seven lines of 35 distracter figures (eg, bird, key, and so forth) and five targets figures (ie, bells). The target figures are arranged so that each appears in equal columns on the page. The patient initially is asked to name items that the examiner points to. If unable to do so because of language problems, he or she is asked to place cards representing each object on top of the object to ensure that the patient can recognize the target and the distracters. The examiner then presents the 398 M. Lanca et al / Neurol Clin N Am 21 (2003) 387–416 test copy and asks the patient to circle all the bells with a pencil. Accuracy and speed are recorded. Studies show that patients with right-hemisphere lesions are more likely to neglect of the left hemifield on this test [38–40]. Neither sex nor education is shown to influence test performance. Benton Judgment of Line Orientation Test The Benton Judgment of Line Orientation Test [41] focuses on the individual’s ability to estimate the angular relationships between two lines and match this angle with other line segments that are arranged in a fanline formation (Fig. 7). Normative data indicate that only 5% of normal controls scored below 63% accuracy [42]. Performance on this test declines with age [43]. A recent fMRI study reveals robust bilateral superior parietal lobe activation in ten right-handed controls [44]. This finding was corroborated by data from a cohort of patients with impairments of either right or left parietal lobe damage or with right parietal damage associated with a more severe deficit. Visual Object and Space Perception Battery Four subtests of the Visual Object and Space Perception Battery focus on simple features of spatial analysis. These tasks are designed to minimize the Fig. 7. Stimuli from the Benton Judgment of Line Orientation Test. (From Benton AL, Hamsher K, Varney NR, Spreen O. Contributions to neuropsychological assessment. New York: Oxford University Press; 1983; with permission.) M. Lanca et al / Neurol Clin N Am 21 (2003) 387–416 399 importance of cognitive skills other than those critical for space perception. The Dot Counting Test probes for single point localization and spatial scanning. The patient is asked to count the number of black dots on a card. The Position Discrimination and Number Location Tests focus on the individual’s ability to determine the relative positions of stimuli in 2-D space. In the Position Discrimination test, the patient is asked to indicate which of two dots is in the center of a square. In the Number Location Test, the patient is asked to match the position of a number stimulus in one square with the position of a dot in another square. The Cube Analysis Test focuses on analysis of 3-D space. In this task, the patient is asked to examine a 2-D drawing that represents a 3-D arrangement of blocks. He or she is asked to determine the number of blocks in the arrangement taking into consideration that some of the blocks may be hidden by others. Performance on this task depends on the patient’s ability to interpret spatial relationships. As with the other tests in the Visual Object and Space Perception Battery, investigations of these four tasks show that damage to right-hemisphere brain regions impedes performance more than damage to left-brain structures [21]. Case Study: patient MA MA was a 68-year-old woman referred for testing to provide information regarding her functional status in light of a history of a right parietal glioblastoma multiforme. MA underwent a total resection of the tumor, radiation therapy, and chemotherapy. In the aftermath of these events, she experienced a left inferior quadrantanopsia, left sided neglect, dressing apraxia, difficulty navigating familiar routes, trouble reading, difficulty dialing phone numbers, decreased attention, worsening peripheral vision, and mild visual blurriness. Imaging studies (Fig. 8) were consistent with right parietal and occipital brain damage. Performance on tests of baseline intelligence fell within the normal range. MA demonstrated mild problems in working memory, but she performed normally on tests of attention, language skills, and reasoning. MA’s memory for day-to-day events was wholly intact. She was well oriented and knowledgeable about personal events. There was evidence, however, of a material specific memory problem in that recognition of words from the Warrington Recognition Memory Test was average (44/50; 75th percentile), whereas facial recognition was impaired (31/50; <fifth percentile). MA’s basic perceptual abilities were impaired. She demonstrated hemispatial neglect when assessed with double simultaneous stimulation. Performance on the Letter Cancellation Test revealed impaired scanning. Whereas most individuals scan from left to right, patients who have sustained damage to right brain regions often begin scanning on the right side of space. In like manner, MA began in the upper right quadrant of space and she scanned vertically in a leftward direction until she came to the center of the page, at which point she returned to the right half of the page. 400 M. Lanca et al / Neurol Clin N Am 21 (2003) 387–416 Fig. 8. Brain imaging study of patient MA. MA neglected to note any of the 30 items in left space (Fig. 9). Scanning problems also were noted on a task requiring her to count a random array of dots on the Warrington Visual Object and Space Perception Battery. Her perceptual identification of degraded letters was impaired. She had difficulty on a task requiring her to judge spatial relations between visual stimuli (2/ 10). Her solution of block design puzzles from the WAIS-III was impaired; there was evidence of broken configuration and failure to appreciate gestalt. Visuoconstruction tests Visuoconstructive disturbances occur when there is a failure in organizing the spatial relations among parts of a visually perceived or imagined object. Given its broad definition, this construct encompasses a variety of spatial tasks, so that it is difficult to localize a specific area of the brain dedicated to preserving visuoconstructive ability. For example, a patient may be asked to assemble blocks to form a design, draw a design from memory, or copy a design. These drawings can consist of simple geometric figures (eg, squares) or more complex designs that have a 3-D element to them (eg, cube drawings). Clearly, these diverse tasks are not equivalent in their cognitive demands on sustained attention, perceptual acuity, and motor skills. The nature and level of difficulty of each task must be considered when assessing visuoconstructional ability. The patient’s reported difficulties should be closely examined when selecting the most appropriate tests to assess specific c Fig. 9. An example of MA’s hemineglect on the Cancellation Test. (From Muselam MM. Principles of behavioral neurology. Philadelphia: FA Davis; 1985.) M. Lanca et al / Neurol Clin N Am 21 (2003) 387–416 401 402 M. Lanca et al / Neurol Clin N Am 21 (2003) 387–416 disturbances. In the next section, a few tests that demand simple and complex visuomotor abilities are reviewed. Bender Visuomotor Gestalt Test The Bender Visuomotor Gestalt Test entails copying a series of nine 2-D line drawings on a blank sheet of paper (Fig. 10). The patient’s productions then are rated according to degree of accuracy and integration. Because of its simplicity, the Bender Visuomotor Gestalt Test is a valuable screening instrument for assessing perceptual-motor abilities in a variety of patients, especially those with low motivational levels, neurologic problems, and psychiatric conditions [45]. The test tends to be a better screening test for visual deficits than a diagnostic tool, because it does not provide detailed information about specific brain damage. Aside from this limitation, the Bender Visuomotor Gestalt Test often is used in the clinical setting perhaps because of its brief, economic, and extensive research norms [46]. Watkins and colleagues found that the Bender Visuomotor Gestalt Test was the sixth most frequently used test among clinical psychologists [47]. Several scoring systems have been developed for the Bender Test, each with advantages and disadvantages. Hutt and Briskin [48], and later Lacks Fig. 10. Items from the Bender Gestalt Test. (From Hutt ML. The Hutt adaptation of the Bender-Gestalt test. 4th edition. New York: Grune and Stratton, 1985; with permission.) M. Lanca et al / Neurol Clin N Am 21 (2003) 387–416 403 [49], outlined 12 ‘‘essential discriminator errors’’ (rotational, fragmentation, perseveration, and so forth) for assessing brain damage, although substantial empiric evidence about normative performance and the use of this classification for anatomic and functional diagnosis does not exist. Interscorer reliabilities for the more popular scoring systems are fairly high. Testretest reliabilities over a 3- to 12-month interval ranged from .57 to .79 [4]. Clock Drawing Test Neurologists’ bedside examinations of cognitive impairment have for many years required the patient to draw a clock [50]. This straightforward test is used to assess visuospatial and visuoconstuction skills and is sensitive to a variety of neurologic disorders. The patient is asked to draw a clock on a blank sheet of paper [38,51]. Several scoring systems and versions of the test are used [52]. Traditionally, patients were asked to set the time at 20 minutes after 8 o’clock; however, more recent versions of this test have requested patients to indicate the time as 10 minutes after 11 o’clock, because these numbers are actually on the face of a clock and, consequently, the task is more demanding [4]. Some versions of the Clock Drawing Test require the patient to draw the face of a clock on predrawn circles, whereas others require the patient to draw the circle and the corresponding numbers. In addition, patients often are asked to copy a drawing of clock. Because there may be dissociation based on the task demand (eg, oral command versus copy), it is recommended that the patient complete both conditions [4]. Despite limited normative data, the simplicity of the Clock Drawing Test makes it one of the most used tests for the screening of dementia, although it does not differentiate well between forms of dementia [53]. There is good test-retest reliability for this test [54] and practice effects have not been reported. Early studies indicated that impaired performance on the Clock Drawing Test was the result of lesions in right or bilateral temporoparietal brain areas [51]. In such cases, qualitative analysis of task performance may be instructive. For example, errors of spatial disorganization tend to be associated with right parietal lesions, whereas errors of task (eg, adding numbers and arranging the spatial layout) may be associated with frontal lesions [55]. Rey-Osterrieth Complex Figure Test The Rey-Osterrieth Complex Figure Test (ROCF) was introduced first by Rey [56] in 1941 as a test for brain damaged individuals. Three years later, the test was standardized by Osterrieth [57]. Although originally developed to assess visual memory impairment, the ROCF in recent years has been reported to assess a variety of visual functions, including visuoperceptual and constructional skills. The original administration asked the patient to copy a complex figure (Fig. 11) and then, without warning, reproduce it from memory three minutes later. More recent versions require the patient to reproduce the figure from memory immediately after copying it, and 404 M. Lanca et al / Neurol Clin N Am 21 (2003) 387–416 Fig. 11. The Rey-Osterrieth Complex Figure. (From Osterreith PA. Le test de copie d’une figure complex: contribution a l’etude de la perception et de la memoire. Arch Psycol 1944;30:286–356; with permission.) then again between 20 minutes to one hour after the original copy trial. Traditional scoring systems have focused on the accuracy of the drawing, and these systems tend to have high inter-rater reliability [58,59]. Some investigators have devised qualitative scoring systems that focus on the strategy that the individual employs in copying the ROCF [60,61]. These scoring systems can be helpful in localizing brain damage. For example, patients with frontal lobe lesions have difficulty planning their approach to the overall figure, whereas patients with right-hemisphere lesions may have difficulty attending to the left half of the figure. (See Fig. 12 for an example of patient with right-hemisphere brain disease.) Chervinsky et al [62], identified several cognitive functions necessary for task performance: visual perception, visuospatial organization, and memory (recall condition). A deficit in any of these domains suggests dysfunction in corresponding brain areas. Visual perception deficits resulting in a distorted copy of the figure may occur as a result of damage to posterior brain Fig. 12. Patient with right-hemisphere brain damage: copy of the Rey-Osterrieth Complex. (From Ostereith PA. Le test de copie d’une figure complex: Contribution a l’etude de la perception et de la memoire. Arch Psychol 1944;30:286–356; with permission.) M. Lanca et al / Neurol Clin N Am 21 (2003) 387–416 405 regions. Organizational problems, characterized by a piece-meal approach to the ROCF, often occur as a result of damage in frontal systems. Impairments in memory for the ROCF may occur as a result of right medial temporal damage. Age may have an adverse effect on recall accuracy, with older adults losing twice as much information as younger adults between copy and recall [63]. Studies assessing the influence of education levels with ROCF performance have been not been conclusive [60,64]. Block Design Test The Block Design Test requires the analysis and synthesis of spatial relations, visuomotor coordination, nonverbal concept formation and perceptual organization. In this test, the patient employs logic and reasoning to solve spatial relationships by using 3-D red, white, and half-red, halfwhite blocks to copy designs. The designs are arranged in increasing complexity. Accuracy and speed of completion are measured. The Block Design Test is sensitive to a wide range of neurologic disorders but, by and large, patients with right-hemisphere damage perform most poorly [65]. Qualitative analyses of error type reveal that extent of broken configuration errors is related to severity and laterality of brain injury; patients with righthemisphere damage perform most poorly [66]. Qualitative scoring also provides rich information about the patient’s overall functional status. Based on standard scoring, incorrect responses all receive a score of zero. Reasons for this, however, ‘‘may run the gamut from eating the blocks (in a confusional state), all the way to a flawless, systematic but slow construction (completed in 65 seconds, or five seconds over the time limit) of a nondemented patient with Parkinson’s Disease’’ [4]. Extensive normative data based on a nation-wide sample is subdivided into groups ranging from 16 to 89 years of age. Performance on this test decreases with age, even when slowness in an elderly population is taken into consideration [67]. Object Assembly Test The Object Assembly Test from the WAIS-III assesses a patient’s perceptual-motor coordination, visual organization, and mental flexibility. The patient is presented with a series of five puzzles, one at a time, and is asked to assemble the pieces to form a common object. Time to completion and accuracy are measured. Normative data are available based on age groups ranging from 16 to 89 years. Unfortunately, this test is vulnerable to a high degree of performance fluctuation, partly because of a potential to solve the puzzle accidentally by fitting parts together. It has a low correlation with other subtests of the WAIS-III, indicating that it is not highly predictive of general intelligence. Strategies used to complete the Object Assembly Test may be mediated by different brain regions. For example, patients with left-hemisphere lesions more often attempt to use edge alignment strategies based on contours, whereas patients with righthemisphere lesions try to put the pieces together with a focus on details [4]. 406 M. Lanca et al / Neurol Clin N Am 21 (2003) 387–416 Case study: patient AA AA was a 72-year-old African American woman who presented with memory difficulties in the context of global cognitive decline. Even though she was oriented, AA misplaced personal belongings and she had difficulty recalling details of conversations and events. Despite these difficulties, AA continued to live in senior housing with assistance from family members who helped with finances and medications. Formal testing revealed that AA had significant deficits in memory, naming, reasoning, visual construction, visual organization, graphomotor speed, and attention. Her clinical history and the pattern of test results were consistent with early stage AD. As with many patients who have dementia, AA encountered considerable difficulties on tasks of visuoconstructive skills that are highly dependent on planning and organization. She had difficulty copying simple geometric designs and her copy of a cube was significantly distorted. She could not correctly place the numbers on a clock face (Fig. 13). AA’s prominent visuoconstructive deficits underscore the fact that these types of problems often occur in the context of diffuse brain damage. Tests of visual attention and memory Assessment of visual attention and memory allows the examiner to determine whether or not the individual can retain visual information over Fig. 13. Patient AA: the Clock Drawing Test. (From Freedman M, Kaplan E, Delis D, et al. Clock drawing: a neuropsychological analysis. New York: Oxford University Press; 1994; with permission.) M. Lanca et al / Neurol Clin N Am 21 (2003) 387–416 407 short or long time intervals in order to guide ongoing behavior. Visual attention is a broad term that encompasses attention span, divided attention, processing speed, and sustained attention. In this section, tests that focus on visual span of attention and visual fluency are presented. Visual memory includes visual working memory and long-term visual memory. Visual working memory refers to the retention and manipulation of information that is in conscious awareness. Long-term visual memory can be broken down into anterograde memory (ie, acquisition of new information) and retrograde memory (ie, retrieval of information that predates an insult or injury to the brain). Memory problems may occur for many reasons, including normal aging, depression, and neurologic conditions. Circumscribed memory difficulties, as seen in patients with amnesia, suggest damage to hippocampal circuitry. Information regarding visual aspects of memory is important for rehabilitative purposes and for the identification of lesion location. Spatial Span Test The Spatial Span Test (Fig. 14), a subtest of the Wechsler Memory ScaleIII (WMS-III [68]), provides information regarding the amount of visual information that an individual can retain ‘‘on line.’’ The examiner points to a sequence of 3-D blocks on a board and the patient is required to repeat the same sequence. The number of blocks pointed to increases with each subsequent trail. There are two conditions: in the forward condition, repetition of the identical sequence is required; in the reverse condition, the patient is asked to imitate the sequence in reverse order. Because the reverse spatial span task requires manipulation of new information and storage, this test also can be seen as a test of visual working memory. Research also shows that patients with right-hemisphere damage perform worse than lefthemisphere patients on this test [69]. Recent findings find that patients with Fig. 14. The Corsi Block-Test. (From Milner B. Interhemispheric differences in the localization of psychological processes in man. Br Med Bull 1971;27:272–77; with permission.) 408 M. Lanca et al / Neurol Clin N Am 21 (2003) 387–416 lesions in the posterior part of the parietal or occipital lobe perform especially worse on spatial-memory tasks [70]. Visual Reproduction Test Another visual memory subtest from the WMS-III [68] is Visual Reproduction. In this test, a series of five designs are shown to the patient one at a time for 10 seconds. After each design is presented and then removed from sight, the patient is asked to draw it immediately from memory. Later, there is a 30-minute delayed memory condition that is made up of several tasks, including having the patient draw the designs from memory, having the patient identify designs seen earlier from 48 designs including original and distractor designs, asking the patient to draw the designs while looking at them, and asking the patient to match a target design on the top of the page to six designs on the bottom. Scoring is based on four conditions: immediate and delayed recall of the design (based on accuracy of the copied design), recognition, copy, and discrimination. Delaney and colleagues found that laterality of lesion did not affect immediate recall of these stimuli [71]. This may in part be the result of the simplicity of the designs, which may encourage verbal encoding. Lateralized differences, however, did appear at the 30-minute delay condition, showing that patients with right temporal lesions obtained significantly lower scores their left temporal lesion counterparts or normal controls. Complementing this finding, a construct validity study using Visual Reproduction found that the delayed reproduction measures of visual memory were more valid than the traditional immediate reproduction administrations, which were more closely associated with visual-perceptual-motor abilities [72]. One recent MRI study investigating the relationship between extrahippocampal limbic structures and memory functioning with patients with temporal lobe epilepsy (TLE) found that immediate visual reproduction performance was significantly related to the right and left amygdala volumes and right mammillary body volume. Only the right amygdala and right mammillary body volume, however, were associated with the delayed Visual Reproduction trial. Results suggest that visual memory may be uniquely associated with extrahippocampal volumes in patients with TLE [73]. Ruff Figural Fluency Test The Ruff Figural Fluency Test focuses on capacity for fluid and divergent thinking, ability to flexibly shift attention from one line of thinking to another, and planning strategies [74]. The patient is presented with a sheet of paper with a set of 35 boxes containing dot configurations. The patient is asked to connect two dots or more using straight lines and to make as many patterns as possible within a 60-second time frame. Test-retest reliability was moderate [74]. There was no effect of gender on task performance, but increased education and younger age have been associated with better M. Lanca et al / Neurol Clin N Am 21 (2003) 387–416 409 performance on this task. Figural fluency is sensitive to right frontal dysfunction [75]. Spatial Working Memory Test Some developers are attempting to bring procedures developed primarily for cognitive neuroscience research into the neuropsychology clinic, using computerized administration, response collection, and scoring [76,77]. This test focuses on the individual’s ability to retain visual stimuli in memory over short delay intervals and with distraction [78]. Stimuli are flashed briefly at random locations on a computer display and the patient touches the screen locations where they recall seeing the stimuli, after varying delays and distraction. A touch-sensitive screen on the computer records the exact location and time of each response and determines how the spatial accuracy of response decreases with increasing delay. An interesting feature of this test is that the difficulty level of the matching process is manipulated dynamically based on the patient’s performance, becoming easier if they make errors and becoming more difficult if they do well. This level of difficulty is then used in subsequent trials with longer delays to determine if there is a working memory deficit, independent of individual differences in perceptual competency. Healthy individuals performing this test show activations of the superior parietal cortex (bilaterally) and parts of the medial and superior frontal cortex [79]. Object Working Memory Test The Object Working Memory Test is another computer-based test focusing on the early component of memory. In this paradigm, the patient is asked to match a complex visual pattern to a previously displayed stimulus. Test difficulty once again is calibrated according to the individual’s performance; if the individual has difficulty with the matching procedure, the test automatically becomes easier and the converse takes place in the event that the individual performs well. The level of difficulty at which 84% of items are matched correctly is then used in subsequent trials with longer delay intervals. In this task, visual working memory can be determined apart from individual differences in perceptual competency. Initial imaging studies have indicated that task performance is mediated by the superior parietal cortices and medial and superior frontal cortices [80]. Biber Figure Learning Test The Biber Figure Learning Test (BFLT) is a test of nonverbal memory that was designed to measure recall and recognition of information that exceeds attention span limitations. The task is designed to complement many of the verbally based list learning tasks that are used in clinical examinations (eg, Rey Auditory Verbal Learning Test and the California Verbal Learning Test). As a result of parallel design features, a comparison between the BFLT and the verbal tasks can be used to provide information regarding material specific aspects of memory. The individual is presented 410 M. Lanca et al / Neurol Clin N Am 21 (2003) 387–416 with a series of 15 geometric figures, presented one at a time (Fig. 15). After the presentation of the entire series, the patient is asked to draw the designs from memory. The same series of designs are presented four more times. After each presentation, recall is tested. After the fifth trial, a distractor set of stimuli is presented. Recall for the distractor items may be impaired as a result of proactive interference. In other words, memory for the original set of 15 designs may interfere with the individual’s ability to learn new items. After recall of the distractor list, recall of the original list is tested. Fifteen to thirty minutes later, delayed recall is examined. Subsequently, delayed recognition of the original designs, which are embedded in a group of foil items, is examined. Information obtained from this test may help determine laterality of brain damage. In at least one study, performance on this task was associated with relative deficits in right temporal brain regions [81]. Warrington Recognition Memory Test The Warrington Recognition Memory Test is one of a handful of tests that provide useful information regarding material-specificity. Some patients present with material-specific memory disorders whereby there is dissociation between verbal and nonverbal memory. It is often difficult, however, to compare verbal with nonverbal memory because memory tasks vary along dimensions other than material specificity. For instance, most tasks of verbal memory use an auditory modality of presentation (ie, words or stories are read aloud) and information is presented in a serial fashion, whereas nonverbal memory tasks employ a visual modality with simultaneous presentation of material. In this visual memory test, recognition of 50 nonverbal stimuli (faces) and 50 verbal stimuli (words) is examined. In the first condition, patients are shown 50 words one at a time at a rate of three seconds per stimulus and then are asked to identify each previously viewed Fig. 15. Stimuli from the Biber Figure Learning Test (From Glosser G, Ryan L, Fedio P. Validation of a new visual memory test in post temporal lobectomy patients. Presented at the National Academy of Neuropsychology meeting. Pittsburgh, 1992; with permission.) M. Lanca et al / Neurol Clin N Am 21 (2003) 387–416 411 word from a choice of two words. In the second condition, there is a similar forced-choice recognition task with 50 black-and-white photographs of male faces. The patient is then shown two faces (one previously seen and one distractor) and asked to point to the picture that previously seen. Validation studies show that patients with right-hemisphere lesions are significantly impaired in facial recognition, whereas their word recognition may be intact [82]. Morris and colleagues studied patients who had undergone unilateral temporal lobectomy and found that patients with right temporal lobectomies were significantly worse than the left lobectomy group on the faces subtest of this test and, conversely, that left temporal lobectomy patients were significantly worse than patients with right lobectomy on the word portion of the test [83]. Furthermore, the facial memory subtest was relatively sensitive and specific in detecting impairment in the right lobectomy patients, whereas the verbal subtest was less sensitive in detecting effects of the left lobectomy group. Also, patients with left cerebral damage perform poorly on the facial and verbal recognition conditions of this test, but their word recognition is disproportionately impaired consistent with the site of their lesions. Case study: patient KT KT was a 36-year-old woman who presented with cognitive and perceptual problems in the context of hypoxic-ischemic brain damage secondary to an episode of respiratory arrest at age six. In the aftermath of this episode, KT demonstrated visual processing problems. Her acuity was diminished (20/80 in the right eye and 20/400 in the left). Visual pursuit was impaired in all directions. Saccades were normal in speed and accuracy. There was evidence of a partial homonymous inferior left quadrantanopsia. Higher-order visual processing problems also were noted. KT was alexic and identified as a letter-by-letter reader. She was unable to recognize friends and family members by their faces and often relied on voices, clothes, and context as identifying cues. Imaging studies (Fig. 16) revealed atrophy in calcarine and peristriate cortices, most notably the right fusiform and biparietal regions. Despite her prominent visual problems, KT was bright and accomplished. She graduated from college and obtained several master’s degrees. At the time of evaluation, she indicated interests in poetry, English literature, and church history. KT’s performance on tests of general cognitive abilities was extremely variable, with superior performance on tasks measuring fund of information, vocabulary, comprehension of social norms, and verbal concept formation. In contrast, she demonstrated impaired performance on tasks of processing speed and perceptual organization. There was a significant discrepancy between verbal intelligence (VIQ = 124) and nonverbal intelligence (PIQ = 69). Her low scores on the visual tests were the result of reduced visual acuity, motor slowness, and problems with visual integration. There was evidence of material-specific memory deficits on 412 M. Lanca et al / Neurol Clin N Am 21 (2003) 387–416 Fig. 16. Brain imaging study of patient KT. the Warrington Recognition Memory Test, where recognition of words was perfect (50/50) but recognition of faces was impaired (29/50, <fifth percentile). Facial discrimination on the Benton Facial Recognition Test was impaired (<first percentile). Identification of famous faces (such as the face of Princess Diana) was impaired (4/73) but she benefited from verbal cuing (67/73), indicating that she was familiar with the famous individuals. Her poor performance on tasks of facial perception and facial memory was consistent with an apperceptive prosopagnosia. Performance on the Visual Object and Space Perception Battery was variable, with adequate performance on tests of shape detection (40/40), spatial scanning (9/10), and location discrimination (10/10). Impaired performance was seen on tests of object recognition (15/40), position discrimination (12/20), and analysis of complex spatial relationships (5/10). Performance on the Benton Line Orientation Test was average (40th percentile). Solution of puzzles was lowaverage on the WAIS-III; there was no evidence of broken configuration or failure to appreciate gestalt. Summary This article introduces the reader to a sample of visual tests used in the neuropsychologic assessment of patients who present with various visual deficits. As discussed, patients often present with visual abnormalities that cannot be assessed exclusively during the opththalmologic examination, partly because these problems extend beyond the fundamental aspects of visual processing. Visual problems occur in the context of focal or diffuse brain damage. Neuropsychologic evaluation can provide valuable diagnostic information and information regarding functional strengths and weaknesses. Many visual tests have been developed for clinical use. Some of these tests have been validated with lesion analytic or neuroimaging studies, M. Lanca et al / Neurol Clin N Am 21 (2003) 387–416 413 which highlight the areas of the brain presumed necessary for task performance. Knowledge regarding the neural substrates of test performance allows the clinician to identify the neuropathologic correlates of test failure, which, in turn, is relevant to differential diagnosis. A profile of functional strengths and weaknesses emerges contributing to the treatment of the patient with a visual disorder. In this article, the authors present a subset of visual tests used primarily in the clinical setting. 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