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,