TY - JOUR
AU1 - Tariq, Usama
AU2 - Parker, Alicia
AU3 - Saadatpour, Leila
AU4 - Doty, Leilani
AU5 - Heilman, Kenneth M
AB - Abstract Background/Objectives Whereas rare cases of hemispatial visual neglect have been reported in patients with a neurodegenerative disease, quadrantic visuospatial neglect has not been described. We report a patient with probable posterior cortical atrophy who demonstrated lower right-sided quadrantic visuospatial neglect, together with allocentric vertical neglect. Methods/Results A 68-year-old man initially noted deficits in reading and writing. Subsequently, he developed other cognitive deficits. On vertical line bisections, he deviated upward, and on horizontal line bisections, he deviated to the left. These deviations together suggest that this man’s neglect might be most severe in his right (head/body-centered) lower (below eye level) visual space. When attempting to perform vertical line bisections in all four egocentric quadrants, his upward deviations were largest in the right lower quadrant. On a cancelation test, he revealed bilateral lower (ventral) allocentric neglect but not egocentric neglect. This patient’s magnetic resonance imaging revealed cortical atrophy, most prominent in the left parietal lobe. Discussion Previous research in stroke patients has demonstrated that the parietal lobes are important in mediating attention to contralateral and inferior visual space. The presence of left parietal atrophy may have induced this right lower (ventral) egocentric inattention as well as bilateral ventral allocentric inattention. Although to our knowledge there have been no prior reports of a patient with right lower quadrantic and lower vertical allocentric visuospatial neglect, patients are rarely tested for these forms of neglect, and this patient illustrates the importance of evaluating patients for these and other forms of neglect. Posterior cortical atrophy, Neurodegenerative disease, Quadrantic neglect, Alzheimer’s disease, Spatial inattention Introduction Benson, Davis, and Snyder (1988) described five patients who had a progressive disorder that most often started with impairments of “higher visual function.” Some of these patients also had cognitive deficits, such as alexia, agraphia, and other elements of the Gerstmann’s syndrome. However, unlike most patients with Alzheimer’s disease (AD), initially, these patients’ episodic memory was intact. Brain imaging of these patients revealed predominant parieto-occipital atrophy. Benson and colleagues called this disorder posterior cortical atrophy (PCA). PCA or Benson’s syndrome is a clinical disorder that often presents with impairments of visuospatial processing. PCA is most commonly associated with the pathological changes associated with AD; however, PCA may be associated with dementia with Lewy bodies (DLB), corticobasal degeneration, Pick’s disease, and prion disease (Alladi et al., 2007; Renner et al., 2004; Tang-Wai et al., 2004). In this report, we describe a patient who appeared to have PCA with right lower egocentric (body-centered) quadrantic spatial visual neglect and lower vertical allocentric (object-centered) visual neglect. Neglect is the failure to report, respond, or orient to the stimuli that cannot be attributed to primary sensory or motor defects (Heilman et al., 1993). When performing horizontal line bisection tests, patients with hemispatial neglect will often reveal a deviation toward the injured hemisphere. Whereas many lesion sites have been reported to induce hemispatial neglect, the most common lesion location is the parietal lobe (Heilman & Rothi, 2012). Although the most frequent cause of spatial neglect appears to be stroke, neglect can also be seen with degenerative diseases such as PCA. For example, Andrade and colleagues (2010) evaluated 24 patients with PCA using a “standardized battery of neglect tests” that included the line bisection and cancelation tests. They found that 16 (67%) of the 24 patients had signs of visual neglect on at least one test and 14 patients (58%) also had visual extinction. They also found that left-sided neglect was more severe than right-sided neglect, but that right-sided neglect had a higher frequency in this population than in those studies of patients with neglect from stroke. In Andrade and colleagues’ study, the patients were not evaluated for vertical neglect. However, there have been some reports of patients who exhibited vertical spatial neglect, caused by stroke, who had inattention to either upper or lower egocentric visual space (Rapcsak et al., 1988; Shelton et al., 1990). Whereas recently, Glazer, Saadatpour, Doty, and Heilman (2017) reported a patient with PCA who revealed upper vertical neglect, inattention to a quadrant of egocentric (body- and head-centered) visual space as well as lower spatial allocentric (object-centered) neglect, to our knowledge, has not been reported. Case Report A 68-year-old right-handed man presented to our memory clinic with a 4-year history of gradual progressive cognitive decline. His wife, who provided further details about his history, accompanied him. Prior to the onset of this disorder, he had been a high-functioning accountant. His symptoms began with changes in his handwriting, particularly in the orientation of the letters. A year later, he retired due to inability to read, which was initially attributed to cataracts. However, after his cataracts were removed, his visual perception has not improved. He had difficulty with reading, including difficulty knowing the location of the letters that compose words and recognizing letters. His ability to name and identify colors was not impaired. Over time, his handwriting became illegible. He developed difficulty with using the lawnmower and inserting gasoline into the mower’s tank. Then he developed an impaired ability to carry out multistep directions. The patient stopped driving due to difficulty with his visual perception. More recently, he developed difficulty with temporal orientation, calculations, naming, and facial recognition. There were no clinical fluctuations. He described 5 years of dream re-enactment behavior wherein he would act out his dreams. More recently, he began to have visual hallucinations of small animals upon awakening, and his wife described episodes suggestive of brief behavioral arrests. Regarding his movements, his wife reported that he had begun to walk more slowly on his daily walks but he had not noticed this change. For several years, he had shaking of his hand when holding a cup. He reported that he has been in a good mood, sleeping well with minimal snoring when on his back, and he had a more relaxed personality since his retirement. He continues performing instrumental activities including housework and yardwork. Although he denied any difficulty with performing these tasks, his wife reported that he occasionally would vacuum over power cords, which could cause problems. He is able to take care of basic activities of daily living; however, he will often put on his shirts inside out, which his wife attributes to his visual impairments. On his review of symptoms, he reported that for four decades he felt lightheaded when first standing. He also complained about constipation for 10 years and nocturia for 3 years. He denied bloating or early satiety. There was no family history of cognitive or movement disorders. His medications included supplements of vitamins B12 and D, which were previously reported to be low. He drinks one glass of wine daily, for many years. On general physical examination, his pulse was 50 beats per minute, with regular rhythm. He had normal S1 and S2; there was no murmur, click, rub, or gallop; and the remainder of his general physical examination was normal. On neurological examination, his cranial nerves appeared to be normal. On visual confrontation testing, he revealed no evidence of a visual field defect. This patient, however, did not receive perimetry testing of his visual fields. His visual acuity was not tested but he was able to read the sentence on the Mini-Mental State Examination (MMSE). The patient was alert and oriented to person, city, and day of the week, time, and location; however, he was not oriented to year, clinic name, season, or county. His thought process was not tangential and his affect was congruent. His speech was fluent with relatively word finding and repetition, with mildly impaired comprehension. The patient underwent several neuropsychological tests. On the MMSE, he scored 17/30, which is the abnormal (dementia) range. He lost four points for orientation, four points for attention and calculation, three points for verbal recall, one point for writing a sentence, and one point for copying a design. In regard to his handwriting, it was illegible and deviated upwards (Fig. 1). With the Montreal Cognitive Assessment, he was also impaired on the Trails B test. When drawing on horizontally positioned paper, this patient’s drawings of the cube and the intersecting pentagons were so impaired that the presence of neglect could not be determined. Fig. 1 Open in new tabDownload slide Example of patient’s handwriting, exhibiting agraphia and the upward deviation of his writing hand as it moves rightward. Fig. 1 Open in new tabDownload slide Example of patient’s handwriting, exhibiting agraphia and the upward deviation of his writing hand as it moves rightward. The patient was asked to draw a clock and to set the hands of this clock to 10 min after 11 o’clock (Fig. 2). The patient first attempted to draw a circle. When attempting to draw this circle, he drew an oval and this oval was slanted, such that the right lower corner of the circle was relatively displaced to the left and upward. When inserting the numbers into the circle, the patient appears to be less accurate in the spatial positioning of the numbers on the right side than those on the left side. In addition, the placement of these numbers does not appear to be properly aligned in relation to the right edge of the circle, suggesting an unawareness of the right half of the circle. The placement of the numbers also appears to be rotated in a clockwise direction. For example, when a clock is correctly drawn and a line is drawn from the number 12 to the number 6, this line should be vertical. However, in this patient’s drawing, if a line is drawn from the number 12 to the number 6, this line is rotated in a clockwise direction. These changes in the clock drawing appear to be related to inattention to right and lower space. Fig. 2 Open in new tabDownload slide Patient’s drawing of a clock. The patient first attempted to draw a circle. When drawing this circle, it appears that the right lower corner of the circle is displaced to the left and upward. When inserting the numbers into the circle, the patient appears less aware of the location of the numbers on the right side and these are not properly aligned in relation to the right edge of the circle, suggesting an unawareness of the right half of the circle. In addition, the placement of the numbers appears to be rotated in a clockwise direction. For example, if line is drawn from the number 12 down to the number 6, this line, which should be vertical, is rotated in a clockwise direction. These changes in the clock drawing may be related to this patient’s spatial inattention to right lower space. Fig. 2 Open in new tabDownload slide Patient’s drawing of a clock. The patient first attempted to draw a circle. When drawing this circle, it appears that the right lower corner of the circle is displaced to the left and upward. When inserting the numbers into the circle, the patient appears less aware of the location of the numbers on the right side and these are not properly aligned in relation to the right edge of the circle, suggesting an unawareness of the right half of the circle. In addition, the placement of the numbers appears to be rotated in a clockwise direction. For example, if line is drawn from the number 12 down to the number 6, this line, which should be vertical, is rotated in a clockwise direction. These changes in the clock drawing may be related to this patient’s spatial inattention to right lower space. On Hopkins Verbal Learning Test, he learned four, four, and five words in the three learning trials. His total score of 13 demonstrates a verbal learning deficit. With delay, he recalled no works but recognized 11 of it with a discrimination index of seven. That he was better able to recognize than recall suggests he had a retrieval deficit; however, because neither his learning nor recognition were normal, he probably also had an encoding deficit. His letter fluency was normal with 26 correct responses when using the letters F-A-S; however, categorical fluency for animals was decreased and he scored 11. He was tested for finger agnosia by having the examiner hold up his own index finger and asking the patient to name this finger (Shenal et al., 2006). He did not have finger agnosia. His calculation was impaired and he had mild right–left confusion. He had impaired naming on Boston Naming Test, correctly naming 10/15 objects. He was unable to name pictures of a helicopter, whistle, beaver, pretzel, and dart. He was able to correctly name 12/15 verbal descriptions of different objects. He was asked to locate five states in an outline map of the USA and he correctly located Maine, Florida, and Texas, but failed to locate California and Oregon. On a Navon figure, which was a large triangle composed of small squares, he recognized the large triangle but not the small squares. On the American Presidential Facial Recognition test, he was able to name only one (President Richard Nixon) of the 10 pictures of presidents. Whereas our Navon figure test and the Presidential Facial Recognition test have not been standardized, this patient was a well-educated accountant and his performance on these tests certainly suggests the presence of prosopagnosia and impairment of focal attention. Although it is possible that he had little or no knowledge of the American presidents, this would be unlikely and his wife did not indicate that this was so. To learn if this patient had neglect, line bisection tests as well as cancelation tests were performed (Table 1). On these tests, the patient sat in a chair and the sheets of paper were held in the coronal plane, eye level, and about 35 cm from the patient’s head. The testing was performed in the coronal plane because when performing on a tabletop and looking down, most people somewhat flex their neck. Thus, the paper on the table is partially in their head’s radial (transverse) plane and partially in their head’s coronal plane. Because we were examining this patient for egocentric vertical neglect, we wanted to make certain that all vertical lines were in the coronal plane. When performing a horizontal line bisection test, it does not make a difference if the paper is on a table or in the coronal plane because a horizontal line is at the intersection of the coronal and transverse planes and the examiner is attempting to learn if there is an attention bias to the right or left side. The same would hold true for the classical cancelation test. On the line bisection testing, he was tested with four horizontal lines (average length, 22.4 cm) and four vertical lines (average length, 22.4 cm) placed in his midsagittal plane. On the horizontal line bisection test, he deviated 1.6 cm to the left, and on the vertical line bisection test, he deviated upward by 2.3 cm. This patient’s leftward deviation was even greater than young healthy participants who normally reveal a greater leftward deviation (pseudoneglect) than do older participants. For example, when attempting to bisect 20 cm lines, younger healthy adults deviate an average of about 1.38 mm (~0.7%; Rotondaro et al., 2015). This patient’s upward vertical deviation was also greater than healthy participants who have a mean deviation of 4 mm (Suavansri et al., 2012). Table 1 Scores of the line bisection and cancelation tests of spatial neglect 1. Horizontal line bisection    Mean deviation = 1.6 cm left 2. Vertical line bisection    Mean deviation = 2.3 cm upward 3. Quadrantic vertical line bisections    Mean left upper = 1.1 cm    Mean right upper = 0.6 cm    Mean left lower = 1.6 cm    Mean right lower = 3.6 cm 4. Letter A cancelation test    Total missed = 4    Right side of page = 3 with 2 in lower quadrant    Left side of page = 1 in upper quadrant 5. Open and closed square cancelation test    Total open squares missed = 11/28    Entire page, upper open squares missed = 3/14    Entire page, lower open squares missed = 8/14    Top of page, open squares missed = 5/14    Bottom of page, open squares missed = 6/14    Right side of page, open squares missed = 6    Left side of page, open squares missed = 5 1. Horizontal line bisection    Mean deviation = 1.6 cm left 2. Vertical line bisection    Mean deviation = 2.3 cm upward 3. Quadrantic vertical line bisections    Mean left upper = 1.1 cm    Mean right upper = 0.6 cm    Mean left lower = 1.6 cm    Mean right lower = 3.6 cm 4. Letter A cancelation test    Total missed = 4    Right side of page = 3 with 2 in lower quadrant    Left side of page = 1 in upper quadrant 5. Open and closed square cancelation test    Total open squares missed = 11/28    Entire page, upper open squares missed = 3/14    Entire page, lower open squares missed = 8/14    Top of page, open squares missed = 5/14    Bottom of page, open squares missed = 6/14    Right side of page, open squares missed = 6    Left side of page, open squares missed = 5 Open in new tab Table 1 Scores of the line bisection and cancelation tests of spatial neglect 1. Horizontal line bisection    Mean deviation = 1.6 cm left 2. Vertical line bisection    Mean deviation = 2.3 cm upward 3. Quadrantic vertical line bisections    Mean left upper = 1.1 cm    Mean right upper = 0.6 cm    Mean left lower = 1.6 cm    Mean right lower = 3.6 cm 4. Letter A cancelation test    Total missed = 4    Right side of page = 3 with 2 in lower quadrant    Left side of page = 1 in upper quadrant 5. Open and closed square cancelation test    Total open squares missed = 11/28    Entire page, upper open squares missed = 3/14    Entire page, lower open squares missed = 8/14    Top of page, open squares missed = 5/14    Bottom of page, open squares missed = 6/14    Right side of page, open squares missed = 6    Left side of page, open squares missed = 5 1. Horizontal line bisection    Mean deviation = 1.6 cm left 2. Vertical line bisection    Mean deviation = 2.3 cm upward 3. Quadrantic vertical line bisections    Mean left upper = 1.1 cm    Mean right upper = 0.6 cm    Mean left lower = 1.6 cm    Mean right lower = 3.6 cm 4. Letter A cancelation test    Total missed = 4    Right side of page = 3 with 2 in lower quadrant    Left side of page = 1 in upper quadrant 5. Open and closed square cancelation test    Total open squares missed = 11/28    Entire page, upper open squares missed = 3/14    Entire page, lower open squares missed = 8/14    Top of page, open squares missed = 5/14    Bottom of page, open squares missed = 6/14    Right side of page, open squares missed = 6    Left side of page, open squares missed = 5 Open in new tab Because this patient revealed both lower vertical and right horizontal spatial neglect on line bisection tests, we wanted to learn if he had more severe neglect of the stimuli presented in the right lower quadrant of his body/head (egocentric) space than neglect in the other three quadrants. Therefore, to learn if this patient had body/head-centered (egocentric) quadrantic neglect, we performed two vertical line bisections in all four quadrants of head-centered (egocentric) space. This included presenting the lines above eye level on the right and left sides of this patient’s midsagittal plane, as well as below eye level on the right and left of the patient’s midsagittal plane. This testing revealed a mean upward vertical deviation in all four quadrants (right upper quadrant mean upward deviation with 21.5-cm lines, 0.6 cm; left upper quadrant mean deviation with 23-cm lines, 1.1 cm; mean upward deviation of 22-cm lines placed in the left lower quadrant, 1.6 cm; and mean upward deviation on the bisection of lines placed in the right lower quadrant, 3.6 cm). Unfortunately, we could not find any papers that have examined vertical bisections in all four egocentric visual quadrants, and thus we could not compare our patient’s performance with normal participants. However, this patient’s upward deviation appeared to be much greater when the lines were placed on the right side of his head and below eye level. On a letter cancelation test, where the patient is presented with a white sheet of paper (8.5 × 11 in) with capital letters printed in black ink and randomly placed on this sheet, the patient was asked to cancel (mark) all the A letters on this sheet. This patient failed to cancel four of the A letters. Three of the letters he failed to cancel were on the right half of the page and two of these three letters were in the lower quadrant. We also tested this patient with what we call an “open box cancellation task.” This test is used to evaluate patients for the presence of vertical and horizontal egocentric (body-centered) neglect (e.g., failing to cancel boxes that are located in the space that is across from one half of their body) as well as for the presence of allocentric (object-centered) neglect. In this test, the patient was presented with a sheet of paper (8.5 × 11 in) that had forty-two 2 × 2-cm squares. Of these 42 squares, 14 had openings on the bottom and 14 had openings on the top. On this cancelation test, this patient did not appear to have a clear egocentric (head/body-centered) vertical spatial bias. For example, on the top half of the sheet, he made five errors, and on the bottom half of the sheet, he made six errors. In addition, on this test, he did not appear to have egocentric lateral neglect. On the right side of the sheet, he made five errors; on the left side, five errors; and at the center, one error. There also did not appear to be quadrantic egocentric neglect. In the left upper quadrant, he made three errors, two errors in his right upper quadrant, two errors in his left lower quadrant and three errors in his right lower quadrant. In regard to object-centered (allocentric) neglect, over the entire sheet of paper, this patient missed canceling 11 of the 28 open squares. Of the open squares that he failed to cancel, eight squares had openings in the lower part and three squares had openings in the upper part. However, we know of no vertical (up-down) allocentric cancelation test that has been standardized with healthy participants. Thus, we cannot compare our patient’s performance with healthy participants. However, this patient’s performance does suggest that he had a lower (ventral) allocentric (object-centered) neglect. In addition to testing this patient for hemianopia using visual confrontation testing, he was also tested for extinction to simultaneous stimulation in his upper and lower visual fields. He was asked to look straight ahead (midsagittal plane), and in addition to detecting one hand being moved, in his right or left visual field, he was asked to detect the simultaneous movements of both hands (one hand movement in his left visual field and the other hand movement in his right visual field). As mentioned, he was not impaired in detecting these unilateral left- and right-sided stimuli. However, with bilateral horizontal simultaneous stimulation, in lower space (below eye level), he was unaware (extinguished-neglected) of the stimuli in his right lower visual field. There was, however, no evidence of tactile neglect or extinction. When this patient was asked to write a sentence, he revealed that he had an apraxic agraphia. In addition, when he was writing, as his hand moved from the left to the right side of the page, his writing moved upward (Fig. 1), and this deviation appears to be related to the neglect of right lower space. His apraxic agraphia was associated with an ideomotor apraxia of his upper limbs, as assessed by asking him to pantomime transitive actions. He did not reveal an ideational apraxia (impaired sequencing of actions), but based on his impairment in filling a gas tank and performing other tasks, he appeared to have a conceptual apraxia, a loss of mechanical knowledge (Heilman & Rothi, 2012), but was not formally tested for this disorder. On motor examination, he had bilateral symmetric cogwheel rigidity and mirror movements. His motor strength was normal; however, he had moderate-to-severe paratonia of his neck and symmetrical paratonia of his extremities. There was a minimal to moderate symmetrical action tremor of both upper limbs, as well as a postural tremor of his upper extremities. There was no evidence of a resting tremor, bradykinesia, or postural instability. Sensory examination was normal to touch, temperature, and vibration. Limb-kinetic apraxia and ataxia were not present. Deep tendon reflexes were 3+ and symmetric. Frontal release signs including the glabellar and snout signs were present. His plantar response (Babinski’s sign) was equivocal bilaterally. He was able to rise from a chair without using his arms, and when walking, he had a normal stride length. He was also able to tandem walk. Mild camptocormia was present, and he had a bilateral decrease of his arm swing. He took four steps when turning his body 180 degrees. There was no evidence of retropulsion. Laboratory studies for reversible causes of dementia were unrevealing and included tests for Lyme disease, thyroid-stimulating hormone and free thyroxine, anti-nuclear antibody, double-stranded DNA antibody, vitamin B12, and sedimentation rate. His electroencephalogram (EEG) was normal. His brain magnetic resonance imaging revealed cortical atrophy that was most prominent in the posterior region of his left hemisphere (Fig. 3). Based on his history and finding, he was diagnosed of PCA with progression; however, the underlying pathophysiology of his disorder remains unknown. Fig. 3 Open in new tabDownload slide Magnetic resonance imaging of the brain revealing cortical atrophy that is most prominent in the posterior regions of this patient’s left hemisphere. Fig. 3 Open in new tabDownload slide Magnetic resonance imaging of the brain revealing cortical atrophy that is most prominent in the posterior regions of this patient’s left hemisphere. Discussion We report a patient who demonstrated lower right-sided quadrantic visuospatial neglect, a clinical disorder that has not been previously reported. This patient also revealed allocentric vertical neglect. This patient’s disorder is most likely a form of PCA that was initially described by Benson and colleagues (1988). Posterior Cortical Degeneration In this initial report, Benson and colleagues (1988) described PCA in five patients, and several of these patients had different symptoms and signs. Several subsequent reports have also indicated that the signs and symptoms of PCA can vary between patients and patients often develop many additional signs and symptoms as PCA progresses (Mendez et al., 2002; Tang-Wai et al., 2004). PCA, however, is a distinctive dementia syndrome in which the most pronounced pathologic involvement is in the posterior temporoparietal and occipital regions independent of the specific underlying pathology. Recently, Crutch, Schott, and Rabinovici (2017) rank-ordered the clinical, cognitive, and neuroimaging features of PCA in terms of frequency. The most common clinical features are insidious onset, gradual progression, and prominent early disturbance of visual and/or other posterior cognitive functions. Our patient revealed these most common features. His early symptoms, like those first reported by Benson and colleagues, were an impairment of reading and writing with evidence of parietal and occipital atrophy. In addition, early in his course, he did not have a memory impairment, and then like many patients with PCA, he subsequently had a progressive cognitive decline. Crutch and colleagues had exclusionary criteria, such as brain tumors, strokes, and metabolic disorders. Our patient did not have any of these exclusionary criteria. Crutch and colleagues also noted that patients classified as PCA-plus must fill the core clinical criteria and fulfill core clinical criteria for at least one other neurodegenerative syndrome. Although to our knowledge there have been no prior reports of a patient with quadrantic and vertical allocentric visuospatial neglect, most brief cognitive screening tests do not assess for these forms of neglect, and this patient illustrates the importance of evaluating patients with degenerative disorders for these disorders. Posterior Cortical Degeneration and Spatial Neglect To be classified as DLB, the patient needs to exhibit at least two major features. This patient did have three core features of DLB, including visual hallucinations, variations in attention and alertness, as well as cogwheel rigidity. Thus, according to Crutch and colleagues (2017), he may be classified as a PCA with additional features (PCA-plus). Andrade, Kas, and Valabrègue (2012) reported that signs of horizontal neglect are associated with PCA, and the presence of vertical (altitudinal) neglect has recently been reported in a patient with PCA (Glazer et al., 2017). Unlike the patient reported by Glazer and colleagues (2017) who had neglect of upper visual space, this report describes a patient who had neglect of lower space. Rapcsak, Cimino, and Heilman (1988) reported a patient with bilateral parieto-occipital infarctions, who demonstrated egocentric lower spatial altitudinal neglect on both visual and tactile bisection of vertical rods. Unlike Rapcsak and colleagues’ patient, our patient had a degenerative disease. Furthermore, on the horizontal line bisection test, our patient revealed evidence of horizontal neglect with deviation toward the left. We think that these two forms of spatial neglect were additive, and it was the combination of these forms of mild downward vertical neglect together with a mild form of rightward horizontal neglect that together induced the more severe right lower quadrant neglect. Egocentric and Allocentric Neglect The term egocentric neglect is used when a patient is inattentive or unaware of the stimuli that are on one side of his or her body or head. Heilman and Valenstein (1979) had patients with left hemispatial neglect perform horizontal line bisections in three portions of egocentric space: left, center, and right of their midsagittal plane. When presented in left hemispace, these patients’ right-sided bias on line bisection became more severe than when presented in right hemispace. This difference indicates that these patients were neglecting the stimuli located at the left side of their body and head (egocentric). Allocentric neglect is the condition where a patient is inattentive or unaware of a part of an object or objects and this unawareness appears to be unrelated to the position of this object in relation to the patient’s head and body. In general, when patients have a spatial deviation on the line bisection test, as did the patient in this report, it is possible that this is a sign of allocentric or egocentric neglect. However, when this stimulus is located in different parts of egocentric space and there are alterations of the severity of neglect, this result suggests the presence of egocentric neglect. On the line bisection task, our patient demonstrated egocentric neglect. As mentioned, this patient did not reveal strong evidence for right lower spatial egocentric spatial neglect on the cancelation test. We could only find one article that discussed PCA and allocentric neglect, and in this prior report, the patient had right-sided allocentric neglect (Zilli & Heilman, 2015). Whereas our patient had both lower spatial allocentric and egocentric neglect, there have been lesion studies, which do reveal that horizontal (right-left) allocentric neglect and egocentric neglect are dissociable and that different lesion sites are often associated with these two forms of spatial neglect. For example, Verdon, Schwartz, Lovblad, Hauert, and Vuilleumier (2010) suggested specific involvement of the right inferior parietal lobule for the development of egocentric visuospatial neglect and temporal lobe regions for the presence of allocentric object-centered neglect. Another study suggested that damage to the supramarginal and superior temporal gyri induced egocentric neglect and damage to the middle temporal, and middle occipital gyri were associated with allocentric neglect (Chechlacz et al., 2012). These findings are consistent with the postulate that whereas the parietal lobe mediates global attention, important in determining “where,” the more ventral temporal occipital areas mediate more focal intention, important in determining “what” (Goodale & Milner, 1992). We could not find any studies of patients with focal lesions that demonstrated lower allocentric neglect, and further research will have to be performed to learn the anatomic and physiological basis of this disorder. Localization and Pathology of Quadrantic Spatial Neglect Binder, Marshall, and Lazar (1992) examined the association between the results of the line bisection and cancelation tests for the detection of spatial neglect. These investigators found no significant correlation between these two tests. Further, these investigators found that all the patients with neglect on the cancelation test, but not line bisection, had a frontal or subcortical lesion. In contrast, patients with posterior lesions had deviation on the line bisection test but often had minimal or no cancelation deficit. Although Binder and colleagues performed their tasks on a tabletop (transverse plane) and we performed our tests vertically (coronal plane), our results are similar to those of Binder and colleagues’ in such a way that our patient with PCA had an egocentric spatial bias when performing line bisections but not on cancelation test. The cancelation test requires a systematic visual search and the allocation of focal attention. Whereas these activities are primarily mediated by the frontal lobes, there are reports of patients with injury to the posterior temporal and inferior parietal lobe who did reveal impairment on the line bisection and cancelation tests (Ten Brink et al., 2016). In contrast to the cancelation test, the line bisection test is more dependent on the allocation of global attention. Our patient revealed egocentric lower spatial inattention together with right horizontal inattention, and these combined deficits produced right lower quadrantic neglect. On the line bisection tests, the presence of right-sided lower visuospatial neglect would suggest that this impairment is most likely related to the degeneration of the left parietal lobe. In addition to this neglect, this patient had many other signs of a left inferior parietal impairment, including an ideomotor apraxia, agraphia, alexia, acalculia, right-left confusion, and anomia. However, this patient also had evidence of other disorders, suggesting degeneration in other areas. For example, this patient had prosopagnosia and this disorder is most often associated with injury to the right fusiform gyrus (Barton et al., 2002). Based on the work of Binder and colleagues (1992) as well as the more recent research by Rorden and colleagues (2006), patients with a degenerative disease such as PCA or AD should be assessed with line bisections in all three directions (horizontal, vertical, and radial) as well as cancelation tests that assess allocentric and egocentric attention (Hillis, 2006). Bender and Teuber (1948) described a 20-year-old sailor who, during the Second World War, sustained a shrapnel injury to the right occipital area (based on skull x-rays). In addition to having a scotoma of his left inferior visual field, he appeared to neglect the stimuli in his left lower quadrant of space. Previous reports have indicated that even in the absence of a scotoma or visual field defect, testing patients with both the line bisection and cancelation tests have revealed neglect of the left lower spatial quadrant, and these patients with this left lower neglect most often had strokes of the right inferior parietal lobe (Halligan & Marshall, 1989; Mark & Heilman, 1997; Mark & Heilman, 1998; Pitzalis et al., 1997). In addition, when attempting to bisect diagonal lines that go from the bottom of the page on the left side to the top of the page on the right side, patients with right parietal lesions deviated more than when attempting to bisect lines that went from lower right side to upper left side (Mark & Heilman, 1997). Thus, lower left quadrantic neglect is thought to be related to the right parietal lobe’s mediating attention to both left hemispace and lower (inferior) hemispace. On brain imaging, our patient appeared to have degeneration of his left parietal lobe. However, unlike the prior patients with quadrantic neglect who suffered with a stroke, this patient has a degenerative disease that was most likely a form of PCA. In addition, his quadrantic neglect was on his right side, and in prior reported patients with strokes who manifest the signs of quadrantic neglect, this deficit has been on the left side. However, while less common, some patients with strokes of their left parietal lobe do develop right-sided neglect (Ten Brink et al., 2017), and it is possible that some of these patients with left parietal strokes will have right lower quadrantic neglect. In addition to right lower egocentric (viewer-centered) quadrantic spatial neglect, this patient also revealed allocentric (object-centered) neglect. When performing a cancelation task where the patient was required to cancel only those squares that have opening on the top or bottom of the square, this patient failed to cancel 66.7% (8/12) of the squares with the openings on the bottom but only 25% (3/12) of those squares with the openings on the top. Right hemispatial allocentric neglect had been previously described (Zilli & Heilman, 2015) with PCA. However, our patient reveal lower (ventral) vertical allocentric neglect, which to our knowledge has not been reported with PCA. The pathological changes in this patient’s brain that may have induced this quadrantic neglect are not known. The underlying histopathology at the autopsy of patients with PCA is most commonly that of AD. However, PCA is infrequently associated with other forms of dementia including DLB, corticobasal degeneration, Pick’s disease, and prion disease (Alladi et al., 2007; Renner et al., 2004; Tang-Wai et al., 2004). It is therefore possible that this patient’s underlying pathology is DLB because in addition to this patient having attentional impairments and difficulties with visual perception, he had visual hallucinations, episodes suggestive of brief behavioral arrests, and parkinsonism traits—signs that are often associated with DLB (McKeith et al., 1996). Limitations and Possible Future Studies The tests we performed with this patient were all performed during single clinic visit and, therefore, there are several limitations of this study. Whereas with the open-square cancelation test, this patient revealed lower object-centered (allocentric) neglect, we unfortunately did not test this patient for horizontal allocentric neglect by having him cancel only those squares or circles that have an opening to the left or right. We were also unable to perform horizontal line bisections and cancelation tests in all four egocentric quadrants in this patient’s coronal plane. Using the Landmark Test, where no arm actions are necessary, may have also allowed us to determine if this patient’s deficit on line bisection was, at least in part, related to an action-intentional bias rather than an attentional bias. On the mapping test, this patient was unable to locate two states on the left side of this map of America. This impairment appears to be inconsistent with the tests that revealed this patient had right-sided neglect. Unfortunately, we did attempt to learn if this was a deficit or a lack of knowledge that existed before the onset of his disease. Mapping in some respect is dependent on imagery and it has been reported that patients with posterior cerebral lesions may have neglect-like impairments in imagery. For example, Bisiach & Luzzatti (1978) reported patients with unilateral spatial neglect that also had spatial neglect when using imagery. In addition, although visuoperceptual and imagery neglects often occur together, they may also be doubly dissociated (Wansard et al., 2016). Therefore, it is possible that whereas this patient had right-sided visuoperceptual neglect, he might have also had left-sided imagery-representational neglect. Unfortunately, we did not test for this disorder and future studies should examine this possibility. Another weakness of this study is that we did not test a healthy control population with all the tests we used for this patient but relied on prior studies that had some minor differences. Patients with neglect might sometimes vary their performance on repeated trials and, unfortunately, we were unable to perform many trials during this patient’s clinic visit. Based on their study of more than 250 patients with right brain injury, Guariglia and colleagues (2014) concluded that using a battery with multiple tests is the best means of obtaining a full understanding. Therefore, future studies examining patients with PCA for similar deficits should be performed. In addition, several of the tests used to evaluate this patient for spatial neglect have not been standardized and there is a need to standardize tests that assess for vertical allocentric and quadrantic neglect. Although there have been case reports of patients with PCA who appeared to benefit from treatment with an anticholinesterase medication that are often used to treat AD (Kim et al., 2005), we could find no reports of the effects of medications, such as an anticholinesterase or memantine, on the spatial neglect that can be associated with PCA. However, in a recent review of the post-stroke pharmacologic treatment of neglect, van der Kemp, Dorresteijn, and Ten Brink (2017) do suggest that anticholinesterases are effective in the post-stroke treatment of neglect. Therefore, the effect of these cholinergic medications on patients with neglect associated with PCA should be studied. 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TI - Posterior Cortical Atrophy with Right Lower Egocentric Quadrantic Neglect and Lower Vertical Allocentric Neglect
JF - Archives of Clinical Neuropsychology
DO - 10.1093/arclin/acz078
DA - 2020-05-22
UR - https://www.deepdyve.com/lp/oxford-university-press/posterior-cortical-atrophy-with-right-lower-egocentric-quadrantic-9p8L1wBDRs
SP - 448
EP - 457
VL - 35
IS - 4
DP - DeepDyve
ER -