Apraxic Agraphia With Neglect-induced Paragraphia Edward Valenstein, MD, Kenneth M. Heilman, MD \s=b\ Agraphia may result from the loss or unavailability of the memory of move- ments necessary to form written letters. For this mechanism to be invoked, it must first be demonstrated that there is no language deficit and that there is no disconnection between language and motor areas. A left-handed patient demonstrated bilateral agraphia and apraxia, but not aphasia, following a right parietal infarction. Preservation of the ability to type with the left hand demonstrated that the right hemisphere was not disconnected from language input. In addition, paragraphic errors while typing were shown to be secondary to left hemispatial neglect. (Arch Neurol 36:506-508, 1979) XJeilman et al1 described a lefthanded patient in whom agraph¬ ia, but not aphasia, developed fol¬ lowing a large lesion in the middle cerebral artery territory of the right hemisphere. The patient had a left hemiplegia but, in addition, he had severe apraxia of his right hand and he could not write with his right hand, even though he had always done so prior to his stroke. Heilman et al1 proposed that in this patient, the left hemisphere was dominant for lan¬ guage but, as the patient was left handed, the right hemisphere was dominant for fine motor control. For the patient to write, he had to transfer information from the left (language) hemisphere to the right (motor) hemi¬ sphere. To write with the right hand, Accepted for publication Nov 28, 1977. From the Department of Neurology, University of Florida College of Medicine, Gainesville. Reprint requests to Department of Neurology, Box J-236, JHMHC, University of Florida, Gainesville, FL 32610 (Dr Valenstein). the right hemisphere had to direct the left motor cortex to make the appro¬ priate movements. Despite the coexis¬ tence of apraxia and agraphia, the authors1 were reluctant to attribute the patient's agraphia to apraxia since it was possible that the defect in writ¬ ing resulted from the unavailability of linguistic input to the right hemi¬ sphere rather than from the unavaila¬ bility of the engrams for forming the letters. Since the patient had a left hemiplegia, the right hemisphere could not be tested to see if it had access to linguistic input. Heilman et al- subsequently reported an analo¬ gous case in which the same problem in interpretation arose. In this case, a large lesion in the left hemisphere of a right-handed patient produced a dense right hemiplegia, but no apha¬ sia. Apraxia and agraphia of the patient's left hand developed. Again, the right hemiplegia prevented test¬ ing the possibility that the left hemi¬ sphere was cut off from linguistic input from the language-dominant right hemisphere. We now describe a patient in whom agraphia and apraxia, but not aphasia, were produced from a lesion restricted to the right parietal lobe. Since the patient was not hemiparetic, the right hemisphere could be tested for its access to linguistic information. REPORT OF A CASE The patient was a 74-year-old retired executive vice-president with a tenthgrade education. He was left handed: writ¬ ing, throwing a ball, using scissors, comb¬ ing his hair, and using a knife (among other activities) were all performed with his left hand. There was no family history of left-handedness. He had adult-onset diabetes, which was treated with small doses of insulin, and he had suffered three Downloaded From: http://archneur.jamanetwork.com/ by a Monash University Library User on 06/17/2015 myocardial infarctions during the previous 20 years. He had no symptoms of neurological dysfunction until May 23, 1977, when he awakened with a headache. His wife noted slurred speech and "confusion" and brought him to a local hospital where he was thought to be hypoglycémie. His serum glucose level, however, was 300 mg/dL. His speech and "confusion" improved and he was discharged after two days. He remained unable to dress himself and unable to write, and he was therefore referred to the Shands Teaching Hospital, Gainesville, Fla, for further evaluation. When the patient was examined on June 8, 1977, his blood pressure was 140/55 mm Hg, his pulse rate was 50 beats per minute and regular, and he was afebrile. The general physical examination was without abnormalities except for a soft systolic murmur heard only over the aortic area. His heart was not enlarged, his chest was clear, and there was no peripheral edema. Neurological examination demonstrated extinction of bilateral simultaneous visual, auditory, and tactile stimuli on the left. Cranial nerve examination showed full visual fields and normal fundi. There was minimal left facial weakness, but no other cranial nerve deficit. There was no weak¬ ness of his extremities. There was upward ("parietal") drift of the extended left upper extremity with the eyes closed. Sensory examination showed normal vibra¬ tion and proprioception in both hands. The muscle stretch reflexes were more brisk on the left than the right. There were bilateral Babinski responses. There were no grasp, root, or suck reflexes. He was alert, attentive, and fully oriented. His digit span was seven num¬ bers forward. He recalled three of three items after five minutes. Remote memory was normal. Topographical localization was done well. He was mildly dysarthric, but there was no other disturbance of spoken language; language comprehension, repetition, and object naming were all absolutely normal. He could read aloud and for comprehen- C] ^^us O /ÎcQr?àssû/s\9/Q^ ND tO YER DGO zbrqha mlincoln 3 AM 4 SVORQ FOUR IN I AM THE IN HOSPITLW GWINEV ILLLLL HOSPITL THE AT E . FL GAINSVILLLLE QWERTYUIO X C V M Fig 1 .—A, Spontaneous writing: patient attempting to write, "You are a doctor." B, Copying. C, Typewriting. C, 1 to 3, Typewriter directly in front of patient. C, 4, Typewriter moved to patient's right side. D, The typewriter keyboard. Note that most of letters missed (A, S, and E) are on left side of keyboard. The patient demonstrated remarkable apraxia, both of face and of limb move¬ ments. He understood the commands, and the limb movements produced were clumsy imitations of the correct movement. His performance did not improve with imita¬ Fig 2.—Computerized tomographic scans with contrast enhancement, demonstrating moderate diffuse cortical atrophy, and a distinct lentiform area of contrast enhancement in right posterior parietal region. This area was of decreased density on noncontrast scan. sion. He could spell accurately, and he understood words spelled to him. In contrast, he could not write even his name. Attempts at writing produced large, poorly formed letters, only a few of which were identifiable. There was no improvement when writing to dictation (Fig 1, A) or copying (Fig 1, B). He spontaneously used his left hand for writing; performance with his right hand was poorer. Typewriting with one finger of his left hand (he had never learned to touch type) was per¬ formed better than writing, but there were still many errors (Fig 1, C,_3). When it was realized that nearly all of these errors were made when he tried to type letters on the left side of the keyboard, the typewriter was moved to the patient's right side. His typewriting (still with his left hand) improved sharply; in striking contrast to his writing, he was able when typing to complete whole sentences with only minor errors (Fig 1, C4). The patient's wife reported his typewriting to be slightly worse with the right hand than with the left. tion. The limb apraxia was bilateral, slight¬ ly worse on the right. Routine laboratory study results were normal, and the serum VDRL test was negative. A lumbar puncture yielded clear, colorless fluid under normal pressure. The CSF protein level was 121 mg/dL, and there were eight mononuclear cells per cubic millimeter. The CSF cultures were negative. The EEG showed generalized right hemisphere slowing in the theta range, which was most pronounced posteri¬ orly. A computerized tomographic scan done 17 days after the onset of his illness showed a discrete area of decreased densi¬ ty in the right posterior parietal region, which enhanced with contrast (Fig 2). There was no mass effect. In addition, mild ventricular dilation and moderate cortical atrophy were noted. No other focal lesions Downloaded From: http://archneur.jamanetwork.com/ by a Monash University Library User on 06/17/2015 were apparent. COMMENT In our patient, most of the common agraphia could be excluded on the basis of the clinical examina¬ tion. Thus, our patient was not aphasie or alexic, and he lacked the other features of the Gerstmann syndrome. There was no evidence of a mass lesion, and he was not confused.3 causes of There was no gross visuospatial disorientation. He did have definite neglect of the left half of space. Patients with unilateral neglect may demonstrate "spatial dysgraphia"4: their writing does not maintain a straight line and is crowded to one side of the page. Their writing is nevertheless legible. Our patient showed only a slight tendency to write on the right side of the page; however, in contrast to patients with spatial dysgraphia, he had difficulty correctly forming even a single letter. Agraphia may be seen in the absence of aphasia as a result of a disconnection of motor centers from linguistic control."1 The combinations of agraphic and apraxic features possible in patients with callosal lesions depend on the patterns of hemisphere dominance in the individ¬ ual patients, and these have been discussed in detail by Heilman et al.1 In the patient with left hemisphere dominance for language, a callosal lesion will produce agraphia in the left hand since the right hemisphere is deprived of linguistic input. Although, theoretically, ipsilateral pathways for crude motor activity might be avail¬ able to enable the left hand to type, the patient described by Geschwind and Kaplan6 with a callosal disconnec¬ tion could not write, type, or arrange anagram letters with his left hand although he could do all three with his right. In contrast, our patient could write with neither hand, but he could use his left hand for typewriting. The fact that he spontaneously used his left hand for typewriting is further evidence that ipsilateral pathways from the left hemisphere were not being used (the left hemisphere should preferentially use the right hand). We conclude that his right hemisphere did have access to language and that his agraphia cannot be explained on the basis of a disconnection of language from motor areas. We propose instead that he lost the memory of the move¬ ments necessary to form written letters. His agraphia can thus be regarded as a specific type of apraxic disorder. Apraxia is frequently seen in asso¬ ciation with left-sided post-Rolandic lesions, including lesions in the parie¬ tal lobes.7 8 Recent electrophysiologi¬ cal work" has identified single cells in areas 5 and (especially) 7 that appear to have a premotor ("command") func¬ tion. Liepmann7 proposed that visuokinesthetic-motor engrams were en¬ coded in these posterior regions. Handedness might reflect an asym¬ metric representation of these engrams. The right-hander thus has bilateral apraxia from left parietal lesions; the left-hander might be expected to become bilaterally apraxic from right parietal lesions. Our patient's lesion was well circum¬ scribed and involved the posterior parietal cortex, which included the inferior parietal lobule and spared the postcentral gyrus and the frontal lobes entirely. It is conceivable that a lesion restricted to the frontal premo¬ tor cortex would have produced a simi¬ lar disorder of praxis and writing in this patient by interfering with the execution of these functions by the premotor and motor cortex. It is possi¬ ble that this mechanism explains some of the cases of agraphia reported from frontal lesions. It is worth noting that our patient's performance on the typewriter not only demonstrated that his right motor cortex had access to linguistic input but also brought out a spatial paragraphia that was only slightly apparent in his written productions. Neglect of the far left side of the typewriter produced errors in type¬ writing (neglect-induced paragraphic errors) that, if more severe, could easi¬ ly have been mistaken for a linguistic deficit. The failure in the previous two patients with agraphia described by Heilman et al1·2 to use anagram letters and to type was thought to be on this basis. However, the defects were not studied systematically and the au¬ thors1-2 could not exclude the possibili¬ ty that a linguistic deficit was also contributory. The simple expedient of moving the typewriter into our patient's normal field eliminated al¬ most all of these typing errors. This maneuver was important not only for theoretical reasons; it also enabled the patient to carry on his correspon¬ dence, which he could not have done alone in any other way. This investigation was supported by grant NS 12218-01A2 from National Institutes of Health and by funds from the Medical Research Service of the Veterans Administration. References 1. Heilman KM, Coyle JM, Gonyea EF, et al: Apraxia and agraphia in a left-hander. Brain 96:21-28, 1973. 2. Heilman KM, Gonyea EF, Geschwind N: Apraxia and agraphia in a right-hander. Cortex 10:284-288, 1973. 3. Ch\l=e'\druF, Geschwind N: Writing distur- bances in acute confusional states. Neuropsycho- logia 10:343-353, 1972. 4. De Ajuriaguerra J, H\l=e'\caenH: Le Cortex C\l=e'\r\l=e'\bral.Paris, Masson et Cie, 1960. 5. Liepmann H, Maas O: Ein fall von linksseitiger agraphie and apraxie bei rechtsseitiger L\l=a"\hmung.J Psychol Neurol 10:214-227, 1907. 6. Geschwind N, Kaplan E: A human cerebral disconnection syndrome. Neurology 12:1678-1685, 1962. 7. Liepmann H: Apraxie. Ergbn Der ges Med 1:516-543, 1920. 8. De Ajuriaguerra J, Tissot R: The apraxias, Downloaded From: http://archneur.jamanetwork.com/ by a Monash University Library User on 06/17/2015 PJ, Bruyn GW (eds): Handbook of Clinical Neurology. Amsterdam, North-Holland Publishing Co, 1969, vol 4, pp 48-66. in Vinkin 9. Mountcastle VB, Lynch JC, Georgopoulous A, et al: Posterior parietal association cortex of the monkey: Command functions for operations within extrapersonal space. J Neurophysiol 38:871-908, 1975.