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Home , Acalculia, Agraphia, He (kana), Ki (kana)

3'ournal ofNeurology, Neurosurgery, and 1995;58:629-632 629 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.58.5.629 on 1 May 1995. Downloaded from SHORT REPORT

Agraphia and after left prefrontal (F1, F2) infarction

Hideo Tohgi, Kou Saitoh, Satoshi Takahashi, Hiroaki Takahashi, Kimiaki Utsugisawa, Hisashi Yonezawa, Kentaro Hatano, Toshiaki Sasaki

Abstract been working in a construction company. His A patient presented with and job was mainly procure building materials. acalculia associated with a left frontal For six years before admission had dia- (Fl, F2) infarction. He made mainly betes and hypertension, which were being phonological but also lexical errors in treated but he had been in normal health. writing (syllabograms), but his ability to Two days before admission, when he was write (morphograms) was relatively talking with a carpenter, he suddenly became preserved. Although he could add and unable to respond with even a single word. subtract numbers, he could neither mul- On admission, he was alert and well ori- tiply nor divide them because of a diffi- ented for both time and space. Neuro- culty in retrieving the multiplication logically, he had a mild right hemiparesis and tables and calculation procedures. a mild stocking type sensory disturbance due Positron emission tomography showed to diabetic neuropathy. Computed tomogra- decreased cerebral blood flow and phy and MRI showed a haemorrhagic infarc- metabolism limited to the infarct site. tion in the left ; the high intensity These findings suggest that agraphia and area on T2 weighted MRI involved mainly acalculia may occur associated with a left the , the upper part of the prefrontal lesion, and that the retrieval , and part of the precen- of arithmetic processes is modality spe- tral gyrus (figure, A, B). In other areas, only a cific. few lacunes were found. Brain PET studies showed a severe (- 70%) reduction in (7 Neurol Neurosurg Psychiatry 1995;58:629-632) regional cerebral blood flow (CBF) and meta- bolic rate of oxygen (CMRo2) in the left pre- frontal area (figure, C). CBF and CMRo2 http://jnnp.bmj.com/ Keywords: agraphia; acalculia; prefrontal cortex were some 20% less than controls in the supramargical and angular gyri, and the Pure agraphia was first ascribed to lesions in reductions were symmetric (figure, C). the premotor cortex (Brodmann's area 6) by Exner in 1881, and this view was supported LANGUAGE by early researchers.' 2 Many later studies, The Japanese writing system consists of kana

however, reported agraphia associated with and kanji. Kana are syllabograms represent- on September 24, 2021 by guest. Protected copyright. Department of parietal lesions,37 implicating the angular ing vowels (a, , , , ) or combinations of , Iwate consonants m, with vow- Medical University, gyrus as a graphic centre,89 or to interruption (k, s, t, , h, y, r, w) Morioka, Japan of the transfer of writing information between els (, , etc) and most kana are ortho- H Tohgi the parietal and frontal cortices.10 More graphically regular. Kanji are morphograms, K Saitoh or from Chinese char- S Takahashi recently there have again been reports of ideographs, developed H Takahashi some patients with pure agraphia due to acters, and are read using the original K Utsugisawa frontal lesions. 11-14 An isolated acalculia Chinese sound or the Japanese sound-for H Yonezawa (anarithmia) has been also ascribed to a instance, a kanji meaning "east" is read as Nishina MemorWial parieto-occipital lesion in most cases,'5-"7 but [tou] (original sound) or as [higashi] Cyclotron Center to a one 18 on the context. (Japan Radioisotope frontal lesion in patient. Some (Japanese sound) depending Association) and patients with agraphia or acalculia showed All Japanese sentences can be written with Cyclotron Research dissociations between different orthographic'4 kana only, but are usually written with both Center, Iwate Medical 19-21 22-24 University, Morioka, or arithmetical operations,'6 suggest- kanji (for nouns and roots of verbs, adjec- Japan ing domain specificity of individual processes tives, and adverbs) and kana (for inflexions, K Hatano in the writing and calculation system. conjunctions, and propositions). T Sasaki describe a patient with pure agraphia and A week after onset, his auditory and read- Correspondence to: Dr Hideo Tohgi, acalculia associated with a left frontal lobe ing comprehension of words and sentences Department of Neurology, (Fl, F2) infarction. were normal (28/30, 93% for each), but his Iwate Medical University, 19-1, Uchimaru, Morioka, ability to carry out oral and written com- 020 Japan. mands (such as to place a coin and a foun- Received 2 August 1994 Case report tainpen on a handkerchief) was severely and in revised form 17 October 1994. The patient, a 59 year old, right handed man impaired (3/19, 30% for each). He could cor- Accepted 27 October 1994 had had 11 years of formal education and had rectly choose a kana that corresponded to a 630 Tohgi, Saitoh, Takahashi, Takahashi, Utsugisawa, Yonezawa, Hatano, Sasaki J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.58.5.629 on 1 May 1995. Downloaded from

(A) T2 weighted MRI of horizontal planes (TR = 2500, = 110) at level of ; (B) at level ofcentrum semiovale; the infarct area includes mainly Brodmann's areas 6 and 8, and a posterior part of area 9, but spares area 44; (C) PET images of cerebral bloodflow (CBF), and cerebral metabolic rate ofoxygen (CMRo,) in the horizontal planes 60 and 70 mm above and parallel to the orbitofrontal (om) line (8 weeks after onset using Headtome IV, Shimadzu, _Japan, with thefull width at half maximum of 4-5 mm). The CBF and CMRo, were determined using C'502 inhalation methods and 1502 respectively. The right side of the head is on the left in allfigures. The CBF and CMRo2 are profoundly decreased in the left prefrontal areas (arrowheads). Quantitative data are as follows (mlllOO mllmin): prefrontal area, CBF 33-8 and CMRo2 2-42 on the right, and CBF 12 2 and CMRo2 0-79 on the left; supramargznal gyrus, CBF 33-6 and CMRo2 2-51 on the right, and CBF 32-8 and 2-42 on the left; , CBF 29-8 and CMRo2 2-45 on the right, and CBF 31 7 and CMRo2 2 58 on the left; and control values, CBFG 40 and CMRo2 - 3 0.

pronounced by the examiner included (table) (a) omission of phonetic (20/20, 100%), could name objects (18/20, marks (two dots on the right upper corner of

90%), and could repeat words orally that a kana) to convert voiceless consonants to http://jnnp.bmj.com/ were spoken by the examiner (10/10, 100%). voiced ones (for example, h to b, k to g, s to He could describe what a person was doing z, and t to d), or of those to convert h to a on single action pictures (7/10, 70%), but voiceless bilabial sound p (a small circle on could not narrate a story for composite pic- the right upper corner of a kana) (60%); (b) tures. He could read aloud and comprehend difficulty in writing kana that are used to perfectly single kana words written in kanji denote double vowels, or to prolong the and kana and sentences composed of both precedent kana's sound (kya, kyo, kyo, or kana and kanji (25/25, 100% for each). If he hou, kou) (14%); (c) confusion with a graphi- on September 24, 2021 by guest. Protected copyright. was asked to say as many words as possible cally similar kana (4%); (d) confusion with (word naming), he said only two words (con- phonetically similar kana (2%); (e) confusion trol > 12). His writing ability was severely with orthographically irregular kana (8%); impaired: the correct responses were far less and U) failure to complete a word (12%). He frequent for spontaneous writing (1/25, 4%) also made similar errors in writing non- than for dictation (7/25, 28%; x2 = 5-4, words. Although Japanese kana are in most p < 0 025). cases orthographically regular, there are a few His linguistic abilities gradually recovered exceptions: the subject of a sentence is indi- after admission. Seven weeks after onset, he cated by a kana postposition "" which is made almost errors in speaking, listening, pronounced as []; the object of a sentence and reading, but made many errors in writ- is indicated by a postposition written by a ing. His writing errors for kana (24/62 words, kana used for "" in ancient times which in 39%) were significantly more frequent than modern Japanese is pronounced simply as for kanji (4/65 words, 6%) (P < 0 001). His "o". He almost always wrote kana "wa" oral responses to 60 pictures of the Boston instead of "ha" as the postposition for the naming test (40-55 for the average Japanese) subject, and kana [o] instead of "wo" for the were correct for 45 pictures (75%), but his object, which was inconsistent with his 11 graphic responses were correct for 31 pictures year educational history. He could correctly (52%)-that is, he made errors in writing in copy words both in kanji and kana. The kanji 14 out of 45 words (31 %) that he could character is composed of a radical that is express orally. His writing errors for kana related to its meaning (semantic component) Agraphia and acalculia after a left prefrontal (Fl, F2) infarction 631

Examples ofwriting errors of the patientfor kana (footnote 1 to 6) and kanji (footnote 7 and 8) The writing is generated by semantic or J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.58.5.629 on 1 May 1995. Downloaded from phonological inputs to in the lin- Types ofer-r-ot-s Cor-rect Japaniese word Patient's writing English meaning guistic processes, and then is processed I Ak-t (/zuI) br (mi/) Water through an orthographic buffer, physical let- 1 + 6 A&s (eln/pi/) i.Ax-_ (e/nb/tsu) Pencil ter code, graphic motor pattern, and graphic 2 Cf 1, (bo/u/) (f lU (bo/shi) Hat code in the peripheral aspects.2' Our patient's [bo:shi] ability to select correct kana and kanji from a 2 4 A < (sa/n/ki/ya/ku) AJbj < (sa/n/ka/ku) Tripod [sankyaku] visual array indicates an intact physical letter 3 A, (/n) ak (/n) Mask code. His ability to write well formed kana 4 UjL 531 (bi//u/bu) AJ -) . (_2I/yo/u/bu) Screen and kanji, although with some confusions for [byo:bu] morphologically or phonetically similar kana, 4+6 I (/) lft(yl/-) Hill suggests that his lexical and non-lexical 5 VLW (watakushi wa) fLA2 (watakushi wa) I am , orthography, and motor 5 fIA (watakushi o) VL4 (watakushi o) To me 2 + 3 + 6 C- tAAk7& j (/u//n//u) Uhak j (ho//n/-/u) Spinach programmes (graphic motor pattern) were [ho:renso:] relatively intact. The main feature of phono- I + 2 + 6 U e1 L (ji/do/u/shilya) LC (ji/to/...) Automobile logical agraphia as contrasted with lexical Uido:shya] agraphia in Indo-European languages is the 7 {ff (/do/) T Child disproportionate failure in writing non-words, 8 41 (tsu/ku/e) j$ff Desk probably because each word (for example, Pronunciations for individual kana are shown in parentheses, and pronunciations for double water) is recognised as if it were an ideogram vowels in square brackets. a 1 = Omission of a mark (double dots at the right upper corner of a kana) to convert k to g, s to (whole word reading) rather than simple z, t to d, and h to b, or omission of a mark (a small circle at the right upper corner of a kana) to combination (w-a-t-e-r) of alphabetical let- convert h to p, or omission of kana denoting pa, pi, pu, pe or po; 2 = difficulty in writing kana that are used to denote a double vowel, or to prolong a precedent kana's sound; 3 = confusion ters. This is not usually the case in Japanese with a graphically similar kana; 4 = confusion with a kana representing similar sound; 5 = errors because kanji are ideograms and because in orthographically irregular kana; 6 = failure to complete a word; 7 = errors in writing the radi- = there are no spaces between words in kana cal (left half) of kanji; 8 errors in writing the non-radical portion (right half) of kanji. writing (like writing "iamalondoner." instead of "I am a Londoner." in English). Although and a non-radical portion that may provide a our patient showed no dissociation between clue as to its Chinese way of reading (pho- the writings of real words and non-words, the netic component). The patient's errors in relative preservation of writing kanji com- writing kanji were in either the radical or non- pared with kana and the most frequent errors radical portions (table). in using phonetic marks to convert pronunci- ations of consonants suggest that impair- CALCULATION ments of phoneme- conversion may A week after onset, he could only perform be the main cause of his agraphia. The failure additions of one digit numbers not including to construct double vowels by combining carrying (for example, 3 + 2 = 5), but could kana that are originally pronounced differ- not add numbers requiring carrying processes ently (for example, kyou (today) from ki-yo- (for example, 7 + 5 = 7 instead of 12), or u) may apparently resemble those in surface subtract one digit numbers. Multiplication in Indo-European languages in

and division were totally impossible because which patients write phonetically correct but http://jnnp.bmj.com/ he could not remember the multiplication lexically incorrect words because of an tables. He could, however, indicate which of impairment of the lexical route.'920 This view, the paired two numbers was greater, and however, cannot be applied to the findings in write numbers corresponding to the numbers our patient's errors in Japanese. In French, spoken, suggesting that he could read, under- for example, one cannot, like in kanji writing, stand, and write digits. write "eau" (/o/; water) without knowing its Seven weeks after onset, he became able to meaning, and the sound IoI is phonetically add and subtract up to three digit numbers ambiguous because it may be written in sev- on September 24, 2021 by guest. Protected copyright. with carrying and borrowing. He sometimes eral different ways (o, au, aux, etc). By con- succeeded in multiplying or dividing one digit trast, the Japanese phoneme-grapheme numbers, but still often made errors (for system is not ambiguous because one can example, 4 x 6 = 48 instead of 24, or 9 + 3 write "kyou" using kana "ki-yo-u" without = 9 instead of 3). He could not multiply or knowing its meaning, and there is no alterna- divide two digit numbers, because of diffi- tive way of writing the same sound. By con- culty in completely remembering the multi- trast, our patient's errors in writing plication tables, and an inability to retrieve orthographically irregular kana that are used calculation procedures (for example, 18 x 8 as postpositions for subjects and objects of - 74 instead of 144). sentences indicate that the patient could not Eight weeks after the onset, his Wechsler correctly write different kana for the sound /oI adult intelligence score (WAIS) was 71 for and /wa/ depending on its syntactic signifi- the verbal tests and 89 for the performance cance. In addition, our patient's more severe tests. impairments of spontaneous writing than of writing to dictation, similar to the discrep- ancy between impaired spontaneous speech Discussion and preserved repetition and comprehension The main findings are the rare associations in transcortical motor , suggest that between pure agraphia and acalculia with a his lexical and semantic routes may also be left frontal lesion and the patterns of ortho- disturbed. graphic and arithmetic errors. Agraphia associated with a left frontal 632 Tohgi, Saitoh, Takahashi, Takahashi, Utsugisawa, Yonezawa, Hatano, Sasaki

lesion is rare: one patient described by The present case illustrates that further J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.58.5.629 on 1 May 1995. Downloaded from Gordnier' could not write or correctly form a careful studies on patients with frontal lesions single letter, and those described by Aimard may provide opportunities to reveal the func- et all and Hodges"3 could write letters and tion of the frontal lobe in writing and calcula- words correctly but extremely slowly and tion. laboriously. Agraphia in these patients may probably be due to kinaesthetic writing disor- We thank Ms Hiroko Ishikawa for her help in the neuropsy- ders. The patient reported by Rapcsaket al14 chological testing, Miss Miharu Sawame for her secretarial assistance, and Dr Paul Langman for reviewing the manu- could spell non-words and regular words bet- script. ter than irregular words, with most of his errors being phonologically correct, and was diagnosed as having lexical agraphia. In our patient phonological impairment was greater than lexical impairment. 1 Gordinier HC. A case of brain tumor at the base of the The neu- second left frontal convolution, with autopsy; the only ropsychiatric characteristics of frontal positive localizing symptom was agraphia uncombined with any form of aphasia. Am .7 Med Sci 1899; agraphias seem, therefore, to be different 117:526-35. depending on the cortical areas involved. 2 Henschen . Clinical and anatomical contribution on brain pathology. Archives of Neurology and Psychiatry The preserved ability to write numbers 1925;13:226-49. despite the disorders in writing words in our 3 Alexander MP, Friedman RB, Loverso F, Fischer RS. Lesion localization of phonological agraphia. Brain Lang patient is similar to the findings in the patient 1992;43:83-95. (with a left premotor lesion) reported by 4 Auerbach SH, Alexander MP. Pure agraphic and unilat- Anderson et al,12 indicating the domain eral optic ataxia associated with a left superior parietal speci- lobe lesion. I Neurol Neurosurg Psychiatry 1981 ;44: ficity for cognitive representations. The 430-2. patient's failures in the processes of 5 Basso A, Taborelli A, Vignolo LA. Dissociated disorders carrying of speaking and writing in aphasia. .7 Neurol Neurosurg and borrowing and in remembering the mul- Psychiatry 1978;41:556-63. tiplication tables in the early period 6 Baxter DM, WarringtonEK. Ideational agraphia: a single despite case study. .7 Neurol Neurosurg Psychiatry 1986;49: his well preserved aspects of numbers is con- 369-74. sistent with isolated acalculia, not with 7 CraryMA, Heilman KM. Letter imagery deficits in a case asym- of pure apraxic agraphia. Brain Lang 1988;34:147-56. bolic (aphasic), or visuospatial acalculia.2 In 8 Benson DF, Cummings JL. Agraphia. In: Vinken PJ, one of the current models of arithmetic Bruyn GW, Klawans HL, Frederiks JAM, eds. pro- Handbook of clinical neurology. Vol 45. Amsterdam: cessing,25 the calculation system consists of Elsevier, 1985:457-72. (a) comprehension of operation signs 9 Leischner A. The agraphias. In: Vinken PJ, Bruyn GW, or eds. Handbook of clinical neurology. Vol 4. Amsterdam: words, (b) retrieval of arithmetic facts, and (c) North Holland 1969:141-80. execution of calculation procedures, 10 Croisile B, Laurent B, Michel D, Trillet M. Pure agraphia and the after deep left hemisphere haematoma. .7 Neurol retrieval of arithmetic facts may involve Neurosurg Psychiatry 1990;53:263-5. modality specific 11 Aimard G, Devic M, Lebel M, Trouillas P, Boisson D. processes.24 The dissocia- Agraphie pure (dynamique?) d'origine frontale: a propos tion between addition and subtraction and d'une observation. Rev Neurol 1975;131:505-12. 12 Anderson SW, Damasio AR, Damasio H. Troubled letters multiplication and division and between rela- but not numbers: Domain specific cognitive impair- tively retained knowledge of the multiplica- ments following focal damage in frontal cortex. Brain 1990;113:749-66. tion tables and the inability to use them seen 13 Hodges JR. Pure apraxic agraphia with recovery after in the later stage are similar to the findings in drainage of a left frontal cyst. Cortex 199 1;27:469-73. 14 Rapcsak SZ, Arthur SA, Rubens AB. Lexical agraphia http://jnnp.bmj.com/ the patient reported by Benson and Weir.'5 In from focal lesion of the left precentral gyrus. Neurology the patient with reported by 1988;38:1 119-23. 15 Benson DF, Weir WF. Acalculia: acquired anarthmetria. Luchelli and Renzi after a left medial frontal Cortex 1972;8:465-672. lesion simple calculations with square roots 16 Warrington EK. The fractionation of arithmetical skills: a single case study. QJ Exp Psychol [A] 1982;35:31-51. and powers were preserved.'8 17 Vemey NR. without aphasia: a lon- Although acalculia is most often associated gitudinal study. Brain Cogn 1984;3:1-9. 18 Luchelli F, De Renzi E. Primary dyscalculia after a medial with aphasia, a few studies have linked iso- frontal lesion of the left hemisphere. _7 Neurol Neurosurg lated acalculia with a left parieto-occipital Psychiatry 1993;56:304-7. on September 24, 2021 by guest. Protected copyright. 17 19 Coltheart M, Masterson J, Byng S, Prior M, Riddoch J. lesion.'5 A regional cerebral blood flow Surface . Q J Ex Psychol [A] 1983;35A:469-96. study in normal volunteers, however, showed 20 Beauvois M-F, Derouesne J. Lexical or orthographic agraphia. Brain 1981;104:21-49. that when the subject was attending to silent 21 Margolin DI. The neuropsychology of writing and arithmetical mental activities there was a con- spelling: semantic, phonological, motor, and perceptual processes. QJf Exp Psychol [A] 1984;36A:459-89. sistent activation of the anterior intermediate 22 Singer HD, Low AA. Acalculia (Henschen): A clinical prefrontal cortex and the middle superior pre- study. Arch Neurol Psychiatry 1933;29:476-98. 23 Dagenbach D, McClosky M. The organization of arith- frontal cortex, in addition to the supramar- metic facts in memory: evidence from a brain damaged ginal and angular gyri of both hemispheres.26 patient. Brain Cogn 1992,20:345-66. 24 McNeil JE, Warrington EK. A dissociation between addi- The results from our patient suggest that the tion and subtraction with written calculation. domains of arithmetic knowledge and of Neuropsychologia 1994;32:717-28. 25 McClosky M, Aliminosa D. Facts, rules, and procedures may be located close together, but in normal calculation: evidence from multiple single- agraphia without acalculia may occur in rare patient studies of impaired arithmetic fact retrieval. Brain Cogn 1991;17:154-203. instances as in the patient reported by 26 Roland PE, Friberg L. Localisation in cortical areas Anderson et al.'2 activated by thinking. _7 Neurophysiol 1985;53: 1219-43.