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Left-handedness and variant patterns of cerebral organization: A case study
Archives of Clinrcd Neumpsycholo#, Vol. 1, Printed in the USA. All rights reserved.
pp.357-369, 1986
Left-Handedness
~Xl77-6177/86S3.CKl
+ .OO
Copyright 0 1987 National Academy of Clinical Neuropsychologistr
and Variant Patterns
of Cerebral Organization:
A Case Study
Rodney D. Vanderploeg Research Service, St. Louis Veterans Administration
JMedlcal Center
A left-middle-cerebraI arrery infarct in a 51-year-old, nonfamilial left-handed man failed to produce aphasia, bur did resuh in imparied visuospatiul funclioning, construction dyspraxia, mild limb dyspraxiu, and iemporal/sequentiul skill dysfunction. The patienr also had severe right-sided sensory and body neglect, right-sided hemiparesis, and mildly dysarthric speech. These neurospsychological findings strongly suggest a reversed partern of cerebral organizarion. Posterior anaromical size asymmetrres were also reversed, in that rhe righr occipiralparietal area was somewhat larger than the left. However, ihis parienr’s limb dyspraxia followed no known pattern of cerebral organization. His dyspraxiu suggests rhar conlrol of complex motor skills in nonfamilial lefr-handers may remain a left-hemisphere or bilaterally represented function, even when orher cognitive abilities are reversed.
With certain notable and consistent exceptions, the pattern of cerebral organization in left-handers has been reported to follow a similar pattern to right-handers, i.e., primarily left-hemisphere representation for language abilities, and almost exclusively right-hemisphere dominance for visuospatial functions (Hecaen, de Agostini, & Monzon-Montes, 1981). However, the exceptions and variations from the typical right-handed pattern of organization have been documented by numerous investigators (Goodglass and Quadfasel, 1954; Hecaen, de Agostini, & Monzon-Montes, 1981; Hecaen and Sauguet, 1971; Humphrey and Zangwill, 1952; Luria, 1970; Satz, 1979). Patterns of language disturbance differ between left- and right-handers following similar unilateral cortical damage. Symptoms of left-handed aphasics generally do not follow the classical aphasia syndromes and are typically milder regardless of hemisphere injured. Recovery is also more rapid and complete in left-handed aphasics (Hecaen and Sauguet, 197 1;
Requests for reprints should be addressed to Rod Vanderploeg, Ph.D., who is now at Psychology Service (116B), James A. Haley Veterans Hospital, 13000 North 30th Street, Tampa, FL 33612 and is affiliated with the Department of Neurology, University of South Florida, College of Medicine.
358
R. D. Vanderploeg
Luria, 1970). Left-handers with right hemisphere impairment, often show some language disturbance in oral and written language, while right-handers with similar damage typically do not (Hecaen et al., 1981). Satz (1979) suggested a model of three types of cerebral organization for language in left-handers: left-hemisphere language dominance in 15%) right dominance in 15%, and bilateral representation in 70%. Other investigators have reported significantly higher percentages of unilateral left hemisphere language representation (7OVo), with less bilateral (IS20%), but similar percentages of right hemisphere language representation (5-15%). For reviews see Hecaen and Albert (1978) and Lishman and McMeeken (1977). A family history of left-handedness has been associated with an increased incidence of cerebral bilaterality of language representation, as well as decreased intrahemispheric language localization. On the other hand, spatial abilities in left-handers, as with right-handers, generally are right hemisphere functions, regardless of side of language dominance. The exception reported in the literature is in nonfamilial left-handers and women, where spatial abilities appear to have a higher degree of bilateral representation (Hecaen et al., 1981). Unfortunately, such group data obscure the actual pattern of cerebral specialization in individual cases. Recently, various researchers have reported that patterns of cerebral organization may vary considerably from individual to individual (Geschwind & Galaburda, 1985a, b, c; Hecaen, de Agostini, & Monzon-Montes, 1981; Heilman, Coyle, Gonyea, & Geschwind, 1973; Kimura & Harshman, 1984). At various stages of prenatal, neonatal, and later development, genetic pre-dispositions may interact with various developmental determinants (e.g., hormonal environments, cerebral insults, developmental skill practice, etc.) differentially influencing brain development and consequently affecting patterns of functional cerebral organization. In these individuals developmental cerebral specialization will have been altered at different periods and to different extents. Consequently, they will be a more variable population and need to be considered on a more individual basis (Geschwind & Galaburda, 1985a). The present study presents a nonfamilial left-hander who developed right hemiplegia without aphasia, impaired visuospatial functioning, and mild limb dyspraxia following an extensive left-hemisphere lesion secondary to a left-middle-cerebral artery infarct. This case suggests that not only may language be represented as a unilateral right-hemisphere function in lefthanders, but that spatial abilities may also be reversed from the typical righthemisphere dominance pattern. The mild limb dyspraxia was not entirely consistent with either ideomotor or ideational apraxia, but had elements of both. However, the presence of such dyspraxic symptoms is highly unusual in that they follow neither hypothesis regarding hemispheric dominance for limb praxic control: 1) Motor engrams (limb praxic dominance) stored in the
Cerebral Organization in Left-Handers
359
parietal region of the language dominant hemisphere (Geschwind, 1965; Heilman & Rothi, 1985; Luria, 1980), nor 2) Limb praxia mediated by the hemisphere contralateral to dominant hand (Brown & Wilson, 1973; Heilman, Coyle, Gonyea, & Geschwind, 1973). In the present case the brain lesion is contralateral to the presumed language dominant hemisphere and ipsilateral to the dominant hand. Thus, the analysis of this case may help elucidate possible variations from more typical patterns of cerebral organization in left-handers.
CASE REPORT
W.W., a 51-year-old, left-handed, white male, suffered a left-middlecerebral artery CVA on May 20, 1983. This CVA was preceded by a myocardial infarction eight days earlier. Clinical examination revealed right hemiplegia. He also had extreme emotional lability and tearfulness (despite generally flattened affect) and dysarthric, but nonaphasic speech. These later symptoms are consistent with pseudobulbar palsy, but he showed only right-sided supranuclear facial weakness and CT scans showed no evidence of any right-sided damage. Visual fields appeared to be intact, but a marked right-sided neglect was evident. This neglect extended to his entire right side. He would refer to his right arm as an object independent of himself, stating, “He’s been getting lazy. He just seems to sit there and don’t want to do nothing.” The patient could become quite confabulatory. He had an elaborate story about how he had dredged up old gold coins from the bottom of the Mississippi River and had established a secret bank account from these monies. He also would assure others that he could walk with the use of a cane. Neither of these stories had any basis in reality. W.W. also had a great deal of difficulty giving an accurate history of his recent illness. This difficulty appeared to be secondary to a very confused sense of time in which weeks often seemed like months to him, while some events which occurred months earlier were experienced as having happened within the past week, CT scans taken six days and 6’/2 months post-onset both showed a massive low density area including the entire area subserved by the leftmiddle-cerebral artery (fronto-temporo-parietal area; see Fig. 1). The patient had no alcohol, drug, or psychiatric history. He had a 10th grade education, plus a GED obtained while in the Navy. He reported to have been the product of a normal pregnancy and delivery, and denied any previous head injuries. He was left-handed for all activities including writing, as well as left-eyed and footed. He was the only left-handed individual in at least four generations in his family (grandparents, parents, seven siblings, and three children). W.W.‘s wife confirmed this historical information.
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R. D. Vanderploeg
FIGURE 1. Sequential CT cuts six and a half months post-CVA. As with all X-rays, the leftright orientation, as presented, is reversed. Note the low density lesion involving the left frontotemporo-parietal area (right side of figure.) subserved by the left-middle-cerebral artery. A CTscan six and a half days post-CVA (not pictured) differed only in showing slightly more frontal and parietal involvement, mild edema, and a slight midline shift.
Neuropsychological Assessment A complete neuropsychological evaluation was conducted 2’12 months post-CVA. The following tests were administered: Halstead-Reitan Neuropsychological Battery (HRNB), Boston Diagnostic Aphasia Examination, Wechsler Adult Intelligence Scale (WAIS), Wechsler Memory Scale (WMS), Bender-Gestalt, Raven’s Coloured Progressive Matrices, and the Hooper Visual Organization Test. These results are summarized in Table 1 and Figs. 2and3.
Cerebral Organization in Left-Handers
TABLE Neuropsychological
WAIS Verbal IQ Performance IQ Full Scale IQ
106 76 93
Information Comprehension Arithmetic Similarities Digit Span Vocabulary
11 11 8 11 11 12
Digit Symbol Picture Completion Block Design Picture Arrangement Object Assembly
0 7 6 6 4
Wechsler Memory Scale Memory Quotient
101
Information Orientation Mental Control Memory Passages Digits Total Visual Reproduction Associate Learning
5 4 5 10 12 2 17.5
Total Raw Score
55.5
Hooper Visual Organization Test Raw Score 16.5 (errors 13.5) Degree of Impairment = Moderate Raven’s Coloured Progressive Raw Score 27 (errors 9) Lateral Left
Dominance Examination Eye Hand Foot X X X
Matrices
361
1 Assessment
Halstead-Reitan Battery Category test (prorated) Tactual Performance Test Left Hand (4 placed) Left Hand (all placed) Left Hand (all placed Total Time Memory Localization Seashore Rhythm Test Raw Score II Rank Score Speech-sounds Perception Test Finger Oscillation Test Dominant (Left) Nondominant (Right) Impairment Index Trail Making Test Part A (0 errors) Part B (I error-disc.
@E)
65 15.0 14.9 7.5’ 31.4 8 0 IO 15 55 0 0.7
132” 166”
Aphasia Screening Test - PossibIe mild dysnomia (naming triangle a diamond) * Possible mild dyslexia (errors in right visual field) * Symbol dysgnosia (mistaking minus sign for equal or division sign) . Construction dyspraxia * Mild articulation difficulty Sensory-Perceptual Examination * Right hemiplegia * Right face decreased sensitivity to touch - Suppressions of the entire right visual field - Suppressions of right ear . Left finger agnosia and fingertip number writing errors
At the time of testing, W.W. was alert, cooperative, and oriented to person, place, situation, and current events. He was several days off on the correct date. Immediate recall, short-term memory, and remote memory were intact, with the exception of short-term visuospatial memory, which was moderately impaired (see Visual Reproduction drawings from the WMS in Fig. 4B). He obtained a WAIS Full Scale IQ of 93 (Average range), with a Verbal IQ of 106 and a Performance IQ of 76. The 30 point disparity
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OF SPEECH CHARACTERISTICS
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FIGURE 2. Results on the Boston Diagnostic
AUDITORY COMPREHENSlON convuwd from objectin 1%xre mcan
WORD FINDING inlamationrl content in relation to fluency
PARAPHASIA IN RUNNING SPEECH
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363
Cerebral Organization in Left-Handers
PAH.P”.S,.
FIGURE
3. Results on individual
subtests of the Boston Diagnostic
Aphasia
Examination.
between Verbal and Performance IQ scores reflects W.W.‘s impaired visuospatial and perceptual-motor skills. On the HRNB he obtained an Impairment Index of 0.7 (5 of 7 indicators impaired) and showed moderate to severe impairment on the Category Test, Tactual Performance Test (Time and Localization scores), Seashore-Rhythm Test, and Speech-sounds Perception test. Language. On the Boston Diagnostic Aphasia Examination, W.W. obtained a severity rating of 5 (minimal discernible speech handicaps). The problems and errors he had were nonaphasic in nature. His speech was high-pitched, harsh, and rapid but variable in rate. Articulation deteriorated with an increase in rate. However, language was within normal limits on sound system, syntax, and vocabulary. He had no naming or word finding prob-
364
R. D. Vanderploeg
FIGURE 4. Patient’s drawings of various neuropsychological test stimuli. All figures are reduced from actual size. (A) The patient’s drawings of the Bender Gestalt figures. (B) The patient’s reproductions of the Wechsler Memory Scale Visual Reproduction subtest stimuli. (0 The patient’s drawing of the key from the Aphasia Screening Test.
lems, and showed no paraphasia. He did demonstrate verbal perseveration on reciting automatic sequences such as the days of the week, which he repeated until stopped by the examiner. Although auditory comprehension was intact, he had difficulty following commands due to a mild limb dyspraxia. Visuospatialfunctioning. As can be seen in Figs. 4A and 4C, W.W.‘s drawings evidence moderate construction dyspraxia even 2’/2 months post-CVA. When his Bender drawings were scored according to the Revised HuttBriskin scoring system (Lacks, 1984), he made five errors (Overlapping difficulty, Retrogression, Perseveration, Collision, and Angulation Difficulty). He also had a great deal of spatial difficulty with both the Block Design and Object Assembly subtests of the WAIS. His performance on the Block Design subtest was typical of that seen in many right-hemisphere impaired individuals, i.e., the loss of the basic two by two or three by three configuration (see Fig. 5; Kaplan, Palmer, Weinstein, Baker, & Weinstraub, 1981; Lezak, 1983, pp. 57-58). He also showed severe right-sided neglect on the Picture Arrangement and Object Assembly subtests. W.W.‘s pattern of im-
Cerebral Organization in Left-Handers
Model
6
q
Patient
365
Attempt
6
N=
FIGURE 5. Models and patient’s attempts of items number 6 and 8 of the WA&. Block Design subtest. Actual materials were in red and white, and the patient worked with three dimensional blocks. Figures are reduced from the test material actual size.
pairment on the Tactual Performance Test of the HRNB also indicates severe spatial difficulties. Although he was able to remember 8 out of the 10 block shapes, he was unable to correctly localize any of them spatially on his memory drawing of the board. Praxis. W.W.‘s basic motor functioning was intact on his left (average of 55 finger taps in 10 s), while his right arm remained plegic and his right leg paretic 2r/z months post-CVA. However, he demonstrated a mild limb dyspraxia. His left arm movements were clumsy and awkward while attempting to pantomime the use of a key (Aphasia Screening Test), despite his attempt to verbally talk himself through it. On a second attempt, without verbal self-mediation, he did adequately reproduce the basic required action. He also had difficulty performing the commands on the Boston Diagnostic Aphasia Examination. Despite verbally repeating the commands his movements were clumsy, he perseverated in the motor activities, and he had difficulty maintaining a posture once assumed. He also had difficulty following the sequence of multiple step commands. Unfortunately, a formal apraxia examination was not conducted and the testing which was completed was done 2l/2 months post-CVA. Nevertheless, the difficulties he demonstrated showed elements of both ideomotor apraxia (e.g., difficulty pantomiming the use of a key, and clumsy, awkward movements) and ideational apraxia (e.g., difficulty following the sequence of multiple step commands).
366
R. D. Vanderploeg
Temporal/sequential abilities. W.W. had extreme difficulty with temporal analysis and sequencing. His sense of time was very distorted with days, weeks, and months blending together. He had extreme difficulty sequencing his recent life events. He also had a great deal of difficulty in sequentially arranging the pictures on the Picture Arrangement subtest of the WAIS. He was unable to pace himself adequately along with the audio tape on the Rhythm and Speech-sounds Perception Tests. Finally, on diadochokinetic speech (i.e., rapid repetition of syllables), he had a severe breakdown in rate and rhythm, particularly on posterior lingual sounds. size asymmetries. Considering that W.W. showed reversed hemispheric organization of cognitive abilities, the CT scans were also examined for reversal of the more usual larger left-occipital-parietal region found in both left- and right-handers (Chui & Damasio, 1980; Koff, Naeser, Pieniadz, Foundas, & Levine, 1986; Lemay, 1977; Lemay & Kido, 1978). When measured according to the methods described by Koff et al. (1986), W.W.‘s right occipital-parietal area was somewhat wider and longer than his left. Thus, both cognitive and hemispheric size asymmetries were reversed from the pattern found in most right- and left-handers.
Hemispheric
DISCUSSION
In the present case of a nonfamilial left-handed individual with extensive left hemisphere damage, the pattern of neuropsychological deficits indicated moderately to severely impaired visuospatial functioning, constructional dyspraxia, limb dyspraxia, and temporal/sequential skill dysfunction. The patient also had severe right-sided sensory and body neglect, right-sided hemiparesis, and mildly dysarthric, but nonaphasic speech. Posterior hemispheric size asymmetries were also reversed, in that his right occipital-parietal area was somewhat larger than his left. This pattern of cognitive and anatomical size reversal most likely is not attributable to a compensatory basis, since the patient had no prior history of brain insults, and the CT scans (with and without constrast) revealed no impaired brain areas other than those resulting from the recent left-middlecerebral artery infarct. However, earlier brain insults lying within the recent massive area of infarct, would not be readily visible on the current CT scans. The possibility of such prior insults, though remote, if they had occurred early in W.W.‘s life might have resulted in a compensatory hemispheric reversal for language dominance, but not in his apparent reversal for visuospatial skill dominance. Language deficits are usually found following left-sided brain damage in both right- and left-handers, regardless of history of familial sinistrality (Hecaen et al., 1981; Hecaen and Sauguet, 1971). However, Delis, Knight,
Cerebral Organization in Left-Handers
367
and Simpson (1983) have reported a case of reversed language dominance in a nonfamilial left-hander who demonstrated a lasting Wernicke’s aphasia following a right-middle-cerebral artery infarct. They suggest that reversed cerebral organization in left-handers may occur only in nonfamilials, while familial sinistrality results in increased bilaterality of language abilities. The current case, with absence of language disturbances but impaired spatial abilities following extensive left hemisphere damage, complements Delis et al.? (1983) paper and is consistent with their hypothesis regarding reversed cerebral organization in nonfamilial left-handers. Cognitive analysis of temporal order or relationships, or of sequential patterns has been found to vary according to type of stimuli presented for analysis (e.g., left, linguistic versus right, nonlinguistic) or according to the type of recognition strategy employed (left, analytic versus right, pattern contour or gestalten approach; Hecaen and Albert, 1978, p. 275). Rightsided lesions of the parieto-temporo-occipital area have been reported to interfere with the comprehension of order and sequence, so that patients have difficulty seeing or dealing with temporal relationships (Lezak, 1979; Milberg, Cummings, Goodglass, & Kaplan, 1979). In the present case, W.W. had a severe breakdown in his appreciation of rate and rhythm, and had difficulty sequentially ordering test stimuli, as well as past historical events. Usually these difficulties are associated with posterior right hemisphere lesions. However, in W.W.‘s case they were a consequence of his severe left hemisphere infarction, indicating a hemispheric reversal for this cognitive ability as well. It is more difficult to account for W.W.‘s mild and atypical limb dyspraxia, considering that it is not consistent with either 1) damage to the language dominant hemisphere (Geschwind, 1965; Heilman & Rothi, 1985; Luria, 1980), or 2) damage to the hemisphere contralateral to dominant hand (Brown & Wilson, 1973; Heilman, Coyle, Gonyea, and Geschwind, 1973). W.W.‘s limb praxic difficulties were not entirely consistent with either ideomotor or ideational dyspraxia, but instead had some symptoms of both. This may be because he had partially recovered in the 2’/2 month time span since cerebral insult. It may also be that his limb praxic difficulties do not represent a true apraxia and would not have, even if assessed earlier. However, his difficulty pantomiming the use of a key, clumsiness in motor execution, difficulty in maintaining a posture once assumed, and difficulty correctly following the sequence of multiple step commands, are most consistent with a mild residual ideomotor dyspraxia. Thus, the presence of these symptoms in this left-hander following left-hemisphere damage, suggests that for him complex motor control (storage of complex motor engrams) is either a left-hemisphere or bilateral function. Left-handers generally have a low incidence of apraxia (Hecaen & Sauguet, 1971), and it has been suggested that left-handers may have a
368
R. D. Vanderploeg
better recovery rate for apraxia than right-handers (Heilman et al., 1973). This suggests the possibility that some left-handers may have bilateral representation for limb praxic control. The present case would be consistent with this hypothesis. The findings of case studies are, strictly speaking, limited to the case at hand. However, they are important in demonstrating exceptions to general population patterns or to widely held theoretical positions. W.W. appears to be an anomaly given the current understanding of cerebral organizational patterns. Even considering Satz’s (1979) model that 15% of left-handers have unilateral right-hemisphere representation for language, the reversal of visuospatial and temporal/sequential functions, in this case, is extremely atypical. However, the present case is consistent with Delis et al.? (1983) hypothesis that complete reversal of cognitive abilities and anatomical size asymmetries likely occurs only in nonfamilial left-handers. W.W.‘s limb dyspraxia, on the other hand, follows no reported pattern of cerebral organization. His dyspraxia suggests that control of complex motor skills in nonfamilial left-handers may remain a left-hemisphere or bilaterally represented function, even when other cognitive abilities are reversed. wish to thank Dr. Claire Matthews for her thorough language evaluatton using the Boston Diagnostic Aphasia Examination. I also wish to thank Drs. Herbert Goldman, Sandra Logan, and Gustave Sison, Jr. for their helpful comments and critiques of this manuscript. Finally, 1 would like to thank Muriel Snow for her typing and careful proofreading.
Acknowledgment-l
REFERENCES Brown, J. W., & Wilson, F. R. (1973). Crossed aphasia in a dextral. A case report. Neurology, 23,907-911. Chui, H. C., & Damasio, A. R. (1980). Human cerebral asymmetries evaluated by computed tomography. Journal of Neurology, Neurosurgery, and Psychiatry, 43.873-878. Delis, D. C., Knight, R. T., & Simpson, G. (1983). Reversed hemispheric organization in a lefthander. Neuropsychologia, 21, 13-24. Geschwind, N. (1965). Disconnexion syndromes in animals and man. Brain, 88, 237-294, 585-644. Geschwind, N., & Galaburda, A. M. (1985a). Cerebral lateralization: Biological mechanisms, associations, and pathology: I. A hypothesis and a program for research. Archives of Neurology, 42,428-459. Geschwind, N., & Galaburda, A. M. (1985b). Cerebral lateralization: Biological mechanisms, associations, and pathology: II. A hypothesis and a program for research. Archives of Neurology, 42, 521-552. Geschwind, N., & Galaburda, A. M. (1985~). Cerebral laterahzation: Biological mechanisms, associations, and pathology: III. A hypothesis and a program for research. Archives of Neurology, 42.634-654. Goodglass, H., & Quadfasel, F. A. (1954). Language laterality in left-handed aphasics. Brain, 77, 521-548.
Hecaen,
H., &Albert,
M. L. (1978). Human nemopsychology.
New York: John Wiley&Sons.
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Hecaen, H., de Agostini, M., & Monzon-Montes, A. (1981). Cerebral organization in lefthanders. Bruin und Language, 12, 261-284. Hecaen, H., & Sauguet, J. (1971). Cerebral dominance in left-handed subjects. Correx, 7, 19-48. Heilman, K. M., Coyle, J. M., Gonyea, E. F., & Geschwind, N. (1973). Apraxia and agraphia in a left-hander. Bruin, 96, 21-28. Heilman, K. M., & Rothi, L. J. G. (1985). Apraxia. In K. M. Heilman & E. Valenstein (Eds.). Clinical neuropsychology (2nd ed.). New York: Oxford University Press. Hooper, H. E. (1958). Manuul: Hooper visual organization fest. Beverly Hills, CA: Western Psychological Services. Humphrey, M. E., & Zangwill, 0. L. (1952). Dysphasia in left-handed patients with unilateral brain lesions. Journal of Neurology, Neurosurgery, und Psychiatry, 15, 184- 193. Kaplan, E., Palmer, P., Weinstein, C., Baker, E., & Weinstraub, S. (1981). Block design: A bruin behavior analysis. Paper presented at the International Neuropsycholdgical Society, Bergen, Norway. Kimura, D., & Harshman, R. (1984). Sex differences in brain organization for verbal and nonverbal functions. In G. J. de Vries, et al. (Eds.). Sex differences in bruin, rekutionship between structure und function. Progress in bruin reseurch series IVol. 611, Amsterdam: Elsevier. Koff, E., Naeser, M. A., Pieniadz, J. M., Foundas, A. L., & Levine, H. L. (1986). Computer tomographic scan hemispheric asymmetries in right- and left-handed male and female subjects. Archives of Neurology, 43, 487-491. Lacks, P. (1984). Bender Gestalt screening for brain dysfunction. New York: John Wiley & Sons. Lemay, M. (1977). Asymmetries of the skull and handedness. Journal of the Neurological
Sciences, 32,243-253. Lemay, M., & Kido, D. K. (1978). Asymmetries of the cerebral hemispheres on computer tomograms. Journal of Computer Assisted Tomography, 2.471-476. Lezak, M. D. (1979). Behavioral concomitants of configurul disorganization. Paper presented at the seventh annual meeting of the International Neuropsychological Society, New York City. Lezak, M. D. (1983). Neuropsychologicalassessment (2nd ed.). New York: Oxford University Press. Lishman, W. A., & McMeeken, E. R. L. (1977). Handedness in relation to direction and degree of cerebral dominance for language. Cortex, 13, 30-43. Luria, A. R. (1970). Traumatic aphasia (Translated from the Russian), The Hague, Mouton. Luria, A. R. (1980). Higher corticalfunctions in man (2nd ed.). New York: Basic Books. Milberg, W., Cummings, J., Goodglass, H., & Kaplan, E. (1979). Case report: A global sequential processing disorder following head injury: A possible role for the right hemisphere in serial order behavior. Journal of Clinical Neuropsychology, 1,213-225. Satz, P. (1979). A test of some models of hemispheric speech organization in the left- and righthanded. Science, 203, 1131-1133.
pp.357-369, 1986
Left-Handedness
~Xl77-6177/86S3.CKl
+ .OO
Copyright 0 1987 National Academy of Clinical Neuropsychologistr
and Variant Patterns
of Cerebral Organization:
A Case Study
Rodney D. Vanderploeg Research Service, St. Louis Veterans Administration
JMedlcal Center
A left-middle-cerebraI arrery infarct in a 51-year-old, nonfamilial left-handed man failed to produce aphasia, bur did resuh in imparied visuospatiul funclioning, construction dyspraxia, mild limb dyspraxiu, and iemporal/sequentiul skill dysfunction. The patienr also had severe right-sided sensory and body neglect, right-sided hemiparesis, and mildly dysarthric speech. These neurospsychological findings strongly suggest a reversed partern of cerebral organizarion. Posterior anaromical size asymmetrres were also reversed, in that rhe righr occipiralparietal area was somewhat larger than the left. However, ihis parienr’s limb dyspraxia followed no known pattern of cerebral organization. His dyspraxiu suggests rhar conlrol of complex motor skills in nonfamilial lefr-handers may remain a left-hemisphere or bilaterally represented function, even when orher cognitive abilities are reversed.
With certain notable and consistent exceptions, the pattern of cerebral organization in left-handers has been reported to follow a similar pattern to right-handers, i.e., primarily left-hemisphere representation for language abilities, and almost exclusively right-hemisphere dominance for visuospatial functions (Hecaen, de Agostini, & Monzon-Montes, 1981). However, the exceptions and variations from the typical right-handed pattern of organization have been documented by numerous investigators (Goodglass and Quadfasel, 1954; Hecaen, de Agostini, & Monzon-Montes, 1981; Hecaen and Sauguet, 1971; Humphrey and Zangwill, 1952; Luria, 1970; Satz, 1979). Patterns of language disturbance differ between left- and right-handers following similar unilateral cortical damage. Symptoms of left-handed aphasics generally do not follow the classical aphasia syndromes and are typically milder regardless of hemisphere injured. Recovery is also more rapid and complete in left-handed aphasics (Hecaen and Sauguet, 197 1;
Requests for reprints should be addressed to Rod Vanderploeg, Ph.D., who is now at Psychology Service (116B), James A. Haley Veterans Hospital, 13000 North 30th Street, Tampa, FL 33612 and is affiliated with the Department of Neurology, University of South Florida, College of Medicine.
358
R. D. Vanderploeg
Luria, 1970). Left-handers with right hemisphere impairment, often show some language disturbance in oral and written language, while right-handers with similar damage typically do not (Hecaen et al., 1981). Satz (1979) suggested a model of three types of cerebral organization for language in left-handers: left-hemisphere language dominance in 15%) right dominance in 15%, and bilateral representation in 70%. Other investigators have reported significantly higher percentages of unilateral left hemisphere language representation (7OVo), with less bilateral (IS20%), but similar percentages of right hemisphere language representation (5-15%). For reviews see Hecaen and Albert (1978) and Lishman and McMeeken (1977). A family history of left-handedness has been associated with an increased incidence of cerebral bilaterality of language representation, as well as decreased intrahemispheric language localization. On the other hand, spatial abilities in left-handers, as with right-handers, generally are right hemisphere functions, regardless of side of language dominance. The exception reported in the literature is in nonfamilial left-handers and women, where spatial abilities appear to have a higher degree of bilateral representation (Hecaen et al., 1981). Unfortunately, such group data obscure the actual pattern of cerebral specialization in individual cases. Recently, various researchers have reported that patterns of cerebral organization may vary considerably from individual to individual (Geschwind & Galaburda, 1985a, b, c; Hecaen, de Agostini, & Monzon-Montes, 1981; Heilman, Coyle, Gonyea, & Geschwind, 1973; Kimura & Harshman, 1984). At various stages of prenatal, neonatal, and later development, genetic pre-dispositions may interact with various developmental determinants (e.g., hormonal environments, cerebral insults, developmental skill practice, etc.) differentially influencing brain development and consequently affecting patterns of functional cerebral organization. In these individuals developmental cerebral specialization will have been altered at different periods and to different extents. Consequently, they will be a more variable population and need to be considered on a more individual basis (Geschwind & Galaburda, 1985a). The present study presents a nonfamilial left-hander who developed right hemiplegia without aphasia, impaired visuospatial functioning, and mild limb dyspraxia following an extensive left-hemisphere lesion secondary to a left-middle-cerebral artery infarct. This case suggests that not only may language be represented as a unilateral right-hemisphere function in lefthanders, but that spatial abilities may also be reversed from the typical righthemisphere dominance pattern. The mild limb dyspraxia was not entirely consistent with either ideomotor or ideational apraxia, but had elements of both. However, the presence of such dyspraxic symptoms is highly unusual in that they follow neither hypothesis regarding hemispheric dominance for limb praxic control: 1) Motor engrams (limb praxic dominance) stored in the
Cerebral Organization in Left-Handers
359
parietal region of the language dominant hemisphere (Geschwind, 1965; Heilman & Rothi, 1985; Luria, 1980), nor 2) Limb praxia mediated by the hemisphere contralateral to dominant hand (Brown & Wilson, 1973; Heilman, Coyle, Gonyea, & Geschwind, 1973). In the present case the brain lesion is contralateral to the presumed language dominant hemisphere and ipsilateral to the dominant hand. Thus, the analysis of this case may help elucidate possible variations from more typical patterns of cerebral organization in left-handers.
CASE REPORT
W.W., a 51-year-old, left-handed, white male, suffered a left-middlecerebral artery CVA on May 20, 1983. This CVA was preceded by a myocardial infarction eight days earlier. Clinical examination revealed right hemiplegia. He also had extreme emotional lability and tearfulness (despite generally flattened affect) and dysarthric, but nonaphasic speech. These later symptoms are consistent with pseudobulbar palsy, but he showed only right-sided supranuclear facial weakness and CT scans showed no evidence of any right-sided damage. Visual fields appeared to be intact, but a marked right-sided neglect was evident. This neglect extended to his entire right side. He would refer to his right arm as an object independent of himself, stating, “He’s been getting lazy. He just seems to sit there and don’t want to do nothing.” The patient could become quite confabulatory. He had an elaborate story about how he had dredged up old gold coins from the bottom of the Mississippi River and had established a secret bank account from these monies. He also would assure others that he could walk with the use of a cane. Neither of these stories had any basis in reality. W.W. also had a great deal of difficulty giving an accurate history of his recent illness. This difficulty appeared to be secondary to a very confused sense of time in which weeks often seemed like months to him, while some events which occurred months earlier were experienced as having happened within the past week, CT scans taken six days and 6’/2 months post-onset both showed a massive low density area including the entire area subserved by the leftmiddle-cerebral artery (fronto-temporo-parietal area; see Fig. 1). The patient had no alcohol, drug, or psychiatric history. He had a 10th grade education, plus a GED obtained while in the Navy. He reported to have been the product of a normal pregnancy and delivery, and denied any previous head injuries. He was left-handed for all activities including writing, as well as left-eyed and footed. He was the only left-handed individual in at least four generations in his family (grandparents, parents, seven siblings, and three children). W.W.‘s wife confirmed this historical information.
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FIGURE 1. Sequential CT cuts six and a half months post-CVA. As with all X-rays, the leftright orientation, as presented, is reversed. Note the low density lesion involving the left frontotemporo-parietal area (right side of figure.) subserved by the left-middle-cerebral artery. A CTscan six and a half days post-CVA (not pictured) differed only in showing slightly more frontal and parietal involvement, mild edema, and a slight midline shift.
Neuropsychological Assessment A complete neuropsychological evaluation was conducted 2’12 months post-CVA. The following tests were administered: Halstead-Reitan Neuropsychological Battery (HRNB), Boston Diagnostic Aphasia Examination, Wechsler Adult Intelligence Scale (WAIS), Wechsler Memory Scale (WMS), Bender-Gestalt, Raven’s Coloured Progressive Matrices, and the Hooper Visual Organization Test. These results are summarized in Table 1 and Figs. 2and3.
Cerebral Organization in Left-Handers
TABLE Neuropsychological
WAIS Verbal IQ Performance IQ Full Scale IQ
106 76 93
Information Comprehension Arithmetic Similarities Digit Span Vocabulary
11 11 8 11 11 12
Digit Symbol Picture Completion Block Design Picture Arrangement Object Assembly
0 7 6 6 4
Wechsler Memory Scale Memory Quotient
101
Information Orientation Mental Control Memory Passages Digits Total Visual Reproduction Associate Learning
5 4 5 10 12 2 17.5
Total Raw Score
55.5
Hooper Visual Organization Test Raw Score 16.5 (errors 13.5) Degree of Impairment = Moderate Raven’s Coloured Progressive Raw Score 27 (errors 9) Lateral Left
Dominance Examination Eye Hand Foot X X X
Matrices
361
1 Assessment
Halstead-Reitan Battery Category test (prorated) Tactual Performance Test Left Hand (4 placed) Left Hand (all placed) Left Hand (all placed Total Time Memory Localization Seashore Rhythm Test Raw Score II Rank Score Speech-sounds Perception Test Finger Oscillation Test Dominant (Left) Nondominant (Right) Impairment Index Trail Making Test Part A (0 errors) Part B (I error-disc.
@E)
65 15.0 14.9 7.5’ 31.4 8 0 IO 15 55 0 0.7
132” 166”
Aphasia Screening Test - PossibIe mild dysnomia (naming triangle a diamond) * Possible mild dyslexia (errors in right visual field) * Symbol dysgnosia (mistaking minus sign for equal or division sign) . Construction dyspraxia * Mild articulation difficulty Sensory-Perceptual Examination * Right hemiplegia * Right face decreased sensitivity to touch - Suppressions of the entire right visual field - Suppressions of right ear . Left finger agnosia and fingertip number writing errors
At the time of testing, W.W. was alert, cooperative, and oriented to person, place, situation, and current events. He was several days off on the correct date. Immediate recall, short-term memory, and remote memory were intact, with the exception of short-term visuospatial memory, which was moderately impaired (see Visual Reproduction drawings from the WMS in Fig. 4B). He obtained a WAIS Full Scale IQ of 93 (Average range), with a Verbal IQ of 106 and a Performance IQ of 76. The 30 point disparity
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FIGURE 2. Results on the Boston Diagnostic
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363
Cerebral Organization in Left-Handers
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between Verbal and Performance IQ scores reflects W.W.‘s impaired visuospatial and perceptual-motor skills. On the HRNB he obtained an Impairment Index of 0.7 (5 of 7 indicators impaired) and showed moderate to severe impairment on the Category Test, Tactual Performance Test (Time and Localization scores), Seashore-Rhythm Test, and Speech-sounds Perception test. Language. On the Boston Diagnostic Aphasia Examination, W.W. obtained a severity rating of 5 (minimal discernible speech handicaps). The problems and errors he had were nonaphasic in nature. His speech was high-pitched, harsh, and rapid but variable in rate. Articulation deteriorated with an increase in rate. However, language was within normal limits on sound system, syntax, and vocabulary. He had no naming or word finding prob-
364
R. D. Vanderploeg
FIGURE 4. Patient’s drawings of various neuropsychological test stimuli. All figures are reduced from actual size. (A) The patient’s drawings of the Bender Gestalt figures. (B) The patient’s reproductions of the Wechsler Memory Scale Visual Reproduction subtest stimuli. (0 The patient’s drawing of the key from the Aphasia Screening Test.
lems, and showed no paraphasia. He did demonstrate verbal perseveration on reciting automatic sequences such as the days of the week, which he repeated until stopped by the examiner. Although auditory comprehension was intact, he had difficulty following commands due to a mild limb dyspraxia. Visuospatialfunctioning. As can be seen in Figs. 4A and 4C, W.W.‘s drawings evidence moderate construction dyspraxia even 2’/2 months post-CVA. When his Bender drawings were scored according to the Revised HuttBriskin scoring system (Lacks, 1984), he made five errors (Overlapping difficulty, Retrogression, Perseveration, Collision, and Angulation Difficulty). He also had a great deal of spatial difficulty with both the Block Design and Object Assembly subtests of the WAIS. His performance on the Block Design subtest was typical of that seen in many right-hemisphere impaired individuals, i.e., the loss of the basic two by two or three by three configuration (see Fig. 5; Kaplan, Palmer, Weinstein, Baker, & Weinstraub, 1981; Lezak, 1983, pp. 57-58). He also showed severe right-sided neglect on the Picture Arrangement and Object Assembly subtests. W.W.‘s pattern of im-
Cerebral Organization in Left-Handers
Model
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365
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FIGURE 5. Models and patient’s attempts of items number 6 and 8 of the WA&. Block Design subtest. Actual materials were in red and white, and the patient worked with three dimensional blocks. Figures are reduced from the test material actual size.
pairment on the Tactual Performance Test of the HRNB also indicates severe spatial difficulties. Although he was able to remember 8 out of the 10 block shapes, he was unable to correctly localize any of them spatially on his memory drawing of the board. Praxis. W.W.‘s basic motor functioning was intact on his left (average of 55 finger taps in 10 s), while his right arm remained plegic and his right leg paretic 2r/z months post-CVA. However, he demonstrated a mild limb dyspraxia. His left arm movements were clumsy and awkward while attempting to pantomime the use of a key (Aphasia Screening Test), despite his attempt to verbally talk himself through it. On a second attempt, without verbal self-mediation, he did adequately reproduce the basic required action. He also had difficulty performing the commands on the Boston Diagnostic Aphasia Examination. Despite verbally repeating the commands his movements were clumsy, he perseverated in the motor activities, and he had difficulty maintaining a posture once assumed. He also had difficulty following the sequence of multiple step commands. Unfortunately, a formal apraxia examination was not conducted and the testing which was completed was done 2l/2 months post-CVA. Nevertheless, the difficulties he demonstrated showed elements of both ideomotor apraxia (e.g., difficulty pantomiming the use of a key, and clumsy, awkward movements) and ideational apraxia (e.g., difficulty following the sequence of multiple step commands).
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Temporal/sequential abilities. W.W. had extreme difficulty with temporal analysis and sequencing. His sense of time was very distorted with days, weeks, and months blending together. He had extreme difficulty sequencing his recent life events. He also had a great deal of difficulty in sequentially arranging the pictures on the Picture Arrangement subtest of the WAIS. He was unable to pace himself adequately along with the audio tape on the Rhythm and Speech-sounds Perception Tests. Finally, on diadochokinetic speech (i.e., rapid repetition of syllables), he had a severe breakdown in rate and rhythm, particularly on posterior lingual sounds. size asymmetries. Considering that W.W. showed reversed hemispheric organization of cognitive abilities, the CT scans were also examined for reversal of the more usual larger left-occipital-parietal region found in both left- and right-handers (Chui & Damasio, 1980; Koff, Naeser, Pieniadz, Foundas, & Levine, 1986; Lemay, 1977; Lemay & Kido, 1978). When measured according to the methods described by Koff et al. (1986), W.W.‘s right occipital-parietal area was somewhat wider and longer than his left. Thus, both cognitive and hemispheric size asymmetries were reversed from the pattern found in most right- and left-handers.
Hemispheric
DISCUSSION
In the present case of a nonfamilial left-handed individual with extensive left hemisphere damage, the pattern of neuropsychological deficits indicated moderately to severely impaired visuospatial functioning, constructional dyspraxia, limb dyspraxia, and temporal/sequential skill dysfunction. The patient also had severe right-sided sensory and body neglect, right-sided hemiparesis, and mildly dysarthric, but nonaphasic speech. Posterior hemispheric size asymmetries were also reversed, in that his right occipital-parietal area was somewhat larger than his left. This pattern of cognitive and anatomical size reversal most likely is not attributable to a compensatory basis, since the patient had no prior history of brain insults, and the CT scans (with and without constrast) revealed no impaired brain areas other than those resulting from the recent left-middlecerebral artery infarct. However, earlier brain insults lying within the recent massive area of infarct, would not be readily visible on the current CT scans. The possibility of such prior insults, though remote, if they had occurred early in W.W.‘s life might have resulted in a compensatory hemispheric reversal for language dominance, but not in his apparent reversal for visuospatial skill dominance. Language deficits are usually found following left-sided brain damage in both right- and left-handers, regardless of history of familial sinistrality (Hecaen et al., 1981; Hecaen and Sauguet, 1971). However, Delis, Knight,
Cerebral Organization in Left-Handers
367
and Simpson (1983) have reported a case of reversed language dominance in a nonfamilial left-hander who demonstrated a lasting Wernicke’s aphasia following a right-middle-cerebral artery infarct. They suggest that reversed cerebral organization in left-handers may occur only in nonfamilials, while familial sinistrality results in increased bilaterality of language abilities. The current case, with absence of language disturbances but impaired spatial abilities following extensive left hemisphere damage, complements Delis et al.? (1983) paper and is consistent with their hypothesis regarding reversed cerebral organization in nonfamilial left-handers. Cognitive analysis of temporal order or relationships, or of sequential patterns has been found to vary according to type of stimuli presented for analysis (e.g., left, linguistic versus right, nonlinguistic) or according to the type of recognition strategy employed (left, analytic versus right, pattern contour or gestalten approach; Hecaen and Albert, 1978, p. 275). Rightsided lesions of the parieto-temporo-occipital area have been reported to interfere with the comprehension of order and sequence, so that patients have difficulty seeing or dealing with temporal relationships (Lezak, 1979; Milberg, Cummings, Goodglass, & Kaplan, 1979). In the present case, W.W. had a severe breakdown in his appreciation of rate and rhythm, and had difficulty sequentially ordering test stimuli, as well as past historical events. Usually these difficulties are associated with posterior right hemisphere lesions. However, in W.W.‘s case they were a consequence of his severe left hemisphere infarction, indicating a hemispheric reversal for this cognitive ability as well. It is more difficult to account for W.W.‘s mild and atypical limb dyspraxia, considering that it is not consistent with either 1) damage to the language dominant hemisphere (Geschwind, 1965; Heilman & Rothi, 1985; Luria, 1980), or 2) damage to the hemisphere contralateral to dominant hand (Brown & Wilson, 1973; Heilman, Coyle, Gonyea, and Geschwind, 1973). W.W.‘s limb praxic difficulties were not entirely consistent with either ideomotor or ideational dyspraxia, but instead had some symptoms of both. This may be because he had partially recovered in the 2’/2 month time span since cerebral insult. It may also be that his limb praxic difficulties do not represent a true apraxia and would not have, even if assessed earlier. However, his difficulty pantomiming the use of a key, clumsiness in motor execution, difficulty in maintaining a posture once assumed, and difficulty correctly following the sequence of multiple step commands, are most consistent with a mild residual ideomotor dyspraxia. Thus, the presence of these symptoms in this left-hander following left-hemisphere damage, suggests that for him complex motor control (storage of complex motor engrams) is either a left-hemisphere or bilateral function. Left-handers generally have a low incidence of apraxia (Hecaen & Sauguet, 1971), and it has been suggested that left-handers may have a
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better recovery rate for apraxia than right-handers (Heilman et al., 1973). This suggests the possibility that some left-handers may have bilateral representation for limb praxic control. The present case would be consistent with this hypothesis. The findings of case studies are, strictly speaking, limited to the case at hand. However, they are important in demonstrating exceptions to general population patterns or to widely held theoretical positions. W.W. appears to be an anomaly given the current understanding of cerebral organizational patterns. Even considering Satz’s (1979) model that 15% of left-handers have unilateral right-hemisphere representation for language, the reversal of visuospatial and temporal/sequential functions, in this case, is extremely atypical. However, the present case is consistent with Delis et al.? (1983) hypothesis that complete reversal of cognitive abilities and anatomical size asymmetries likely occurs only in nonfamilial left-handers. W.W.‘s limb dyspraxia, on the other hand, follows no reported pattern of cerebral organization. His dyspraxia suggests that control of complex motor skills in nonfamilial left-handers may remain a left-hemisphere or bilaterally represented function, even when other cognitive abilities are reversed. wish to thank Dr. Claire Matthews for her thorough language evaluatton using the Boston Diagnostic Aphasia Examination. I also wish to thank Drs. Herbert Goldman, Sandra Logan, and Gustave Sison, Jr. for their helpful comments and critiques of this manuscript. Finally, 1 would like to thank Muriel Snow for her typing and careful proofreading.
Acknowledgment-l
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