A Longitudinal Examination of Crossed Aphasia Gustavo J. Rey, PhD; Bonnie E. Levin, PhD; Raul Rodas, MD; Brian C. Bowen, MD, PhD; Kester Nedd, DO Objective: To longitudinaly examine neuropsychological performance in an adult dextral man with crossed aphasia after cerebrovascular accident. Design: Case report using longitudinal neuropsycho- logical, neurological, and radiological examinations performed in close temporal proximity to one another. Setting: The patient was seen on both an inpatient and an outpatient basis by members of the Departments of Neurology and Radiology of the University of Miami (Fla) sic Broca's dysphasia, visual neglect, and visuospatial dis- turbances. The visuospatial disturbance resolved within 6 months whereas expressive language remained severely impaired. There was a dissociation between praxis and language. Mood was jovial with indifference toward his neurologic and cognitive limitations. Serial magnetic resonance imaging studies unequivocally localized the lesions to the right hemisphere, involving the right frontal, anterior parietal, and subcortical white matter. Patient: Thirty-four-year-old right-handed monolingual Hispanic man without family history of lefthandedness. Conclusions: The clinicoanatomic correlation is compatible with the view that crossed aphasia is a "mirror" representation of that seen in cases of uncrossed aphasia. The course of recovery suggests complete lateralization of language to the right hemisphere with bilateral or crossed representation of nonverbal skills. Results: Initial neuropsychological testing revealed clas- (Arch Neurol. 1994;51:95-100) School of Medicine. CROSSED APHASIA refers to disturbances of lan¬ guage following a right- hemisphere lesion in right-handed individu¬ als. Although it is estimated to occur in 1% to 2% of all dextral aphasies, welldocumented cases of crossed aphasia con¬ tinue to be rare.12 Published studies fre¬ quently lack longitudinal evaluation of the aphasie disturbance and/or associated neu¬ From the Departments of Neurology (Drs Rey, Levin, Nedd, and Rodas), Psychology (Dr Levin), Radiology (Dr Bowen), and Rehabilitation (Dr Nedd), University of Miami (Fla). ropsychological findings, and do not in¬ clude correlative neurodiagnostic proce¬ dures. These studies are frequently confounded by cases with familial his¬ tory of sinistrality or the inclusion of pa¬ tients with chronically debilitating neu¬ rologic diseases or neurologic conditions that result in diffuse brain abnormalities. This article presents detailed neuropsycho¬ logical testing and magnetic resonance im¬ aging data in a young adult dextral man with Downloaded From: http://archneur.jamanetwork.com/ by a University of Calgary User on 05/26/2015 crossed aphasia at 1 week and at 1, 6, and 18 months after suffering a stroke. REPORT OF A CASE The patient was a 34-year-old fully righthanded (Edinburgh handedness inven¬ tory, 10) ,3 monolingual (Spanish) white man with a ninth-grade education. His medical history was significant for a 28year history of diabetes requiring split dos¬ ing of mixed insulin preparation, a 2-year history of well-controlled hypertension, cigarette smoking, and a 4-year history of headaches (HAs). There was no history of perinatal complications or learning disabil¬ ity. Psychiatric history was significant for depression from 12 to 15 years of age, sec¬ ondary to difficulty accepting and adjust¬ ing to the diagnosis of diabetes. Family his¬ tory was noncontributory. There were no known left-handed relatives. Figure 1. Axial T2-weighted image on initial magnetic resonance study. CLINICAL PRESENTATION AND INITIAL FINDINGS History of the present illness dates to August 30,1989, when he was awakened from sleep by a severe right frontotempo¬ ral HA, associated with mild left upper extremity weakness and expressive language difficulty with preserved compre¬ hension. He was seen in the emergency department the same day and was found to be alert and oriented. General and physi¬ cal examinations revealed dystrophic skin changes of the lower extremities and familial proptosis. The initial neurologic ex¬ amination demonstrated left facial weakness, left upper ex¬ tremity hemiparesis, and expressive aphasia. Sensory exami¬ nation was normal, pupils were equal and reactive, and in¬ tact visual acuity, ocular motility, and color discrimination were documented. There was no evidence of visual neglect on bedside neurologic examination. A thorough cardiovas¬ cular evaluation failed to reveal any abnormalities. A grade 2 diabetic retinopathy was evident and, throughout the hospitalization, control of his diabetes was difficult and man¬ agedby the endocrinology service. An electroencephalogram showed abnormal slowing over the right parietal area with¬ out epileptiform activity. Neuroradiologic results are pre¬ sented in Figure I and Figure 2 Initial magnetic reso¬ nance imaging showed areas of prolonged , and T2-relaxation time in the right frontal and anterior parietal lobes involv¬ ing cortex and subcortical white matter, as well as the right caudate and anterior lenticular nucleus, associated with mass . - Figure 2. Postgadolinium ,-weighted coronal image 1 week after cerebrovascualr accident. effect. Postgadolinium images showed minimal peripheral enhancement in the involved areas. A repeated magnetic reso¬ nance imaging 5 days later again showed similar signal ab¬ normalities on long TR images but with decreased mass ef¬ fect. Postgadolinium images demonstrated prominent gyral enhancement. These findings were consistent with evolving infarcts in the right middle cerebral and anterior cerebral ar¬ terial distribution. No signal abnormalities were identified in the left hemisphere or posterior fossa. The neuropsychologic test results are summarized in Table I and Table 2. Initial neuropsychologic examination was performed 1 week after admission and the following results were obtained. LANGUAGE EXAMINATION Language was assessed with the Multilingual Aphasia Examination-Spanish (MAE-S) ,4 the Test de Vocabulario en Imágenes Peabody,5 and translated portions of the Boston Diagnostic Aphasia Examination.6 Oral expressive language skills were severely compromised, with no spontaneous in¬ telligible verbalizations. He was unable to perform simple orolingual manipulations, recite automatized series, or re¬ peat simple words. Written expressive skills were also se¬ verely compromised, as he was unable to write simple words to copy or to dictation (Figure 3, left ). He managed to write letters and numbers to dictation with approximately 50% accuracy. Simple written arithmetic calculations were mark¬ edly defective. Downloaded From: http://archneur.jamanetwork.com/ by a University of Calgary User on 05/26/2015 Table 1. Language-Related Test Results at 1 Week, and at 1, 6, and 18 Months After Cerebrovascular Accident* Table 2. Associated Cognitive Skills at 1 Week, and at 1, 6, and 18 Months After Cerebrovascular Accident* Time After Cerebrovascular Accident 1 wk 1 mo Time After Cerebrovascular Accident 6 mo 18 mo 1 wk Receptive Language Receptive vocabulary (TVIPSS) 106 Line Bisection Test Benton's R/L-personal 118 Auditory comprehension of complex (raw score) (raw score) (BDAE raw score) Aural comprehension (MAE-S percentile) 8/8 8/8 50 90 90 (MAE-S percentile) <1f 30 90 (MAE-S percentile) <1f 2t 2t Written comprehension Token test 1t Benton's Facial Recognition (BDAE raw score) 3/12f (MAE-S percentile) <1t Sentence repetition (raw score) Rey-Osterreith Figure (percentile) WAIS-R Block Design (SS) <1t (MAE-S percentile) Writing words to dictation (raw score) <1t Writing letters to dictation (raw score) Writing sentences to copy (raw score) 0/9f <1t 2/9t 2/31 51 20 7 Delayed 10/25 8.25 9/25 4/25 (WMS) (total score) 7.5 5.5 5 Memory Immediate 2/81 (raw score) Immediate Delayed Wepman's Visual Memory (raw score) 3/3 Buccofacial (raw score) Limb gesture (raw score) Ideomotor (raw score) TVIP indicates Test de Vocabulario en Imágenes Peabody; BDAE, Boston Diagnostic Aphasia Examination; and MAE-S, Multilingual Aphasia * Right-left orientation7 to self was normal but impaired in extrapersonal space. Mild left visual field neglect was evi¬ dent on a line bisection test and a simplified letter cancel¬ lation task. He was unable to spontaneously draw a clock. The copy condition of the Rey-Osterreith Complex Figure8 and clock drawing to copy revealed distinct left visual field inattention (Figure 4, lop). Reproduction of the Rey fig¬ ure was impaired and segmented, with omissions and dis¬ tortions of left-sided details. Angular judgments9 and dis¬ crimination of simple geometric designs10 were impaired. 43 7 2/91 ASSOCIATED COGNITIVE SKILLS 391 9f Visual reproduction racy, respectively. Receptive vocabulary on the Test de Vocabulario en Imágenes Peabody was average. The MAE-S Aural Comprehension ofWords Phrases was also well within normal limits, but aural comprehension on the MAE-S To¬ ken Test was severely impaired. Written comprehension of simple words and phrases in the MAE-S was defective. 41 &.SrS& /4y>*->e»<» ¿aja ift'a 7~/sfro /J /t -Aa / ''' Figure 3. Left, Word writing to dictation on initial neuropsychologic examination. Dictated words are as follows: mío, tira, casa, perro, primo, llave, yate, entregar, manchado. Right, Word writing to dictation on 6-month follow-up neuropsychologic examination. Dictated words are as follows: casa, mía, tira, perro, llave, entregar, manchado, and yate. C3 Figure 4. Top, Reproduction of the Rey-Osterreith Complex Figure and spontaneous clock drawing on initial neuropsychologic examination. Bot¬ tom, Reproduction of the Rey-Osterreith Complex Figure and spontaneous clock drawing on 6-month follow-up neuropsychologic examination. sive residual expressive impairments in visual naming, sen¬ repetition, and word fluency. Spontaneous writing and writing words to dictation also remained defective (Figure tence 3, right). He was able, however, to write numbers and letters to dictation and copy sentences with 100% accuracy. Writ¬ to within ofwords and ten comprehension phrases improved normal limits, but he continued to exhibit marked difficulty in the Token Test. His ability to perform simple arithmetic calculations improved, but was still below expectation. Within the visuospatial domain, right-left orientation, Block Design, line bisection, spontaneous clock drawing, facial recognition, and judgment of line orientation were scored within the low average to average range. Copy of the Rey figure improved to the borderline range (Figure 4, bottom). He continued to use a segmented ap¬ proach in the reproduction of this figure, and subtle omis- Downloaded From: http://archneur.jamanetwork.com/ by a University of Calgary User on 05/26/2015 sion of left-sided details and perseverative errors were still evident. However, the line bisection test did not reveal left visual field inattention. Visual psychomotor scanning on Trails A was slow but accurate. Shifting of letter-number remained severely impaired. Immediate and delayed memory for logical discourse information on the Wechsler Memory Scale-Revised subtest14 were low average, but paired associate learning was moderately impaired. On this latter task, he managed to recall correctly all semantically relatedword associations, but none of the unrelated word pairs. Immediate and de¬ layedvisuographic memory on the Wechsler Memory ScaleRevised were lo w average. Visual recognition memory was within normal limits. Incidental recall of the Rey figure decayed to the mildly impaired range. All buccofacial, limb gestures, and ideomotor praxis items were performed with 100% accuracy. Affect remained jovial, with indifference toward his neurologic limitations and communication problems. Neurologic progress was complicatedby the develop¬ ment of partial motor seizures involving the left side of his face and left hand, with secondary generalization on June 12,1990. He was effectively treated with carbamazepine and maintained at therapeutic levels. A follow-up electroencepha¬ logram on July 24,1990, demonstrated persistent slowing over the right hemisphere with no epileptiform activity. An 18-monthfollow-upneurologic examina tionshowed persistent left facial and upper extremity weakness, associ¬ ated with increased tone. Other aspects of his neurologic ex¬ amination remained unchanged, but continued functional improvement in ambulation capacity was documented. Se¬ rum carbamazepine levels were normal, without clinical or laboratory evidence of toxicity. Neuropsychologic testing revealed a stable pattern of language performance. Sponta¬ neous speech was minimal, with short, effortful utterances containing phonemic substitutions. Oral agility in the per¬ formance of simple orolingual manipulations remained im¬ paired. A subtle improvement was evident in the recitation ofautomatized sequences, as he recited the days of the week correctly and made one error reciting the months. Mental tracking also improved. He recited the days backward and made two errors counting from 20 backward to 1. On the MAE-S subtests, persistent deficits were evident in word re¬ trieval, sentence repetition, controlled word association, and aural comprehension on the Token Test. Word writing to dictation was also defective, but he managed to write letters and numbers to dictation without difficulty, and copy sen¬ tences with 100% accuracy. Simple arithmetic calculations continued to be performed with 50% accuracy. All praxis tion, new verbal learning, and incidental memory for the Rey figure. Visuographic memory on the Wechsler Memory ScaleRevised and visual recognition memory remained within the low average range. Affect remained unconcerned andjovial. sets on Trails items were performed without errors. Visuospatial skills also remained relatively stable, with the exception of a decline in the judgment of angles. No sig¬ nificant changes were evident in right-left orientation, con¬ structional praxis, visual discrimination, line bisection, and facial recognition. Memory testing revealed decreased per¬ formance in the delayed recall of logical discourse informa- COMMENT Our case study is unique in that it used neuropsychologic and magnetic resonance imaging data to examine longi¬ tudinally the course ofcrossed aphasia in a young dextral monolingual man without a familial history of left hand¬ edness. In this patient, primary compromise of the right frontal, anterior-parietal, and underlying brain regions re¬ sulted in a classic Broca's type dysphasia. This clinicoanatomic correlation is compatible with the view that the lan¬ guage disturbance in crossed aphasia is a "mirror" repre¬ sentation of that seen in cases ofuncrossed aphasia.15 This clinical presentation has been found to occur more fre¬ quently than other forms of anomalous language profiles in patients with crossed aphasia.2 Visuoperceptual disturbances and left hemifield inat¬ tention have been reported in case studies of crossed aphasia,15J0 but most studies do not address the nature and evolution of these impairments over time. In our case, ini¬ tial evaluation 1 week after cerebrovascular accident revealed left visual field inattention and pervasive visuospatial/ constructive deficits that resolved gradually over time. Seg¬ mentation, perseverative errors, and overall preservation of spatial relationships in the reproduction of a complex line drawing suggest thatsubtle residualconstructional dyspraxia was partly related to an "executive" disturbance. While it is possible that both language and visuospatial functions are lateralized exclusively to the right hemisphere, this is considered to be a remote possibility since there are no ra¬ diologie or electrophysiologic data to indicate dysfunction of the left hemisphere. Conversely, the remarkable recov¬ ery of nonverbal cognitive functions in the context of a large right-hemispheric lesion raises the possibility of bilateral representation or crossed hemispheric dominance for visu¬ ospatial skills. This pattern of reversed lateralization of non¬ verbal cognitive skills has been recently reported in patients with lesions to the left hemisphere.21 When praxis performance is studied in patients with crossed aphasia, buccofacial skilled movements are typi¬ cally impaired, with relative preservation of limb praxis.2,22·23 Our findings of severe impairment in simple orolingual agility and language skills, with preserved buc¬ cofacial and ideomotor praxis indicates a dissociation be¬ tween praxis and language24 and supports the view that ideomotor praxis may be independent of hemispheric lan¬ guage dominance.2 Memory functioning in crossed aphasia hasbeen sparsely investigated and findings have been inconsistent. In our pa¬ tient, performance on nonverbal memory tasks followed a course similar to that described above for visuospatial skills, with recovery to relatively normal levels of performance by Downloaded From: http://archneur.jamanetwork.com/ by a University of Calgary User on 05/26/2015 the 6-month follow-up. It was not possible to formally as¬ during the acute and subacute stages of recovery due to the severity of his language disturbance. At 6 months after cerebrovascular accident, the patient dem¬ onstrated relatively preserved memory for logical discourse information. On paired associate learning, our patient ex¬ hibited selective difficulty learning semantically unrelated word pairs, a pattern of performance that may also repre¬ sent "executive" dysfunction rather than a true memory dis¬ order.25'26 The observation that verbal memory was dispro¬ portionately compromised relative to visual memory raises the possibility of crossed lateralization of memory skills. Al¬ though controversy exists as to the neurologic substrates involved in the expression and comprehension of emotional responses, hemispheric differences in the regulation of emo¬ tional behaviors are well established. Patients with left an¬ terior cerebral involvement and nonfluent dysphasia fre¬ quently experience a "catastrophic" reaction characterized by profound depression.27·28 Conversely, patients with left posterior cerebral lesions and those with right-hemispheric compromise typically show indifference, apathy, and dimin¬ ished insight into their cognitive alterations.28 Our patient's affective presentation was not typical of that seen in cases of Broca's dysphasia following left anterior cerebral involve¬ ment in that he consistently displayed an inappropriatejo¬ vial mood and indifference toward his neurologic and cog¬ nitive limitations. At no time were depressive symptoms clini¬ cally evident or reportedby the patient. Of particular interest is the observation that his unsuccessful attempts to com¬ municate, typically a source of great frustration in patients with Broca's aphasia, were accompanied by spontaneous laughter and jesting. These findings suggest that depression in patients with Broca's dysphasia may be independent of the language disturbance and reflects compromise of un¬ derlying brain systems responsible for the regulation of mood. Regarding affective components of communicative behav¬ ior, our patient's facial expression was normal and he man¬ aged to identify emotional facial expressions to confron¬ tation without difficulty. The mechanisms involved in atypical cerebral local¬ ization are yet to be determined. The presence of perina¬ tal or early developmental trauma has been related to the crossed lateralization of language and other cognitive func¬ tions.29 Similarly, disorders of neuronal migration during early stages of fetal development can result in a wide range of neurologic disturbances, which may be associated with anomalous patterns of cognitive hemispheric dominance.30 However, in cases of crossed aphasia where there is no his¬ tory of neuropathologic insult or aberrant prenatal devel¬ opment, the cause of crossed hemispheric dominance re¬ mains poorly understood. Longitudinal case studies of simi¬ lar patients with crossed lateralization of cognitive functions may provide important insight regarding the clinical mani¬ festations of these rare disorders. sess verbal memory Accepted for publication December 8, 1992. We thank Arthur Benton, PhD, andRachel Tomer, PhD, for reviewing the manuscript and Esther Feldman, PhD, for assisting in the administration ofneuropsychological measures. Reprint requests to the Division of Neuropsychology, Department of Neurology, Universityof Miami School of Medicine, 1150 NW 14th St, Suite 715, Miami, FL33136 (Dr Rey). REFERENCES 1. Zangwill OL. Two cases of crossed aphasia. Neuropsychologia. 1979;17:167-172. 2. Alexander MP, Fischette MR, Fisher RS. Crossed aphasia can be mirror image or anomalous: case reports, review and hypothesis. Brain. 1989:112:953-973. 3. Oldfield RC. The assessment and analysis of handedness: the Edinburgh in- ventory. Neuropsychologia. 1971;9:97-113. 4. Rey GJ, Benton AL. Multilingual Aphasia Examination-Spanish: Administration Manual. Iowa City, Iowa: AJA Associates Inc; 1991. 5. Dunn LM, Padilla ER, Lugo DE, Dunn LM. Test de Vocabulario en Im\l=a'\genes Peabody. Diablo, Calif: Dunn Educational Services Inc; 1986. 6. 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Neuropsychology of Human Emotion. New York, NY: The Guilford Press; 1983. 29. Strauss E, Wada J. Lateral preferences and cerebral speech dominance. Cortex. 1983;19:165-177. 30. Brown MC, Levin BE, Ramsay RE, Landy HJ. Comprehensive evaluation of left hemisphere type I schizencephaly. Arch Neurol. In press. Downloaded From: http://archneur.jamanetwork.com/ by a University of Calgary User on 05/26/2015