Transcortical motor aprosodia: Functional and anatomical correlates

Grand Rounds

Transcortical Motor Aprosodia: Functional and Anatomical

Correlates

Anthony Y. Stringer and Cfaire Hodnett Emory University

Tr~&ordcai motor aprosodia~~A~, one of eight hypot~s~ed disorders of @ecrive co~~.~a~on, is charucterised by impaired production ofajfbive prosody and facial gestures, withintact imitationand comprehensionof afj?ect.It has been proposed that cortical TMA arisesfrom lesions in the superior or anterior lateral surface of the right frontal lobe, but for variousreasons it has not been possible to fully test this proposal. There have been few cases of TMA reported, and lesions have been too &ruse to permh accurate localization.A case ispresentedthatmeets both theFermi and anato~‘~~ criteria~ro~sedfor cortical TMA, thusproviding support for this system of chzssifyingdisorders of afective communication. Results suggest that the prosodic and gesturai deficits in TMA may be dissociated, and thatthe gestural componentextends to nonaf$ectivefacialmovements.

Neuroanatomicai studies of lesions that produce aphasia in right-handers have established the left hemisphere’s role in mediating the semantic and grammaticaI components of language (Damasio & Geschwind, 1984). Monrad-Krohn (1947) identified a third component of Ianguage, which he termed “prosody,” having to do with changes in the rhythm, pitch, and stress with which words are spoken. Variations in prosody and in facial expression are used to modify the meaning of speech and to express subtle shades of emotion. Patients with right-hemisphere damage often have a reduced ability to communicate emotions via prosody and facial gestures (Ross & Mesulam, 1979; Tucker, Watson, & Heilman, 1977; Weintraub, Mesulam, 8z Kramer, 1981). In addition, impairment in the ability to recognize emotions in others may be present. Ross (1981) introduced the term “aprosodia” to describe this syndrome of impaired emotional compilation following ant-hemisphere damage. Address reprint requests to Anthony Y. Stringer, Ph.D., Department of Rehabilitation Medicine, Emory University, 1441 Clifton Road, N.E., Atlanta, GA 30322. The authors thank Patricia M. Higgins and Bonnie Schaude for conducting ratings. 89

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Drawing an analogy to the clinical subtyping of aphasia, Ross (1981) described eight theoretical subtypes of aprosodia: motor; sensory; global; conduction; anemic; transcortical motor; sensory; and mixed aprosodia. Righthemisphere lesions producing each of the aprosodia subtypes were theorized to parallel the left-hemisphere lesions that produce the analogous subtypes of aphasia. One objection to this subtyping is that it is based on an aphasia classification that is not universally accepted. However, there is considerable agreement on the clinical and anatomical features of the aphasias despite differences in the labels used across classification systems (Benson, 1985). -While agreement on aphasia classification is far from complete, there is arguably sufficient commonality to form a basis for speculation on how deficits in emotional communication may be subtyped. Of the more than 30 cases of aprosodia that have appeared in the literature, most have had lesions in the predicted areas (Gorelick & Ross, 1987; Ross, 1981, 1988; Ross, Anderson, & Morgan-Fisher, 1989; Ross, Harney, delacoste-Utamsing, & Purdy, 1981; Ross & Mesulam, 1979; Weintraub, Mesulam, & Kramer, 1981; Wolfe & Ross, 1987). However, less is known about the localization of the lesion producing transcortical motor aprosodia (TMA). Transcortical motor aphasia arises from medial frontal lobe lesions (Alexander & Schmitt, 1980), or lesions superior or anterior to Broca’s area (Freedman, Alexander, & Naeser, 1984; Rubens, 1975) in the language-dominant left hemisphere. Transient cases of transcortical motor aphasia have also been reported following left striatal lesions (Alexander & LoVerme, 1980). If the analogy to transcortical motor aphasia is valid, TMA should consist of impaired production of affective prosody and facial gestures with intact imitation and comprehension of affect, arising from lesions in the medial, superior, or anterior right frontal lobe, with a transient syndrome produced by a striatal lesion. Only limited data is available for evaluating the analogy between TMA and transcortical motor aphasia. Of the two cases of TMA reported by Ross (1981), one had a lesion confined to the right striatum (resulting in a transient syndrome). The other case had a metastatic adenocarcinoma involving the right frontal, parietal, and temporal lobes. A third case was described who had a mixed transcortical aprosodia when examined six months after her stroke, which evolved over several months to TMA. Her CT scan showed a large area of infarction involving the right frontal, parietal, and superior temporal lobes, with an additional small area of infarction in the left anteromedial frontal lobe. We have been unable to find subsequent reports of TMA in the literature. Thus, a precise functional-anatomical relationship has not been determined for TMA (Ross, 1985). We recently examined a patient who met the criteria for TMA specified by Ross (1981). The disorder arose following surgical removal of an anaplastic astrocytoma in the right frontal lobe. Because our patient presented with a

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lesion more focal in nature than Ross’s original cases of cortical TMA, we have an opportunity for further localizing TMA and for testing Ross’s system of classification. CASE REPORT J. G. was a 30-year-old, right-handed, white, male attorney, who was admitted to the Emory University Center for Rehabilitation Medicine in 1986 with a left hemiparesis. A right frontal anaplastic astrocytoma had been diagnosed in 1981 following the onset of grand mal seizures. The seizures were initially treated with medication (primidone and carbamazepine), but became increasingly uncontrolled, necessitating surgery. A magnetic resonance imaging (MRI) scan was obtained prior to surgery. The sagittal view reveals a massive tumor in the posterior and superior right frontal lobe (Figure 1). There were no abnormalities seen in the left hemisphere or posterior fossa. Resection of the tumor was performed in March 1986 and the patient had an excellent postoperative recovery. The bulk of the tumor was removed in two sections, respectively measuring 3 x 2.5 x 1 cm and 3 x 1.5 x 0.4 cm. Additionally, tissue was removed from the margins of the tumor in three aggregates, ranging from 3.5 x 2.5 x 1 cm to 1 x 0.5 x 0.2 cm. An MRI scan obtained after surgery, shows the extent of the surgical resection, and compression of the right lateral ventricle by a small mass effect (Figure 2). Upon admission to the Rehabilitation Center, J. G. had a left hemiparesis (worse in the upper extremity), mild lower left facial weakness, and a normal sensory examination. When commanded, he performed simple facial movements well (e.g., pursing the lips, opening and closing the mouth, protruding and retracting the tongue, biting, blowing, and sniffing), but he was clumsy and would grope for the correct movement when asked to produce or imitate more complex facial movements (e.g., simultaneously knitting the brow, wrinkling the nose and showing the teeth). Despite having weakness only in the

FIGURE 1. Presurgical magnetic resonance imaging scan (sagittal plane) showing an anaplastic astrocytoma in the posterior-superior right frontal lobe.

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lower face, he showed difficulty performing movements involving the upper face as well. The patient’s speech was quite monotonic, and he showed little variability in facial expression, even when discussing his illness. The patient’s friends also detected the change in him, and he reported receiving comments about the flatness of his voice when he spoke over the telephone. Despite the change in vocal quality, his speech articulation and phonation were completely intact. In a videotape of a birthday party one month prior to surgery, the patient showed a normal range of affective expression, in contrast to his current presentation. The results of neuropsychological testing are presented in Table 1. As can be seen, there was a 35point discrepancy in the patient’s Wechsler Verbal and Performance IQs consistent with the presence of right-hemisphere pathology. While the patient performed between one and two standard deviations below average on the timed, perceptual-motor tests of the Wechsler Performance Scale, he was able to produce spatially accurate drawings of geometric figures (circle, square, triangle and cube), complex designs (Rey Figure), and objects (clock and bicycle). J. G. was also normal in his ability to make the fine visual discriminations required by the Benton Facial Recognition Test. J. G. showed a consistent mild to moderate deficit in his ability to learn and retain verbal information as measured by the California Verbal Learning Test and the Logical Memory section of the Wechsler Memory Scale (WMS). In contrast, he was intact in his ability to remember the WMS Visual Reproduction Figures and the Rey Complex Figure. This was an unexpected pattern given the patient’s right-sided brain lesion. J. G.‘s performance was intact on the majority of tests measuring various aspects of frontal lobe functioning, including Finger Tapping in the right hand (the left hand was too impaired for testing), Luria’s Motor Programmes, and the Wisconsin Card Sorting Test. The patient was mildly impaired in the speed with which he completed the Grooved Pegboard (right hand only), and was low normal in his word fluency (Controlled Oral Word Association Test). This generally intact performance on tests of frontal lobe functioning is not surprising given that most of the tests administered are capable of being verbally mediated and are likely to be most sensitive to left-sided frontal lesions. The Minnesota Multiphasic Personality Inventory (MMPI) (Dahlstrom, Welsh, & Dahlstrom, 1975) was also administered to J. G. He showed a clinically significant T-score elevation only on scale 3, with many of the items he endorsed reflecting realistic somatic complaints (muscle twitching, poor balance, not in good physical health) rather than a characterological adjustment. All other MMPI scales were within normal limits suggesting the patient was free of significant emotional distress and depression. Formal examination of J. G.‘s affective communication was conducted at seven months postsurgery. For comparison, ten healthy, white, male volun-

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TABLE 1 Neuropsychological Evaluation of J. G.

Test Wechsler Adult Intelligence Scale-Revised (Wechsler. 1981) Information Digit Span Vocabulary Arithmetic Comprehension Similarities Picture Completion Picture Armneement Block DesignObject Assembly Digit Symbol Verbal IQ Performance IQ Full Scale IO Wechslex Memo+ Scale (Wechsler. 1945) Logical Memory - Immediate Recall - 30 min. Delayed Recall Visual Reproduction - Immediate Recall - 30 min. Delayed Recall California Verbal Learning Test (Del;iir,, Ober,& Kaplan, 1986) Trial 5 Total Intrusions Total Perseverations Total Semantic Cluster Score Alternate List Short Delay - Free Recall - Cued Recall Long Delay - Free Recall - Cued Recall - Recognition - False Positives Rey-Osterreith Complex Figure (L”zc&&$Jp. 444-447) Immediate Recall Delayed Recall Benton Facial Recognition Test (Benton, Hamsher, Vamey, & Spree& 1983) Lime Drawings Finger Tapping (Reitan &Davison_ 1974) - Right Hand - Left Hand Grooved Pegboard (Matthews & Klove, 1964) - Right Hand - Left Hand Lwia’s (1980)Motor Proar-es Ma;ldN’s Triple Loops Controlled Oral Word Association Test (FAS) (Benton & Hamsher, 1978) Total Words Wisconsin Card Sorting Test (Grant & Berg. 1948) Total Sorts

Results

11 14 12 ::. 15 5 :: 5 113 ;z 13 6 12 12 7 li 0 9 13 6 8 10

/

1;

1 centile 3: 35 45 normal 52 -

75 s. normal normal 25

6

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Transcortical Motor Aprosodia

J.G.M

Normal controls EB

100 90 80 70 60 50 40 30 20 10 05

Prosody

Gesture

Comprehension FIGURE 3. Affective communication profiles (scores are averaged across the two examiners).

teers (average age: 33.1 years, range: 21-40; average education: 18.6 years, range: 1%21), having no history of neurologic or psychiatric disease, were also examined. The examination was conducted by the second author. To assess imitation and production of affective prosody, a neutral content sentence (e.g., “It rained yesterday.“) was read to subjects in either an angry, tearful, happy, or surprised tone of voice, which they were asked to imitate. Following this, subjects were instructed to say the sentence in each of the remaining three tones of voice. This procedure was repeated for eight neutral content sentences. All responses were videotaped. Two raters (the authors) independently assigned scores of 1 or 0 for tone of voice and word stress for each response. Ratings for tone of voice and word stress were summed to obtain composite affective prosody imitation and production scores. Imitation of affective facial expressions was assessed by having the subjects imitate happy, sad, angry, surprised, and disgusted expressions (twice each). Subjects subsequently were asked to produce each expression twice without benefit of a model to imitate. Each response wa.s again videotaped and later independently scored 1 or 0 by the two raters. Since the patient had mild lower facial weakness, careful attention was paid to the upper part of his face when assigning him scores. Finally, comprehension of affective communication was assessed by having the subjects attempt to identify the emotion in the examiner’s tone of voice (angry, tearful, happy, or surprised) or facial expression (happy, sad, angry,

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surprised, or disgusted). The stimuli were identical to those used to assess imitation and production. Responses were again videotaped and subsequently scored. The results of the examination of the patient and normal controls are summarized in Figure 3. Interrater reliability was .71 and .99, respectively, for ratings of imitation and production of affective prosody. For ratings of imitation and production of emotional facial gestures, interrater reliability was .70 and .83, respectively. Thus, interrater reliability was generally high. As the examination of affective comprehension did not involve assignment of ratings, reliability coefficients were not computed, and as expected, there was no disagreement between the examiners. The results in Figure 3 are averaged across the two examiners. While statistical analysis is not possible with a single case, some tentative conclusions can be drawn from a comparison of J. G. with the normal controls. Figure 1 indicates that J. G. had good comprehension of both prosody and affective gestures, performing at a level comparable to the normal controls. While J. G. had mild difficulty with imitation of affective prosody relative to the controls, his production of affective prosody to command was much more severely impaired. In contrast, J. G. performed far below the normal controls both in his imitation and production of affective facial gestures. While the patient was slightly better when imitating facial gestures, the difference between his imitation and production of gestures was quite small. As a check on the possibility that the authors’ ratings were biased by their knowledge of TMA and of J. G.‘s history, two additional raters were recruited and asked to independently rate J. G.‘s imitation and production of affect from the same videotaped examinations used by the experimenters. The second set of raters were speech pathologists who were unfamiliar with Ross’s classification of aprosodia and who were not told the details of J. G.‘s history. The second set of raters duplicated the authors’ pattern when rating J. G.‘s imitation (82% of J. G.‘s responses were rated as correct) and production (51% of J. G.‘s responses were rated as correct) of prosody. The speech pathologists also found J. G.‘s affective gestures to be grossly impaired, but rated his imitation (25% of J. G.‘s responses were rated as correct) worse than his production (45% of J. G.‘s responses were rated as correct).

DISCUSSION

While we readily acknowledge the limitations of studying only single cases, we think the results of our examination provide an interesting basis for conjecture. Compared to normal controls, our patient had significant clinical impairment in the production of affective prosody, while imitation and comprehension of a model’s affective prosody were relatively intact. This pattern

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of results was duplicated by two additional raters who were unfamiliar with the patient’s history and with Ross’s categorization of aprosodia. While it would have been desirable for both sets of raters to be blind during assessment of the patient, this was not possible in the case of the first two raters (the authors) who were aware of the patient’s background at the time of his initial referral for clinical assessment. Thus, the second two raters, who were blind, provide an important control for the authors’ possible rating biases. The deficit in production of affective prosody arose in our patient following surgical removal of an astrocytoma in the superior lateral surface of the patient’s right frontal lobe. These characteristics match the functional and anatomical criteria proposed by Ross (1981) to define cortical TMA. The only previously reported cases of cortical TMA met Ross’s functional criteria, but had damage too diffuse to permit localization of the syndrome. Thus, our case provides new evidence supporting Ross’s classification of disorders of affective communication. Unlike Ross’ initial clinical-perceptual studies, which relied upon the subjective impressions of examiners to diagnose and describe aprosodia (Gorelick & Ross, 1987; Ross, 1981; Ross & Mesulam, 1979; Ross, Harney, delacosteUtamsing, & Purdy, 1981), the current study employed a more objective rating procedure, used multiple independent raters, and demonstrated high interrater reliability. More recent investigations have employed computer-based pitch analyzers to do a more sophisticated acoustical analysis of affective prosody (Ross, Edmondson, Seibert, & Homan, 1988; Shapiro & Danly, 1985). However, the equipment is expensive and is not widely available in acute-care clinical settings where aprosodia cases are most common. Acoustical analysis is most useful in studying the degree of variability in affective prosody; it currently is not as useful in studying the more qualitative features of affective prosody that make it possible for a listener to distinguish one affect from another or identify the same affect across individuals (Ross, Edmondson, Seibert, & Homan, 1988). Thus, there is a role in the evaluation of aprosodic patients for less expensive, objective psychometric methods that can capture more of the qualitative features of affective communication. A dissociation between deficits in affective prosody and affective facial gesture has previously been noted (Ross, 1981), and was found in our case as well. While only the production of affective prosody was impaired, both imitation and production of affective facial gestures were impaired. Production of affective gestures was rated as more impaired than imitation by the authors, but this pattern was not duplicated by the two additional naive raters. It is unlikely that the dissociation between prosody and gesture in our patient is due to his mild lower left facial weakness as careful attention was paid to the upper face in scoring the patient’s responses. An alternative hypothesis is that affective prosody and gesture are mediated by distinct areas within the right hemisphere that are, however, in close physical proximity.

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and C. Hodnett

This would permit them to be differentially impacted by a focal lesion, while still having a high rate of concomitance following larger lesions. If this interpretation is correct, then the central feature of aprosodia may be a prosodic deficit, with the gestural disorder being only a frequent companion. It is notable, that in our patient, only the prosodic deficit matched the pattern of deficits in transcortical motor aphasia. Perhaps the gestural disorder may more accurately be considered an apraxia for facial expressions. Finally, it should be noted that our patient showed a deficit not only in producing affective facial gestures, but also in producing complex facial movements even when there was no intent to communicate an emotion. This is consistent with our interpretation of his gestural deficit as an apraxia. Righthemisphere-damaged patients have been shown to be impaired in both affective and nonaffective prosody (e.g., the ability to change a statement into a question via voice inflection) (Weintraub, Mesulam, & Kramer, 1981). Our findings suggest that the gestural deficit is also not limited to affective expressions, but instead encompasses a broad range of complex facial movements. The importance of assessing affective communication is highlighted in this case since the patient, following resection of the astrocytoma, showed largely normal performance on a variety of other tests considered to be sensitive indicators of frontal lobe pathology including Luria’s Motor Programmes and the Wisconsin Card Sorting Test. Many “frontal lobe tests” used by neuropsychologists are mainly sensitive to left frontal lobe injury., Consequently, some right frontal lobe patients could be misclassed as normal if attention is not paid to their affective communication. We believe our results, along with the growing literature on aprosodia, warrants the inclusion of measures of affective communication in neuropsychological examinations.

REFERENCES Alexander, M. P., & LoVerme, S. R. (1980). Aphasia after left hemispheric intracerebral hemorrhage. Neurology, 30,1193-1202. Alexander, M. I?, & Schmitt, M. A. (1980). The aphasia syndrome of stroke in the left anterior cerebral artery territory. Archives of Neurology, 37.97-100. Benson, D. F. (1985). Aphasia. In K. M. Heilman & E. Valenstein (Eds.), Clinical neuropsycholgy (2nd ed.). (pp. 1748). New York: Oxford University Press. Benton, A. L., & Hamsher, K. deS. (1978). Multilingual aphasia exuminufion. Iowa City: University of Iowa. Benton, A. L., Hamsher, K. de&, Vamey, N. R., & Spreen, 0. (1983). Contributions to neuropsychologicui assessment. New York: Oxford University Press. Dahlstrom, W. G., Welsh, G. S., & Dahlstrom, L. E. (1975). An MMPI handbook, WI. Clinical interpret&ion. Minneapolis: University of Minnesota Press. Damasio, A. R., & Geschwind, N. (1984). The neural basis of language. Annual Review of Neuroscience,

7.127-148.

Delis, D., Kramer, J., Ober, B. A., & Kaplan, E. (1986). The Culiforniu verbal learning test: Administrution and interpret&on. New York The Psychological Corporation.

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Motor Aprosodia

99

Freedman, M., Alexander, M. P., & Naeser, M. A. (1984). Anatomical basis of transcortical motor aphasia. Neurology, 34,409417. Gorelick, P. B., & Ross, E. D. (1987). The aprosodias: Further functional-anatomical evidence for the organization of affective language in the right hemisphere. Journal of Neurology, Neurosurgery and Psychiatry, 50.553-560.

Grant, D. A., & Berg, E. A. (1948). A behavioral analysis of degree of reinforcement and ease of shifting to new responses in a Weigl-type card-sorting problem. Journal of Experimental Psychology, X&40441 1. Lezak, M. D. (1983). Neuropsychological assessment (2nd ed.). New York: Oxford University Press. Luria, A. R. (1980). Higher corticalfunctions in man (2nd ed.). New York: Basic Books, Inc. Matthews, E. G., & Klove, H. (1964). Instruction manual for the adult neuropsychology test battery. Madison, WI: University of Wisconsin Medical School. Monrad-Krohn, G. H. (1947). Dysprosody or altered “melody of language.“Brain, 70.405-415. Reitan, R. M., & Davison, L. A. (1974). Clinical neuropsychology: Current status and applicatiom. New York: Hemisphere. Ross, E. D. (1981). The aprosodias. Functional-anatomic organization of the affective components of language in the right hemisphere. Archives of Neurology, 38.561-569. Ross, E. D. (1985). Modulation of affect and nonverbal communication by the right hemisphere. In M. M. Mesulam (Ed.), Principles of behavioral neurology (pp. 234-257). Philadelphia: F. A. Davis. Ross, E. D. (1988) Prosody and brain lateralization: Fact vs. fancy or is it all just semantics? Archives of Neurology, 45.338-339.

Ross, E. D., Anderson, B., & Morgan-Fisher, A. (1989). Crossed aprosodia in strongly dextral patients. Archives of Neurology, 46.206-209. Ross, E. D., Edmondson, J. A., Seibert, G. B., & Homan, R. W. (1988). Acoustic analysis of affective prosody during right-sided Wada test: A within-subjects verification of the right hemisphere’s role in language. Brain andlanguage, 33,128-145. Ross, E. D., Harney, J. H., delacoste-Utamsing, C., & Purdy, P D. (1981). How the brain integrates affective and propositional language into a unified behavioral function. Hypothesis based on clinico-anatomic evidence. Archives qfNeurology, 38.745-748. Ross, E. D., & Mesulam, M. M. (1979). Dominant language functions of the right hemisphere? Prosody and emotional gesturing. Archives qfNelrrology, 36, 144-148. Rubens, A. B. (1975). Aphasia with infarction in the territory of the anterior cerebral artery. Cortex, 11.239-250. Shapiro, B., & Danly, M. (1985). The role of the right hemisphere in the control of speech prosody in propositional and affective contexts. Brain and Language, 25.19-36. Tucker, D. M., Watson, R. T., & Heilman, K. M. (1977). Discrimination and evocation of affectively intoned speech in patients with right parietal disease. Neurology, 27.947-950. Wechsler, D. A. (1945). A standardized memory scale for clinical use. Journal of Psychology, 19, 87-95.

Wechsler, D. A. (1981). Wechsler Adult Intelligence Scale Revised Manual. New York: The Psychological Corporation. Weintraub, S., Mesulam, M. M., & Kramer, L. (1981). Disturbances in prosody. A right-hemisphere contribution to language. Archives qfNeurology, 38,742-744. Wolfe, G. I., & Ross, E. D. (1987). Sensory aprosodia with left hemiparesis from subcortical infarction: Right hemisphere analogue of sensory-type aphasia with right hemiparesis? Archives of Neurology, 44,668-67 1.