NOTE REVERSAL OF EAR ADVANTAGE IN RECOVERY REPORT NANCY NICCU~I’ and Hennepin County Medical Center, (Accepted ALAS APHASIA: A CASE B. RURESS hlinneapolis, 70 November FROM Minnesota. U.S.A. 1982) Abstract-A reversal from a left ear advantage to a right ear advantage on a digit dichottc listening test was observed during the first 3 months post-onset of aphasta In a 52-yr-old male patient. Explanations for this pattern of recovery were discussed under both a “lesion effect” and a “dominance effect” interpretation. COSTRIBUTION of the two cerebral hemispheres to recovery from aphasia is an issue that has evoked considerable interest in recent years. Investigators have sought to identify ways of determining the extent to which recovery of language is based on reorganization of function in the left hemisphere or on transfer of function to the right hemisphere. DARLEY [3] suggested that verbal dichotic listening tests might provide information relevant to this question. However. despite the fact that most studies report virtually identical outcomes, two quite different interpretations of the direction and magnitude of dichotic ear advantages observed for aphasic patients have predominated in the literature [l, 5, 6, 8. 9, 1 l-13]. The “dominance effect” interpretation postulates that ear advantages observed for aphasic patients reflect hemispheric dominance for language processing in the same fashion as ear advantages observed for non-brain-damaged listeners [ 1,5,9, 123. That is, the higher score occurs for the ear contralateral to the dominant hemisphere. The “lesion effect” interpretation assumes that degradation due to the lesion may “interact with and possibly override the premorbid ear asymmetry so that dominance can no longer be inferred” [13, p. 1573. Thus, the left ear advantages (LEA’s) that are the most common observation for aphasic patients are interpreted as a reflection of right hemisphere language processing under the dominance effect interpretation and as a reflection ofdamage in the hemispherecontralateral to the ear with the lower score (i.e., ofleft hemisphere damage) under the lesion effect interpretation. Investigators that have looked at changes in dichotic listening performance over time in aphastc patients have either tested for diflerences between subjects grouped on the basis of time post-onset [I, 51 or have used a test-retest procedure [l. 9. 121. Most of these studies have reported increases in the magnitude oj le/i ear otkcmrages (LEA’s) over time and have interpreted this finding to be evidence of increusing rronsfer of‘languuge dominance to Ihe right hemisphere during recovery from aphasia [5, 9, 121. However, systematic longitudinal invaestigations ofdichotic listening performance for individual aphasic patients have not been reported. We currently are obtatning such information as part of a comprehensive study of recovery from aphasia. This report will describe the on/~ case of a clear reversal in ear advantage over time that we have observed in the longitudmal data collected for more than 25 aphasic patients. THE METHOD The patient was a 52-yr-old, right-handed, white male with 8 yr of formal education. His neurological history included mild closed-head trauma with a 4-hr confusional state 34 yr prior to the present illness and treated hypertension of recent onset. The present illness, a stroke. was characterized by a transient flaccid right brachial *Address correspondence to: Nancy E. Niccum, Ph.D., Aphasia Unit, 701 Park Avenue South, Minneapolis, MN 55415. Tel: (612) 347-5848. 265 Hennepin County Medical Center, 266 KOTE monoplegia and global aphasia soon after admission. However. the motor hndmgs became mmimal within several hours. and his language deficit evolved into a persisting conduction aphasia. Emergency angiography was significant only for minimal plaque formation bilaterally at the origins of the internal carotid arteries. Initial CT scans demonstrated a non-enhancing, low-attenuation lesion in the left temporopartetal region without mass effect. He was seen by us at monthly intervals from 1 to 6 months post-onset of symptoms and again at 9 and 12 months. Minimal right upper extremity weakness and a right homonymous hemianopia were present at hfonth 1. but had resolved by the second month. No pathologic reflexes were exhibited at any month. Sensory examinatton was normal on all visits. A schematic representation of this patient’s lesion location is shown along with four sections from a computerized tomographic (CT) scan obtained at 5 months post-onset in Fig. I. Small, patchy areas of low attenuation were seen just anterior and lateral to the left frontal ventricular horn. Another small lesion was noted in the posterior portion of the insula that extended into the adjacent intrasylvian portion of the posterior temporal lobe where it meets the insula and the parietal operculum. However, Heschl’s gyrus and the remaining planum temporale appeared to be spared. A separate lesion involved supramarginal cortex with deep white matter extension reaching the trigone of the left lateral ventricle. Sfimdi and procedures The dichotic digit test used in the present study has been described previously [lo, 111. The stimuli include the numbers 1-6, spoken by a male talker, and aligned by reference to the onset of energy in the digitized waveforms. Each ofthesix numbers were paired with the other five in the two possible stimulus-to-channel orientations to create 30 different pairs. The patient was seen at monthly intervals from Month 1 through Month 6 and then again at Months 9 and 12. The Neurosensory Center Comprehensice Examinationfor Aphasin (NCCEA) and the dichotic digit test were given each month. The Boston Dingnosric Aphasia Examinarion (BDAE) was given on Months 1.3,6.9 and 12. All dichotic tests were administered in a sound-treated booth (Korfund, Noiseguard). The patient identified 30 stimuli/ear in the monotic conditions and 60 pairs ofstimuli in the dichotic conditions of the digit test. The order in which ears were tested in the monotic conditions and the channel-to-ear orientations in the dichotic conditions were counterbalanced across months. Channel-to-ear orientations also were reversed after the first 30 pairs within months. RESULTS Pure tone audiometry on Month 1 revealed bilaterally symmetrical (within 10 dB) normal thresholds at 250,500 and loo0 Hz. Hearing losses at 2000 and 4000 Hz ranged from mild to severe, with the more pronounced losses observed for the left ear (LE). Estimates ofspeech reception thresholds for the two ears (average of thresholds at 500, 1000 and 2000 Hz) differed by 18 dB. Retest on Month 6 indicated good pure tone threshold stability. Actual speech reception thresholds were not obtained until Month 6 and at that time a 9 dB asymmetry between ears was observed with the more sensitive hearing noted for the right ear (RE). Stimuli were presented at 80 and 90 dB respectively to the right and left ears in the monotic and dichotic conditions to offset partially the differences in hearing sensitivity. Language tests revealed a moderate language impairment at 1 month post-onset that improved to a mild deficit by Month 6. Profiles on the rating scale of the BDAE indicated that the patient’s spontaneous speech was fluent with occasional paraphasias, the number of which decreased slightly between Months 1 and 6. The NCCE:A percentile scores for the Token Test and the sentence repetition subtest are shown together with the BDAE mean z-scores for auditory comprehension and phrase repetition in Table 1. Auditory comprehension for conversational speech had Table 1. Performance levels on the Token Test and the sentence repetition subtest of the NCCEA are shown in percentile scores and performance levels on the auditory comprehension and phrase repetition subtests of the BDAE are shown as mean z-scores Percentiles Token Test Sentence repetition BDAE: Mean z-scores Aud. comprehension Phrase repetition I 2 3 Months 4 post-onset 5 6 9 12 41 16 47 26 50 41 55 33 75 56 73 64 87 64 76 72 + 0.78 + 0.40 + 1.01 + 0.40 + 1.05 + 0.93 NCCEA: + 0.03 -0.91 + 0.82 -0.09 267 NOTE 0 = Deep @ = Surface FIG. 1. Four sections from a CT’scan and a schematic representation of the lesion locations. NOTE 269 returned to near normal levels by Month 3. although performances on the Token Test remained moderately impaired through Month 4. Performance on the sentence repetition subtests was disproportionately impaired on most months. This pattern of performance on the language test was felt to be most compatible with the diagnosis of conduction aphasia. The monotic condition of the digit test yielded a left ear (LE) score of 907: correct and a right ear (RE) score of 83% correct on Month 1. Scores for both ears approached ceiling (> 957;) by Month 2, but occasional errors were noted throughout the recovery study. Scores for the dichotic condition of the digit test are shown in Fig. 2. The LE FIG. 2. Changes in right (0) and left ( x ) ear scores over time on the digit dichotic test. score of 73% correct on Month 1 fell gradually to less than 60% correct by Month 6. The RE, which had the better hearing sensitivity, initially had a score near chance. However, the score for the RE improved dramatically to better than 70%correct on Month 2, and to better than 90%correct by Month 3. Thus, the initial left ear advantage (LEA) actually reversed, and became a sizable right ear advantage (REA) by Month 3. Scores for both ears evidenced only minor changes across subsequent months. DISCUSSION The reversal in ear advantage from an LEA to an REA for this patient is in direct opposition to the usual findings reported in studies of the evolution of dichotic listening performance in aphasic patients [I, 5, 9, 121. The most common observation reported in these studies is that the magnitude of LEA’s increases over time and this increase has been interpreted as evidence that language dominance is transferring increasingly to the right hemisphere as recovery occurs. Pmtr and NOLL [ 121, for example, stated that,“there is an even stronger left ear preference after this 2-month interval during which language improvement took place. Thus, there is strong evidence for the argument that a shift in dominance occurs as the aphasic improves in language ability” (p. 197). JOHNSON et al.[S] stated, “Thus, in addition to a lessening ofedema and the establishment of collateral circulation, we might wish to add the apparent shift in cerebral dominance for speech as one of the possible underpinnings for observable recovery” (p. 127). If the EA does reflect hemispheric dominance for the patient described in this report, however, then we must conclude that recovery of language function was based on a reversal from right hemisphere language dominance on Month 1 to left hemisphere dominance on Month 3. Such a course of recovery could be explained within a “dominance effect interpretation” as resulting from an initial dependence on the intact right hemisphere with progressive resumption of left hemisphere processing as recovery occurred. Independent evidence for a shift in language dominance during recovery is not available for this patient, but techniques such as positron emission tomography (PET) may be able to provide evidence relevant to this question in the future. This explanation of a shift from right hemisphere dominance to left hemisphere dominance would seem plausible, but such a pattern of recovery is directly counter to thejndings most commonly reported in the literature. Furthermore, when similar findings have been reported, they have been interpreted as ’ “lesion effects” rather than as “dominance effects”. CASTRO-CALDUS and B~TELHO Cl] obtained a significant shift toward REA’s in a group of fluent aphasic patients, 270 Nort- and they concluded that “The lesion el‘fcct reglstered in dlchotic hstenlng after the brxn lesion will disappear and a tendency to REP IS observed” (p. 151 J. However, they still interpreted the slgnficant shift toward LE,\‘s observed In non-tluent patients as ebldence of a shift III language dominance. D~XIGI~ and D-\~sIo [7] tested two patients on a single occasion sometlmedurlnp the first 3 months post-onset. Both r\ereclassified as ha\mgconduction aphasia (as was our patlent) and both exhIbIted RE “extinctlon” (LEA’s). irhich the Damaslos Interpreted as a lesion effect. diminished over the If the results for our patient are interpreted as a “lesion effect”. then the effect systematically first 3 months post-onset of symptoms. The finding of a stron, 0 imtial lesion effect for this patient IS somewhat puzzhng because both the prtmary audrtory cortex and the geniculo-cortical pathway appeared to be spared. However. three possible loci for a lesion effect habe been identified. The first IS Heschl’r gyrus. .+.lthough Ioh attenuation was not evident in the region of Heschl’s gyrus. temporary physiological dysfunction due to ischemia or due to subtotal damage of this area could still have occurred in conJunction with the lesion in the posterior insula. The second possible locus ofa lesion etTect is the observed damage that occured where the Intrasylvtan portion of the posterior temporal lobe, the insula. and the parietal operculum meet. The anatomy of the human auditory cortex is not Hell understood. but investigators recently have demonstrated “parietal extension of the auditory region” in cytoarchltectonic studies [4. p. 6051. and this area was damaged In our patient. The third possible locus of a lesion effect is the geniculo-cortical pathway. Auditory fibers leaving the medial geniculate. course laterally and superiorly toward the primary audltory cortex, until this direct route IS interrupted by the downward folding of the insular cortex. The auditory fibers at this point are forced to loop down and around the inferior aspect of the insula before continuing on to Heschl’s gyrus [7]. The geniculo-cortical pathway m this patlcnt. thus, would be immediately subjacent to the lesion in the posterior Insula. It is possible that the leston actually may have involved portions of the pathway directly, or temporary dysfunction of the pathway may have been caused by ischemia. Improvement in the RE score over time could be due to improved utilization of the remaining geniculo-cortical neurons, reduction of ischemic effects due to the establishment of collateral circulation. or powbly c\en to regenerative processes. Although independent evidence supporting the hypothesis that the “lesion erect” diminished over time is not available for this patlent, it is possible that techniques such as auditory-evoked potentials might provide such evidence in the future. The slight reduction of the LE score ober time that was observed for this patient may have resulted from increased competition as the quality of the RE signal improbed. In summary. plausible explanations of the observed reversal in ear advantage can be developed under either a “dominance effect” or a “lesion effect” interpretation. Our interpretation of dichotic listening results for aphasic patients in general, however, is that they are most compatible with a”leslon effect” [Ill. As LINEBAUGH [8] correctly pointed out, “a determination of lateral dominance based on dichotic listening tests assumes the integrity of the entire auditory system including the primary sensory and association cortices of both hemispheres and their collosal connectlons” (p. 598). and this assumption is not met for most aphasic patients. If a “dominance effect” Interpretation is adopted, however, then the direction of the reversal in ear advantage (from LEA to REA) for this patient provides evidence that recovery of language function is not mediated by a transfer of dominance to the right hemisphere in all aphasic patients. .-I~~,lo~clellyerrlvrlr \ Thts research ~a$ supported by NlNCDS thank DAVID S. KNOI~AS. M D., and Do~~r.~s Yws. M.D., Srwrs. Ph.D.. for his contributions concerning interpretation Contract NO I-NS-2378. The authors would ltkc to for their comments regarding the CT-scan and Or,\ of data from the language tests. REFERENCES 1. CASTRO-CI\LIXS. A. and BOTELMI. M. A. S. Dichotic listening In the recoberq of aphasia after stroke. Brain Lang. 10, 145-151. 1990. 1 D~MASIO, H. and DASI~SIO, A. Dlchotic listening pattern In conduction aphasia. Brain Lang. 10, X-286. 1980. ;: DARLEY. F. The efficacy of language rehabilitation in aphasia. J. Spwcl~ Hwr. Dis. 37, 3 -21. 1972. 4. GAL.ABURDA, A. and SAstt)Es. F. 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Dichotlc listening performance. language impairment. and lesion location in aphasic listeners. J. Speech Hear. Res.. in press, 1983. 271 NOTE 12. PETTIT. J. >I. and NOLL. J. D. Cerebral dominance in aphasia recovery. Bruin L~ny. 7. 191-200. 1979. 13. SCHULHOFF, C. and GOODGLASS. H. Dichotic lisrening. stde of brain injury. and cerebral dommance. .Vrwopsycholoyia 7, 149-160. 1969. L'inversion d'un avantage oour l'oreille gauche en un avantaqe POW l'oreille droite dans un test dichotique (liste de chiffres) a it6 observee au cows des trois premiers nuis suivant une aphasic chez un malade de 52 ans. L'explication de cette forme de rkuo6ration do&e est en termes d'un "effet lkion", et d'un "effet dominance". Zusammenfassung: Eine UmkehrunR einem der ersten Patienten zwei des dichotlschen 3 hlonate beobachte:. Interpretatlonen Lmksohrvortells m Zahlen Test mit nach Einsetzen ErklSrungen dlskutiert: eincn 31s der fiiv Rechtsohrvorte11 Stin;ulunmater~al Aphasle dleses Lzislonseffekt be1 emer bei wurde \‘erlaufsmuster und wShrend 5ZjShrlgen L)ominnnzeffekt. werden untet