Intern. J . Neuroscience. 1992, Vol. 63, p. 17-29
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DICHOTIC LISTENING STUDIES OF HEMISPHERIC ASYMMETRY IN BRAIN DAMAGED PATIENTS KENNETH HUGDAHL AND KNUT WESTER*
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Department of Biological and Medical Psychology, and *Department of Neurosurgery, Haukeland University Hospital, University of Bergen, Norway (Received October 5. 1990)
In the present paper we review the empirical evidence for structural versus attentional explanations of the right ear advantage (REA) phenomenon in dichotic listening (DL). The ear advantage in DL is a behavioral ”marker” of language function in the cerebral hemispheres. Dichotic listening data from four brain-lesioned patients are presented. The patients had a tumor or cyst in the left Sylvian region (2 cases); hemorrhage in the left frontotemporal region ( 1 case); and severe destruction of the left hemisphere (1 case). The results from all four patients showed marked reductions in correct recall of the right ear items, while left ear recall was left unaffected. In two of the cases, the DL data showed an immediate reinstatement of the REA after neurosurgery. It is concluded that the results favor a structural/ anatomical explanation of the ear advantage phenomenon in DL, rather than an attentional bias explanation.
The right ear advantage (REA) in dichotic listening (DL) is generally believed to reflect left cerebral hemisphere specialization for language (Kimura, 1961 ; Bryden, 1967; Studdert-Kennedy and Shankweiler, 1970; see also Hugdahl, 1988). The observation of superior right ear correct reports in the dichotic situation is a robust empirical phenomenon. However, although empirically robust, the theoretical basis for the REA, and the neurological mechanisms responsible for the effect are not completely understood (cf. Nebes and Nashold, 1980; Bradshaw and Nettleton, 1988; Springer, 1986). At the same time, because of its simplicity, two bursts of auditory signals exactly at the same time, one in each ear, the DL technique should be an ideal vehicle for an understanding of the nature of brain asymmetry in general, and language asymmetry in particular. The general outline of the DL situation is seen in Figure 1. Kimura (1967) attributed the REA to the anatomical difference in number of nerve fibers connecting to the contralateral as compared to the ipsilateral temporal cortex. As a consequence, the auditory signal from the ear should have a greater impact on the contralateral side of the brain. This has been shown to be the case when comparing the amplitude of evoked potentials over the two hemispheres of the brain, evoked by auditory input (Rosenzweig, 1950; Connolly, 1985). Furthermore, Maximilian (1982) showed an increase in regional blood flow over the contralateral temAddress all correspondence to: Professor Kenneth Hugdahl, Deqartment of Biological and Medical Psychology, Somatic Psychology Division, University of Bergen, Arstadveien 21, 5009 Bergen, Norway. FAX: 47-5-294853. The present research was financially supported by a grant from the Norwegian Medical Research Council (NAVF-RMF) to Knut Wester and Kenneth Hugdahl. 17
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FIGURE 1
K. HUGDAHL AND K . WESTER
Illustration of the basic principle behind dichotic listening in studies of languagc asymmetry
poral areas after monaural auditory input, indicating increased energy expenditure in contralateral brain areas. Finally, Rogers et al. (1990) found that the magnetic wave fields of the brain were of larger amplitude on the contralateral temporal cortex after auditory stimulation. The ascending auditory signal is propagated from the auditory receptors to the cerebral cortex. The pathway is interrupted at several levels, with the cochlear nuclei, the superior olive, the inferior colliculus, and the medial geniculate body in the posterior thalamus as important relay stations (see Figure 2 ) . According to Brodal (1981), the inferior colliculus receives fibres from the cochlear nuclei, the superior olive, and the lateral lemniscus, while it projects to the medial geniculate, the midbrain tegmentum, and the dorsolateral pontine nucleus. The projection ascending to the inferior colliculus is larger from the contralateral ear, while the projection from the colliculus is larger on the ipsilateral ear. Thus, there is a favour for the contralateral projection from the ear to the auditory cortex. Relating this to the DL situation, when two auditory signals are put in conflict (as in the dichotic situation), then the contralateral input is believed to block or suppress the ipsilateral signal. The car contralateral to the language dominant cortical side should thus project stronger than the ipsilateral ear. As a result, the projection from the ear ipsilateral to the nondominant hemisphere would have access to the processing loci, while the projection from the ear contralateral to the nondominant hemisphere would first have to traverse the corpus callosum in order to reach the processing loci in the dominant hemisphere (cf. Sparks and Geschwind, 1968). The better report obtained from the right ear (REA) in right-handed subjects is thus a consequence of the “degradation” that the left ear signal undergoes in its route to the dominant left hemisphere (Berlin, 1977; Nebes and Nashold, 1980). The REA is usually in the order of magnitude of 15-20% in normal right-handed individuals (Hugdahl, Wester and Asbjernsen, 1990a), and is observed in about 85% of a sample tested. This is shown in Figure 3 for children data. In one of her two 1961 studies, Kimura showed that patients with a REA in dichotic listening could also be verified to be left hemisphere dominant for speech when tested with the sodium amytal procedure, while patients that were right hemisphere dominant for speech when tested with sodium amytal, showed a left ear advantage (LEA) in DL. Furthermore, Witelson (1983) has shown a positive correlation between the magnitude of the REA in dichotic listening and the size of areas in the left temporal lobe important in language function. Another, less structural, view on the basis of the REA effect in dichotic listening is that ear advantages in DL are caused by attentional shifts to one ear due to biased
19
DTCHOTIC LISTENING AND BRAIN DAMAGE
PAC
MGB
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IC
FIGURE 2 Schematic outline of the auditory pathways from the cochlea in the ear to the auditory cortcx CNC = cochlear nucleus; IC = infcrior colliculus; MGB = medial geniculate body; PAC = primary auditory cortex.
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(N=126)
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F'IGURE 3 Normative data for dichotic listening performance in right- and left-handers. 8 L E = percentage left ear comect recall %RE = percent right ear correct recall. Each dot represents one Subject. Small numbers in the scatter-gram = two or more subjects occupy the same coordinates.
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K . HUGDAHL AND K . WESTER
priming or attending to certain stimuli (Kinsbourne, 1970). Kinsbourne holds the view that behavioral asymmetries reflect covert shifts of attention to the side of the more activated hemisphere for a particular kind of tasks or stimuli. This activity then “spills over” to motor centers which control activity in the contralateral side (see also Kinsbourne, 1973). Furthermore, Bradshaw and Nettleton (1988) have argued that neither the traditional dichotic paradigm nor references to the anatomy and physiology of the auditory system are necessary to generate an ear advantage. The spatial location of a sound source may be as determinant as the projection pathways from the ear to the cortex in determining an ear advantage in DL. Thus, there are two major explanatory models for the REA effect in dichotic listening, one that refers to the anatomy and physiology of the auditory system, the other that refers to attentional and other cognitive influences. The most frequently used method of validating dichotic listening performance to brain function is the administration of sodium amytal to the left or right hemisphere, and to record how speech function is suppressed when sodium amytal is injected into one hemisphere at a time. Although this probably is the most reliable method to observe brain asymmetry for language, the sodium amytal technique mainly assesses expressive speech function, while DL additionally picks up functions related to language reception. Another way of looking at a structural versus attentional explanation for the REA is to study patients with unilateral lesions restricted to one hemisphere. Several studies have reported a lesion effect such that unilateral damage to areas involving auditory pathways may lead to reduced frequency of correctly reported items from the contralateral ear (e.g. Sparks, Goodglass and Nickel, 1970). Furthermore, Roberts, Varney, Paulsen, and Richardson (1990) showed that patients with complex partial seizures improved their dichotic listening performance after anticonvulsant medication. This is what may be expected from a structural explanation for the REA effect. However, from the point of view of an attentional explanation, unilateral left temporal lobe damage should not necessarily lead to a drastic reduction in the contralateral right ear report, the decrease may as well be manifested in a reduction of correct reports from the ipsilateral ear (cf. Hugdahl, Wester, and Asbjomsen, 1990b). In the present paper we report four cases of unilateral brain lesions who were the subjects for neurosurgery. All patients were between 18 and 28 years, and were referred to the neurosurgery unit because of tumors or cysts in the left temporal lobe (2 cases); hemorrhage from the left middle cerebral artery (1 case), and severe destruction of the left hemisphere in a traffic accident (1 case). Three of the patients were right-handers, one was a left-hander (see details about each patient below). The Dichotic Test
In addition to the dichotic test, the patient’s hearing was tested by a standard audiometer screening technique in order to assess hearing capacity within the critical 500-6000 Hz region for dichotic stimuli. The dichotic stimulus-materials consisted of the six stop-consonants /b/, /d/, /g/, /p/, /t/, /k/ which were paired with the vowel /a/ to form six basic consonant-vowel (CV) syllables (/ba/, /ga/, /pa/, etc.). The syllables were paired with each other for all possible combinations, thus yielding 36 pairs including the homonymic pairs (the homonyms were used as test trials and excluded from statistical analysis). Each pair was randomly recorded three times on the tape. Thus, the total number of trials on the tape was 108. The intertrial interval (ITI) between stimulus presentations varied between 4 and 5 s. The dichotic tape was prepared on a
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PDP 11/45 computer. Each CV-syllable had a duration of 320 ms., and temporal alignment between channels was set at the first visible energy-release in the conqo-ant segment of each syllable. Maximum onset difference between the channels was 0.5 ms. due to D / k multiplexer resolution and the sampling frequency (10 KHz). Each syllable was originally read by a male voice and fed to the computer. After computer analysis, the syllables were recorded onto a NAGRA IV tape recorder. In order more easily to test the patients in the hospital environment the NAGRA tape was copied onto a chrome dioxide cassette and played from a SONY WM DD I1 minicassette player with “plug-in”-type earphones. The output of the minicassette player was calibrated and the mean intensity was 84 db SPL measured by a Bruel and Kjaer 2204 sound level meter. The patients had to answer with the syllable they heard on each trial. The answer was marked by the experimenter on a specially designed scoring-sheet. A short pause was put in after every list of 36 dichotic presentations in order to give the patient some rest (and in some of the patients to give new instructions). Two of the patients reported below also had to go through two forced-attention conditions (see Hugdahl and Anderson, 1986) in which attention was focused on either the right or left ear input. In the “nonforced” attentional condition, the patient was instructed to report the syllable he/she identified best. Thus, no specific instruction concerning allocation of attention was given. In the “forced-right’’ condition, the patient was told to attend only to the right ear and to report only from that ear. In the “forced-left” condition, he/she was told to focus attention on the left ear input and report only from that ear. Order of presentation of the three conditions was randomized across test-sessions. The audiometer screening tests for hearing acuity included presentations of tones between 500 and 6000 Hz (which includes most of the energy in the CV-syllable). Threshold differences between the ears were not allowed to exceed 10 db at any frequency. CASE REPORTS Case # I The first case study was aimed at elucidating the structural versus attentional explanations for ear advantage effects in DL. Sparks and Geschwind (1968) showed that the left ear signal in DL was almost extinct in a patient with callosotomy. They attributed this finding to the fact that the left ear signal, reaching only the right hemisphere through the contralateral pathways, could not be transmitted to the left hemisphere for processing because of sectioning of the corpus callosum. Thus, the Sparks and Geschwind (1968) finding provides support for a structural explanation. One way to follow-up and to test the structural model further would be to show that a patient with a right hemisphere language dominance, and with a left hemisphere lesion (or disrupted callosal transmission) would reveal a right ear extinction effect. Furthermore, if the patient did not increase right ear correct reports when focusing attention to only the right or left ear, an attentional explanation for the ear advantage effect in DL would be even less likely. The patient was a young left-handed female (tested with the handedness questionnaire developed by Raczkowski, Kalat and Nebes, 1974) who had suffered a severe head injury in a traffic accident a few years before. She had virtually no remaining left hemisphere tissue. Since she did not show any signs of speech or language disturbance despite a nonexistent left hemisphere, she had to be using the
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K. HUGDAHL AND K. WESTER
right hemisphere for language. It was therefore predicted that she should demonstrate a drastic reduction in right ear performance in the DL test (contralateral to the damaged left hemisphere), while left ear performance should remain intact. From a structural explanation, there should furthermore be no major changes in performance when instructed to attend to either side. An attentional explanation would, however, mean that although the contralateral right ear signal would be blocked because of tissue loss in the left hemisphere, the ipsilateral pathway would be intact, with the result that attending to the right ear should drastically increase right ear performance. Figure 4 shows a computer tomography (CT) scan revealing the substantial tissue loss in the left hemisphere. The patient had normal hearing thresholds for both ears when tested with screening audiometry before the dichotic tests. She was tested about four years after her initial trauma, and under all three attentional instructions. The dichotic listening results are seen in Figure 5; her right ear scores were zero, or close to zero for all three attentional conditions, while her left ear scores were between 67% correct to 87% correct (which is within the normal range). There are two arguments for the view that she was right hemisphere dominant for language before the accident; 1) she was a left-hander, with an increased probability of right hemisphere language dominance (Fennell, 1986), and 2) her language functions were intact after near-complete destruction of the left hemisphere. The present data thus favor a structural rather than an attentional explanation. The absence of any correct reports from the right ear in the DL situation (despite normal hearing) must be attributed to the fact that the contralateral right ear signal is blocked from further transmission after reaching the (remaining) left temporal areas. Attending to either ear did not affect the right ear scores. The number of correctly reported items were zero in both the forced-attention conditions (see Figure 5 ) . It is therefore unlikely that an attentional model, which attributes the ear advantage to a biased priming effect of attending to a particular ear of input, can explain dichotic listening performance. Case # 1 has revealed a paradoxical right ear extinction effect in a left-hander with an almost nonexisting left hemisphere. This is a new finding, since previously only left ear paradoxical effects have been reported in the literature after unilateral hemisphere lesions. Case #2
The second case was a young right-handed male who underwent craniotomy because of an intracerebral, spheric tumor in the left central region above the Sylvian fissure. The location and extent of the tumor is seen in Figure 6 which shows a magnetic resonance image (MRI) of the location and extent of the tumor. The tumor was radically removed during craniotomy, and a control MRI one month after surgery showed no signs of residual tumor. The patient did not show any overt signs of language disturbance in the neurological examination after being admitted to the hospital. However, since the tumor was located in the left Sylvian fissure affecting the language receptive areas, he was admitted to dichotic listening testing. It was hypothesized that one effect of the tumor would be an increased intracerebral pressure on the surrounding tissue, possibly affecting the processing of the contralateral right ear signal. If this was true, it could be predicted that the patient should reveal a lejl ear advantage (LEA) when tested before the operation, but a right ear advantage (REA) when tested after the operation. Since the patient was consistently right-handed when tested with the hand-
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DICHOTIC LISTENING AND BRAIN DAMAGE 23
5
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Case # 1 Rfar
LEar
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FIGURE 5 Mean percentage correct reports from the left (LEar) and right (REar) ears in dichotic listening in Patient # 1 during three different attentional instructions. See text for further explanations.
edness questionnaire (Raczkowski, et al. 1974) he would most likely also be left hemisphere dominant for language (Bryden, 1988). Thus, a shift from a LEA to a REA after the removal of the tumor would further strengthen a structural explanation of the ear advantage in DL, and also validate the DL procedure. The patient was tested with dichotic listening the day before surgery, two days after surgery, four days after surgery, and five weeks after surgery. For clinical reasons he was only tested with the nonforced attentional instruction. Hearing was normal when tested with audiometer screening. The DL results for percentage correctly reported items from the right and left ear during the four test occasions are seen in Figure 7. As can be seen in Figure 7, the patient had a slight overall reduction in correctly reported items compared to the normative data (see above, and Figure 3). However, more important, he showed a leji ear advantage on the day before surgery that shifted to a right ear advantage almost immediately after the removal of the tumor. Second, the right ear advantage stayed stabile at both the immediate and long-term followup tests (see Figure 7). It is further interesting to note that the magnitude of the REA at the five weeks follow-up test was clearly in the normal region (in the order of 20%). The slight difference in the magnitude of the REA from the first to second postoperative test was probably due to the edema caused by the operation. To sum up, Case #2 has shown an example of how displacement of brain tissue in the left
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FIGURE 6 MRI scan showing the location of a tumor above the left Sylvian fissure in Patient #2. Note that the left side of the brain is shown to the right in the scan according to radiological standards.
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FIGURE 7 Mean percentage correct reports from the left and right ears in dichotic listening in Patient #2. Pre-op = The day before operation; Post-opI = Two days after the operation; Post-opII = four days after the operation; Post-opIII = five weeks after the operation.
K. HUGDAHL AND K. WESTER
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=
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FIGURE 8 Mean percentage correct reports from the left (LEar) and right (REar) in dichotic listening in Patient #3 during the three attentional instructions (see text for further details).
hemisphere that is involved in language processing also disrupts the contralateral right ear signal in dichotic listening, resulting in a left ear advantage (in an otherwise left hemisphere language dominant person). Removal of the pressure-inducing force in the critical areas in the temporal lobe has the consequence of an almost immediate shift back to a normal right ear advantage which then persists, and grows stronger as the patient recovers from the operation. Thus, DL seems to monitor closely hemisphere language function on a neuroanatomical basis. Case #3
The third patient had a subarachnoid hemorrhage involving an aneurysm of the left middle cerebral artery. He had a manifest motor aphasia when admitted to hospital, which gradually improved during the next three weeks. He was treated conservatively for the hemorrhage with bedrest for three weeks at the hospital. He was tested with dichotic listening the first time two days before he was released from the hospital, i.e., about three weeks after acute illness. He was later retested 3.5 months after the first DL test. The results from the DL tests are seen in Figure 8; patient #3 showed a reduction in correct right ear reports (down to the order of 10%). This was furthermore independent of attentional instruction. Thus, instructing the patient to attend to the right ear did not affect his right ear scores (see Figure 8). Left ear performance was
DICHOTIC LISTENING AND BRAIN DAMAGE
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in the normal 60-70% region, with a slight decrease during the forced-right condition, and an increase during the forced-left condition. Thus, correctly reported items from the left ear was affected by the attentional conditions (a slight reduction in left ear performance when attending to the opposite right ear, and a marked increase when attending to the “correct” left ear). Right ear performance was however not affected by the attentional instructions. It, therefore, seems that the hemorrhage in language areas in the left hemisphere suppresses processing of the contralateral right ear signal, and this cannot be counteracted by focusing attention to the right ear.
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Case #4
Patient #4 had a slightly expanding arachnoid cyst in the left temporal lobe believed to cause his moderate clinical symptoms (headache). The cyst was drained with a shunt. He did not show any overt signs of language disturbance in the neurological examination. The patient was tested with the standard DL set-up used with the other reported cases, including forced-attention instructions in addition to the free-report instruction. The patient was a right-handed 23-year old male. He was tested the first time the day before the operation, and the second time the day after operation, he was then followed-up in a third test six weeks after the operation. The DL results are seen in Figure 9 (only data from the nonforced attentional condition are reported). As can be seen in Figure 9, the overall level of performance was reduced preoperatively. More importantly, however, there was no significant REA preoperatively. This is probably explained as a result of the increased force on brain tissue in the temporal lobe critically involved in auditory processing. Since the dichotic listening situation means that the contralateral right ear signal normally should have better access to the left temporal areas, absence of the REA indicates in this case that the right ear signal is suppressed because of displacement of tissue in this region of the brain. Looking at the results from the two postoperation tests in Figure 9 (middle and right hand panels), the REA appears immediately the day after operation, and it is still present at the six weeks follow-up test (right hand panel in Figure 9). Another important aspect of the data in Figure 9 is that not only does the REA appears on the day after the operation, but overall right ear performance also increases into the normal range. The magnitude of the REA is also within the normal range seen in young adult males (about 20%). A final aspect of the results is that the REA during the two postoperation tests are caused by an increase in right ear performance (see Figure 9). Since right ear performance in DL is both anatomically (Kimura, 1967; Eslinger and Damasio, 1988), and physiologically (Strauss, 1988) linked to left temporal lobe functioning, it is difficult to escape the conclusion that DL is a sensitive index of functional brain recovery (cf. Hugdahl, et al., 1990b). Summary and Conclusions
In the present report we have presented dichotic listening data from four case-studies with various lesions in the left hemisphere. In two of the right-handed cases, there was a marked reduction in contralateral right ear performance before surgical treatment. This behavioral deficit was drastically improved immediately after surgery, indicating both a structural and functional relationship between contralateral ear performance and left hemisphere language function.
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Case # 4
go
I I
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FIGURE 9 Mean percentage correct reports from the left (LEar) and right (REar) ears in dichotic listening in Patient #4. Pre-op = the day before the operation; post-opI = the day after the operation; Post-opll = six weeks after thc operation.
The lesion-approach to DL provides a new way of validating the dichotic listening technique for the study of brain asymmetry. The results further support a structuralanatomical rather than a functional-attentional explanation of the ear advantage phenomenon seen in dichotic listening. This strengthens the theoretical model of the REA in dichotic performance provided by Kimura (1967). There are clinical and radiological reasons to believe that Patients #2 and 4 had lived with their expanding pathological conditions (tumor and cyst) for many years. The prompt normalization of DL-findings after decompressive surgery in these patients is therefore surprising. It indicates that even brain tissue that has been suppressed for many years due to local pressure, may regain its language functions. It is furthermore possible that the results of the DL-tests may provide information that is relevant for indications for operation. This is especially relevant for patients with mild to moderate overt symptoms from congenital arachnoid cysts.
REFERENCES Berlin, C. I. (1977). Hemispheric asymmetry in auditory tasks. In S . Hamad, R. W. Doty. L. Goldstein, J. Jaynes. & (3. Krauthamer (Eds.). Lorertrlizarion in the n e r w i u sysrern. New York: Academic Press.
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Bradshaw, J. L. & Nettleton, N. C. (1988). Monaural asymmetries. In K. Hugdahl (Ed.). Handbook of dichotic listening: Theory, methods, and research. Chichester, U.K.: Wiley & Sons. Brodal, A. (1981). Neurological anatomy in relation to clinical medicine. (3rd ed.) New York: Oxford University Press. Bryden, M. P. (1967). An evaluation of some models of laterality effects in dichotic listening. Acta Oto-Laryngologica, 63, 595-435. Bryden, M. P. (1988). An overview of the dichotic listening procedure and its relation to cerebral organization. In K. Hugdahl (Ed.). Handbook of dichotic listening: Theory, methods, and research. Chichester, U.K.: Wiley & Sons. Connolly, J. F. (1 985). Stability of pathway-hemispheric differences in the auditory event-related potential (ERP) to monaural stimulation. Psychophysiology, 22, 87-96. Eslinger, P. J. & Damasio, H. (1988). Anatomical correlates of paradoxic ear extinction. In K. Hugdahl (Ed.). Handbook of dichotic listening: Theory, methods, and research. Chichester, U . K . : Wiley & Sons. Fennel]. E. B. (1986). Handedness in neuropsychological research. In J. Hannay (Ed.). Experimental techniques in human neuropsychology . New York: Oxford University Press. Hugdahl, K. (1988). Handbook of dichotic listening: Theory, methods, research. Chichester, U.K.: Wiley & Sons. Hugdahl, K. & Andersson, L. (1986). The “forced-attention paradigm” in dichotic listening to CVsyllables: A comparison between adults and children. Cortex. 22, 417-432. Hugdahl, K., Wester, K., & Asbjarnsen, A. (1990a). The role of the left and right thalamus in language asymmetry: Evidence from Parkinson patients undergoing stereotactic thalamotomy . Brain and Language, 39, 1-13. Hugdahl, K., Wester, K., & Asbjarnsen, A. (1990b). Dichotic listening in an aphasic male patient after a subcortical hemorrhage in the left fronto-parietal region. International Journal of Neuroscience, 54, 139-146. Kimura, D. (1961). Some effects of temporal lobe damage on auditory perception. Canadian Journal Of PSyChOlOgy, 15, 156-165. Kimura, D. (1967). Functional asymmetry of the brain in dichotic listening. Cortex, 3 , 163-168. Kinsbourne, M. (1970). The cerebral basis of lateral asymmetries. Acta Psychologica, 33, 193-201. Maximilian, V. A. (1982). Cortical blood flow asymmetry during monaural verbal stimulation. Brain and Language, 15, 1-11. Nebes, R. D. & Nashold, B. S. (1980). A comparison of dichotic and visuo-acoustic competition in hemispherectomized patients. Brain and Language, 9, 246-254. Raczkowski, D., Kalat, J . W., & Nebes, R. D. (1974). Reliability and validity of some handedness questionnaire items. Neuropsychologia, 12, 43-47. Roberts, R. J., Varney, N. R., Paulsen, J. S., & Richardson, E. D. (1990). Dichotic listening and complex partial seizures. Journal of Clinical and Experimental Neuropsychology, 12, 448-458. Rogers, R. L., Papanicolaou, A. C., Baumann, S. B., Eisenberg, H. M., & Saydjari, C. (1990). Spatially distributed cortical excitation patterns of auditory processing during contralateral and ipsilateral stimulation. Journal of Cognitive Neuroscience, 2, 44-50. Rosenzweig, M. R. (1951). Representations of the two ears at the auditory cortex. American Journal O f Physiology, 167. 147-214. Sparks, R. & Geschwind, N. (1968). Dichotic listening in man after section of neocortical commissures. Cortex. 4 , 3-16. Sparks, R., Goodglass, H., & Nickel, B. (1970). Ipsilateral versus contralateral extinction in dichotic listening resulting from hemispheric lesions. Cortex. 6, 249-260. Springer, S. P. (1986). Dichotic listening. In J. Hannay (Ed.). Experimental techniques in human neuropsychology. New York: Oxford University Press (pp. 138-166). Strauss, E. (1988). Dichotic listening and sodium amytal: Functional and morphological aspects of hemispheric asymmetry. In K. Hugdahl (Ed.). Handbook of dichotic listening: Theory, methods, and research. Chichester, U.K.: Wiley & Sons (pp. 117-138). Studdert-Kennedy, M. & Shankweiler, D. (1970). Hemispheric specialization for speech perception. Journal of the Acoustical Sociely of America, 48, 415-420. Witelson, S. F. (1983). Bumps on the brain: Right-left asymmetry as a key to functional lateralization. In S. J. Segalowitz (Ed.). Language functions and brain organization. New York: Academic Press.
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DICHOTIC LISTENING STUDIES OF HEMISPHERIC ASYMMETRY IN BRAIN DAMAGED PATIENTS KENNETH HUGDAHL AND KNUT WESTER*
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Department of Biological and Medical Psychology, and *Department of Neurosurgery, Haukeland University Hospital, University of Bergen, Norway (Received October 5. 1990)
In the present paper we review the empirical evidence for structural versus attentional explanations of the right ear advantage (REA) phenomenon in dichotic listening (DL). The ear advantage in DL is a behavioral ”marker” of language function in the cerebral hemispheres. Dichotic listening data from four brain-lesioned patients are presented. The patients had a tumor or cyst in the left Sylvian region (2 cases); hemorrhage in the left frontotemporal region ( 1 case); and severe destruction of the left hemisphere (1 case). The results from all four patients showed marked reductions in correct recall of the right ear items, while left ear recall was left unaffected. In two of the cases, the DL data showed an immediate reinstatement of the REA after neurosurgery. It is concluded that the results favor a structural/ anatomical explanation of the ear advantage phenomenon in DL, rather than an attentional bias explanation.
The right ear advantage (REA) in dichotic listening (DL) is generally believed to reflect left cerebral hemisphere specialization for language (Kimura, 1961 ; Bryden, 1967; Studdert-Kennedy and Shankweiler, 1970; see also Hugdahl, 1988). The observation of superior right ear correct reports in the dichotic situation is a robust empirical phenomenon. However, although empirically robust, the theoretical basis for the REA, and the neurological mechanisms responsible for the effect are not completely understood (cf. Nebes and Nashold, 1980; Bradshaw and Nettleton, 1988; Springer, 1986). At the same time, because of its simplicity, two bursts of auditory signals exactly at the same time, one in each ear, the DL technique should be an ideal vehicle for an understanding of the nature of brain asymmetry in general, and language asymmetry in particular. The general outline of the DL situation is seen in Figure 1. Kimura (1967) attributed the REA to the anatomical difference in number of nerve fibers connecting to the contralateral as compared to the ipsilateral temporal cortex. As a consequence, the auditory signal from the ear should have a greater impact on the contralateral side of the brain. This has been shown to be the case when comparing the amplitude of evoked potentials over the two hemispheres of the brain, evoked by auditory input (Rosenzweig, 1950; Connolly, 1985). Furthermore, Maximilian (1982) showed an increase in regional blood flow over the contralateral temAddress all correspondence to: Professor Kenneth Hugdahl, Deqartment of Biological and Medical Psychology, Somatic Psychology Division, University of Bergen, Arstadveien 21, 5009 Bergen, Norway. FAX: 47-5-294853. The present research was financially supported by a grant from the Norwegian Medical Research Council (NAVF-RMF) to Knut Wester and Kenneth Hugdahl. 17
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FIGURE 1
K. HUGDAHL AND K . WESTER
Illustration of the basic principle behind dichotic listening in studies of languagc asymmetry
poral areas after monaural auditory input, indicating increased energy expenditure in contralateral brain areas. Finally, Rogers et al. (1990) found that the magnetic wave fields of the brain were of larger amplitude on the contralateral temporal cortex after auditory stimulation. The ascending auditory signal is propagated from the auditory receptors to the cerebral cortex. The pathway is interrupted at several levels, with the cochlear nuclei, the superior olive, the inferior colliculus, and the medial geniculate body in the posterior thalamus as important relay stations (see Figure 2 ) . According to Brodal (1981), the inferior colliculus receives fibres from the cochlear nuclei, the superior olive, and the lateral lemniscus, while it projects to the medial geniculate, the midbrain tegmentum, and the dorsolateral pontine nucleus. The projection ascending to the inferior colliculus is larger from the contralateral ear, while the projection from the colliculus is larger on the ipsilateral ear. Thus, there is a favour for the contralateral projection from the ear to the auditory cortex. Relating this to the DL situation, when two auditory signals are put in conflict (as in the dichotic situation), then the contralateral input is believed to block or suppress the ipsilateral signal. The car contralateral to the language dominant cortical side should thus project stronger than the ipsilateral ear. As a result, the projection from the ear ipsilateral to the nondominant hemisphere would have access to the processing loci, while the projection from the ear contralateral to the nondominant hemisphere would first have to traverse the corpus callosum in order to reach the processing loci in the dominant hemisphere (cf. Sparks and Geschwind, 1968). The better report obtained from the right ear (REA) in right-handed subjects is thus a consequence of the “degradation” that the left ear signal undergoes in its route to the dominant left hemisphere (Berlin, 1977; Nebes and Nashold, 1980). The REA is usually in the order of magnitude of 15-20% in normal right-handed individuals (Hugdahl, Wester and Asbjernsen, 1990a), and is observed in about 85% of a sample tested. This is shown in Figure 3 for children data. In one of her two 1961 studies, Kimura showed that patients with a REA in dichotic listening could also be verified to be left hemisphere dominant for speech when tested with the sodium amytal procedure, while patients that were right hemisphere dominant for speech when tested with sodium amytal, showed a left ear advantage (LEA) in DL. Furthermore, Witelson (1983) has shown a positive correlation between the magnitude of the REA in dichotic listening and the size of areas in the left temporal lobe important in language function. Another, less structural, view on the basis of the REA effect in dichotic listening is that ear advantages in DL are caused by attentional shifts to one ear due to biased
19
DTCHOTIC LISTENING AND BRAIN DAMAGE
PAC
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FIGURE 2 Schematic outline of the auditory pathways from the cochlea in the ear to the auditory cortcx CNC = cochlear nucleus; IC = infcrior colliculus; MGB = medial geniculate body; PAC = primary auditory cortex.
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F'IGURE 3 Normative data for dichotic listening performance in right- and left-handers. 8 L E = percentage left ear comect recall %RE = percent right ear correct recall. Each dot represents one Subject. Small numbers in the scatter-gram = two or more subjects occupy the same coordinates.
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K . HUGDAHL AND K . WESTER
priming or attending to certain stimuli (Kinsbourne, 1970). Kinsbourne holds the view that behavioral asymmetries reflect covert shifts of attention to the side of the more activated hemisphere for a particular kind of tasks or stimuli. This activity then “spills over” to motor centers which control activity in the contralateral side (see also Kinsbourne, 1973). Furthermore, Bradshaw and Nettleton (1988) have argued that neither the traditional dichotic paradigm nor references to the anatomy and physiology of the auditory system are necessary to generate an ear advantage. The spatial location of a sound source may be as determinant as the projection pathways from the ear to the cortex in determining an ear advantage in DL. Thus, there are two major explanatory models for the REA effect in dichotic listening, one that refers to the anatomy and physiology of the auditory system, the other that refers to attentional and other cognitive influences. The most frequently used method of validating dichotic listening performance to brain function is the administration of sodium amytal to the left or right hemisphere, and to record how speech function is suppressed when sodium amytal is injected into one hemisphere at a time. Although this probably is the most reliable method to observe brain asymmetry for language, the sodium amytal technique mainly assesses expressive speech function, while DL additionally picks up functions related to language reception. Another way of looking at a structural versus attentional explanation for the REA is to study patients with unilateral lesions restricted to one hemisphere. Several studies have reported a lesion effect such that unilateral damage to areas involving auditory pathways may lead to reduced frequency of correctly reported items from the contralateral ear (e.g. Sparks, Goodglass and Nickel, 1970). Furthermore, Roberts, Varney, Paulsen, and Richardson (1990) showed that patients with complex partial seizures improved their dichotic listening performance after anticonvulsant medication. This is what may be expected from a structural explanation for the REA effect. However, from the point of view of an attentional explanation, unilateral left temporal lobe damage should not necessarily lead to a drastic reduction in the contralateral right ear report, the decrease may as well be manifested in a reduction of correct reports from the ipsilateral ear (cf. Hugdahl, Wester, and Asbjomsen, 1990b). In the present paper we report four cases of unilateral brain lesions who were the subjects for neurosurgery. All patients were between 18 and 28 years, and were referred to the neurosurgery unit because of tumors or cysts in the left temporal lobe (2 cases); hemorrhage from the left middle cerebral artery (1 case), and severe destruction of the left hemisphere in a traffic accident (1 case). Three of the patients were right-handers, one was a left-hander (see details about each patient below). The Dichotic Test
In addition to the dichotic test, the patient’s hearing was tested by a standard audiometer screening technique in order to assess hearing capacity within the critical 500-6000 Hz region for dichotic stimuli. The dichotic stimulus-materials consisted of the six stop-consonants /b/, /d/, /g/, /p/, /t/, /k/ which were paired with the vowel /a/ to form six basic consonant-vowel (CV) syllables (/ba/, /ga/, /pa/, etc.). The syllables were paired with each other for all possible combinations, thus yielding 36 pairs including the homonymic pairs (the homonyms were used as test trials and excluded from statistical analysis). Each pair was randomly recorded three times on the tape. Thus, the total number of trials on the tape was 108. The intertrial interval (ITI) between stimulus presentations varied between 4 and 5 s. The dichotic tape was prepared on a
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PDP 11/45 computer. Each CV-syllable had a duration of 320 ms., and temporal alignment between channels was set at the first visible energy-release in the conqo-ant segment of each syllable. Maximum onset difference between the channels was 0.5 ms. due to D / k multiplexer resolution and the sampling frequency (10 KHz). Each syllable was originally read by a male voice and fed to the computer. After computer analysis, the syllables were recorded onto a NAGRA IV tape recorder. In order more easily to test the patients in the hospital environment the NAGRA tape was copied onto a chrome dioxide cassette and played from a SONY WM DD I1 minicassette player with “plug-in”-type earphones. The output of the minicassette player was calibrated and the mean intensity was 84 db SPL measured by a Bruel and Kjaer 2204 sound level meter. The patients had to answer with the syllable they heard on each trial. The answer was marked by the experimenter on a specially designed scoring-sheet. A short pause was put in after every list of 36 dichotic presentations in order to give the patient some rest (and in some of the patients to give new instructions). Two of the patients reported below also had to go through two forced-attention conditions (see Hugdahl and Anderson, 1986) in which attention was focused on either the right or left ear input. In the “nonforced” attentional condition, the patient was instructed to report the syllable he/she identified best. Thus, no specific instruction concerning allocation of attention was given. In the “forced-right’’ condition, the patient was told to attend only to the right ear and to report only from that ear. In the “forced-left” condition, he/she was told to focus attention on the left ear input and report only from that ear. Order of presentation of the three conditions was randomized across test-sessions. The audiometer screening tests for hearing acuity included presentations of tones between 500 and 6000 Hz (which includes most of the energy in the CV-syllable). Threshold differences between the ears were not allowed to exceed 10 db at any frequency. CASE REPORTS Case # I The first case study was aimed at elucidating the structural versus attentional explanations for ear advantage effects in DL. Sparks and Geschwind (1968) showed that the left ear signal in DL was almost extinct in a patient with callosotomy. They attributed this finding to the fact that the left ear signal, reaching only the right hemisphere through the contralateral pathways, could not be transmitted to the left hemisphere for processing because of sectioning of the corpus callosum. Thus, the Sparks and Geschwind (1968) finding provides support for a structural explanation. One way to follow-up and to test the structural model further would be to show that a patient with a right hemisphere language dominance, and with a left hemisphere lesion (or disrupted callosal transmission) would reveal a right ear extinction effect. Furthermore, if the patient did not increase right ear correct reports when focusing attention to only the right or left ear, an attentional explanation for the ear advantage effect in DL would be even less likely. The patient was a young left-handed female (tested with the handedness questionnaire developed by Raczkowski, Kalat and Nebes, 1974) who had suffered a severe head injury in a traffic accident a few years before. She had virtually no remaining left hemisphere tissue. Since she did not show any signs of speech or language disturbance despite a nonexistent left hemisphere, she had to be using the
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K. HUGDAHL AND K. WESTER
right hemisphere for language. It was therefore predicted that she should demonstrate a drastic reduction in right ear performance in the DL test (contralateral to the damaged left hemisphere), while left ear performance should remain intact. From a structural explanation, there should furthermore be no major changes in performance when instructed to attend to either side. An attentional explanation would, however, mean that although the contralateral right ear signal would be blocked because of tissue loss in the left hemisphere, the ipsilateral pathway would be intact, with the result that attending to the right ear should drastically increase right ear performance. Figure 4 shows a computer tomography (CT) scan revealing the substantial tissue loss in the left hemisphere. The patient had normal hearing thresholds for both ears when tested with screening audiometry before the dichotic tests. She was tested about four years after her initial trauma, and under all three attentional instructions. The dichotic listening results are seen in Figure 5; her right ear scores were zero, or close to zero for all three attentional conditions, while her left ear scores were between 67% correct to 87% correct (which is within the normal range). There are two arguments for the view that she was right hemisphere dominant for language before the accident; 1) she was a left-hander, with an increased probability of right hemisphere language dominance (Fennell, 1986), and 2) her language functions were intact after near-complete destruction of the left hemisphere. The present data thus favor a structural rather than an attentional explanation. The absence of any correct reports from the right ear in the DL situation (despite normal hearing) must be attributed to the fact that the contralateral right ear signal is blocked from further transmission after reaching the (remaining) left temporal areas. Attending to either ear did not affect the right ear scores. The number of correctly reported items were zero in both the forced-attention conditions (see Figure 5 ) . It is therefore unlikely that an attentional model, which attributes the ear advantage to a biased priming effect of attending to a particular ear of input, can explain dichotic listening performance. Case # 1 has revealed a paradoxical right ear extinction effect in a left-hander with an almost nonexisting left hemisphere. This is a new finding, since previously only left ear paradoxical effects have been reported in the literature after unilateral hemisphere lesions. Case #2
The second case was a young right-handed male who underwent craniotomy because of an intracerebral, spheric tumor in the left central region above the Sylvian fissure. The location and extent of the tumor is seen in Figure 6 which shows a magnetic resonance image (MRI) of the location and extent of the tumor. The tumor was radically removed during craniotomy, and a control MRI one month after surgery showed no signs of residual tumor. The patient did not show any overt signs of language disturbance in the neurological examination after being admitted to the hospital. However, since the tumor was located in the left Sylvian fissure affecting the language receptive areas, he was admitted to dichotic listening testing. It was hypothesized that one effect of the tumor would be an increased intracerebral pressure on the surrounding tissue, possibly affecting the processing of the contralateral right ear signal. If this was true, it could be predicted that the patient should reveal a lejl ear advantage (LEA) when tested before the operation, but a right ear advantage (REA) when tested after the operation. Since the patient was consistently right-handed when tested with the hand-
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DICHOTIC LISTENING AND BRAIN DAMAGE 23
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FIGURE 5 Mean percentage correct reports from the left (LEar) and right (REar) ears in dichotic listening in Patient # 1 during three different attentional instructions. See text for further explanations.
edness questionnaire (Raczkowski, et al. 1974) he would most likely also be left hemisphere dominant for language (Bryden, 1988). Thus, a shift from a LEA to a REA after the removal of the tumor would further strengthen a structural explanation of the ear advantage in DL, and also validate the DL procedure. The patient was tested with dichotic listening the day before surgery, two days after surgery, four days after surgery, and five weeks after surgery. For clinical reasons he was only tested with the nonforced attentional instruction. Hearing was normal when tested with audiometer screening. The DL results for percentage correctly reported items from the right and left ear during the four test occasions are seen in Figure 7. As can be seen in Figure 7, the patient had a slight overall reduction in correctly reported items compared to the normative data (see above, and Figure 3). However, more important, he showed a leji ear advantage on the day before surgery that shifted to a right ear advantage almost immediately after the removal of the tumor. Second, the right ear advantage stayed stabile at both the immediate and long-term followup tests (see Figure 7). It is further interesting to note that the magnitude of the REA at the five weeks follow-up test was clearly in the normal region (in the order of 20%). The slight difference in the magnitude of the REA from the first to second postoperative test was probably due to the edema caused by the operation. To sum up, Case #2 has shown an example of how displacement of brain tissue in the left
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FIGURE 6 MRI scan showing the location of a tumor above the left Sylvian fissure in Patient #2. Note that the left side of the brain is shown to the right in the scan according to radiological standards.
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FIGURE 7 Mean percentage correct reports from the left and right ears in dichotic listening in Patient #2. Pre-op = The day before operation; Post-opI = Two days after the operation; Post-opII = four days after the operation; Post-opIII = five weeks after the operation.
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FIGURE 8 Mean percentage correct reports from the left (LEar) and right (REar) in dichotic listening in Patient #3 during the three attentional instructions (see text for further details).
hemisphere that is involved in language processing also disrupts the contralateral right ear signal in dichotic listening, resulting in a left ear advantage (in an otherwise left hemisphere language dominant person). Removal of the pressure-inducing force in the critical areas in the temporal lobe has the consequence of an almost immediate shift back to a normal right ear advantage which then persists, and grows stronger as the patient recovers from the operation. Thus, DL seems to monitor closely hemisphere language function on a neuroanatomical basis. Case #3
The third patient had a subarachnoid hemorrhage involving an aneurysm of the left middle cerebral artery. He had a manifest motor aphasia when admitted to hospital, which gradually improved during the next three weeks. He was treated conservatively for the hemorrhage with bedrest for three weeks at the hospital. He was tested with dichotic listening the first time two days before he was released from the hospital, i.e., about three weeks after acute illness. He was later retested 3.5 months after the first DL test. The results from the DL tests are seen in Figure 8; patient #3 showed a reduction in correct right ear reports (down to the order of 10%). This was furthermore independent of attentional instruction. Thus, instructing the patient to attend to the right ear did not affect his right ear scores (see Figure 8). Left ear performance was
DICHOTIC LISTENING AND BRAIN DAMAGE
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in the normal 60-70% region, with a slight decrease during the forced-right condition, and an increase during the forced-left condition. Thus, correctly reported items from the left ear was affected by the attentional conditions (a slight reduction in left ear performance when attending to the opposite right ear, and a marked increase when attending to the “correct” left ear). Right ear performance was however not affected by the attentional instructions. It, therefore, seems that the hemorrhage in language areas in the left hemisphere suppresses processing of the contralateral right ear signal, and this cannot be counteracted by focusing attention to the right ear.
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Case #4
Patient #4 had a slightly expanding arachnoid cyst in the left temporal lobe believed to cause his moderate clinical symptoms (headache). The cyst was drained with a shunt. He did not show any overt signs of language disturbance in the neurological examination. The patient was tested with the standard DL set-up used with the other reported cases, including forced-attention instructions in addition to the free-report instruction. The patient was a right-handed 23-year old male. He was tested the first time the day before the operation, and the second time the day after operation, he was then followed-up in a third test six weeks after the operation. The DL results are seen in Figure 9 (only data from the nonforced attentional condition are reported). As can be seen in Figure 9, the overall level of performance was reduced preoperatively. More importantly, however, there was no significant REA preoperatively. This is probably explained as a result of the increased force on brain tissue in the temporal lobe critically involved in auditory processing. Since the dichotic listening situation means that the contralateral right ear signal normally should have better access to the left temporal areas, absence of the REA indicates in this case that the right ear signal is suppressed because of displacement of tissue in this region of the brain. Looking at the results from the two postoperation tests in Figure 9 (middle and right hand panels), the REA appears immediately the day after operation, and it is still present at the six weeks follow-up test (right hand panel in Figure 9). Another important aspect of the data in Figure 9 is that not only does the REA appears on the day after the operation, but overall right ear performance also increases into the normal range. The magnitude of the REA is also within the normal range seen in young adult males (about 20%). A final aspect of the results is that the REA during the two postoperation tests are caused by an increase in right ear performance (see Figure 9). Since right ear performance in DL is both anatomically (Kimura, 1967; Eslinger and Damasio, 1988), and physiologically (Strauss, 1988) linked to left temporal lobe functioning, it is difficult to escape the conclusion that DL is a sensitive index of functional brain recovery (cf. Hugdahl, et al., 1990b). Summary and Conclusions
In the present report we have presented dichotic listening data from four case-studies with various lesions in the left hemisphere. In two of the right-handed cases, there was a marked reduction in contralateral right ear performance before surgical treatment. This behavioral deficit was drastically improved immediately after surgery, indicating both a structural and functional relationship between contralateral ear performance and left hemisphere language function.
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Case # 4
go
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FIGURE 9 Mean percentage correct reports from the left (LEar) and right (REar) ears in dichotic listening in Patient #4. Pre-op = the day before the operation; post-opI = the day after the operation; Post-opll = six weeks after thc operation.
The lesion-approach to DL provides a new way of validating the dichotic listening technique for the study of brain asymmetry. The results further support a structuralanatomical rather than a functional-attentional explanation of the ear advantage phenomenon seen in dichotic listening. This strengthens the theoretical model of the REA in dichotic performance provided by Kimura (1967). There are clinical and radiological reasons to believe that Patients #2 and 4 had lived with their expanding pathological conditions (tumor and cyst) for many years. The prompt normalization of DL-findings after decompressive surgery in these patients is therefore surprising. It indicates that even brain tissue that has been suppressed for many years due to local pressure, may regain its language functions. It is furthermore possible that the results of the DL-tests may provide information that is relevant for indications for operation. This is especially relevant for patients with mild to moderate overt symptoms from congenital arachnoid cysts.
REFERENCES Berlin, C. I. (1977). Hemispheric asymmetry in auditory tasks. In S . Hamad, R. W. Doty. L. Goldstein, J. Jaynes. & (3. Krauthamer (Eds.). Lorertrlizarion in the n e r w i u sysrern. New York: Academic Press.
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Bradshaw, J. L. & Nettleton, N. C. (1988). Monaural asymmetries. In K. Hugdahl (Ed.). Handbook of dichotic listening: Theory, methods, and research. Chichester, U.K.: Wiley & Sons. Brodal, A. (1981). Neurological anatomy in relation to clinical medicine. (3rd ed.) New York: Oxford University Press. Bryden, M. P. (1967). An evaluation of some models of laterality effects in dichotic listening. Acta Oto-Laryngologica, 63, 595-435. Bryden, M. P. (1988). An overview of the dichotic listening procedure and its relation to cerebral organization. In K. Hugdahl (Ed.). Handbook of dichotic listening: Theory, methods, and research. Chichester, U.K.: Wiley & Sons. Connolly, J. F. (1 985). Stability of pathway-hemispheric differences in the auditory event-related potential (ERP) to monaural stimulation. Psychophysiology, 22, 87-96. Eslinger, P. J. & Damasio, H. (1988). Anatomical correlates of paradoxic ear extinction. In K. Hugdahl (Ed.). Handbook of dichotic listening: Theory, methods, and research. Chichester, U . K . : Wiley & Sons. Fennel]. E. B. (1986). Handedness in neuropsychological research. In J. Hannay (Ed.). Experimental techniques in human neuropsychology . New York: Oxford University Press. Hugdahl, K. (1988). Handbook of dichotic listening: Theory, methods, research. Chichester, U.K.: Wiley & Sons. Hugdahl, K. & Andersson, L. (1986). The “forced-attention paradigm” in dichotic listening to CVsyllables: A comparison between adults and children. Cortex. 22, 417-432. Hugdahl, K., Wester, K., & Asbjarnsen, A. (1990a). The role of the left and right thalamus in language asymmetry: Evidence from Parkinson patients undergoing stereotactic thalamotomy . Brain and Language, 39, 1-13. Hugdahl, K., Wester, K., & Asbjarnsen, A. (1990b). Dichotic listening in an aphasic male patient after a subcortical hemorrhage in the left fronto-parietal region. International Journal of Neuroscience, 54, 139-146. Kimura, D. (1961). Some effects of temporal lobe damage on auditory perception. Canadian Journal Of PSyChOlOgy, 15, 156-165. Kimura, D. (1967). Functional asymmetry of the brain in dichotic listening. Cortex, 3 , 163-168. Kinsbourne, M. (1970). The cerebral basis of lateral asymmetries. Acta Psychologica, 33, 193-201. Maximilian, V. A. (1982). Cortical blood flow asymmetry during monaural verbal stimulation. Brain and Language, 15, 1-11. Nebes, R. D. & Nashold, B. S. (1980). A comparison of dichotic and visuo-acoustic competition in hemispherectomized patients. Brain and Language, 9, 246-254. Raczkowski, D., Kalat, J . W., & Nebes, R. D. (1974). Reliability and validity of some handedness questionnaire items. Neuropsychologia, 12, 43-47. Roberts, R. J., Varney, N. R., Paulsen, J. S., & Richardson, E. D. (1990). Dichotic listening and complex partial seizures. Journal of Clinical and Experimental Neuropsychology, 12, 448-458. Rogers, R. L., Papanicolaou, A. C., Baumann, S. B., Eisenberg, H. M., & Saydjari, C. (1990). Spatially distributed cortical excitation patterns of auditory processing during contralateral and ipsilateral stimulation. Journal of Cognitive Neuroscience, 2, 44-50. Rosenzweig, M. R. (1951). Representations of the two ears at the auditory cortex. American Journal O f Physiology, 167. 147-214. Sparks, R. & Geschwind, N. (1968). Dichotic listening in man after section of neocortical commissures. Cortex. 4 , 3-16. Sparks, R., Goodglass, H., & Nickel, B. (1970). Ipsilateral versus contralateral extinction in dichotic listening resulting from hemispheric lesions. Cortex. 6, 249-260. Springer, S. P. (1986). Dichotic listening. In J. Hannay (Ed.). Experimental techniques in human neuropsychology. New York: Oxford University Press (pp. 138-166). Strauss, E. (1988). Dichotic listening and sodium amytal: Functional and morphological aspects of hemispheric asymmetry. In K. Hugdahl (Ed.). Handbook of dichotic listening: Theory, methods, and research. Chichester, U.K.: Wiley & Sons (pp. 117-138). Studdert-Kennedy, M. & Shankweiler, D. (1970). Hemispheric specialization for speech perception. Journal of the Acoustical Sociely of America, 48, 415-420. Witelson, S. F. (1983). Bumps on the brain: Right-left asymmetry as a key to functional lateralization. In S. J. Segalowitz (Ed.). Language functions and brain organization. New York: Academic Press.
