Auditory laterality and attentional deficits after thalamic haemorrhage

J Neurol (2001) 248 : 676–683 © Steinkopff Verlag 2001 Knut Wester Dexter R. F. Irvine Kenneth Hugdahl Received: 27 October 2000 Received in revised form: 23 January 2001 Accepted: 19 February 2001 K. Wester (쾷) Department of Neurosurgery Haukeland University Hospital 5021 Bergen, Norway. Tel.: +47-55 97-50 00 Fax: +47-55 97-56 99 e-mail: knut.gustav.wester@haukeland.no D. R. F. Irvine Department of Psychology Monash University Victoria 3800, Australia K. Hugdahl Department of Biological and Medical Psychology University of Bergen Årstadvn 21 5009 Bergen, Norway The present research was financially supported by a grant to Knut Wester and Kenneth Hugdahl from the Norwegian Research Council – Medical Research Division. ORIGINAL COMMUNICATION Auditory laterality and attentional deficits after thalamic haemorrhage ■ Abstract Thalamic lesions have been shown to produce severe cognitive deficits involving language and memory. A majority of the studies have reported cognitive deficits after lesions in the anterior and dorsomedial thalamic nuclei. We report five case studies of effects on language processing after postero-dorsal thalamic haemorrhages. Four of the patients had lesions on the right side, and one patient had a lesion on the left side. Effects on language processing were investigated with the dichotic listening test with consonant-vowel syllables. This test, in which conflicting auditory stimuli are presented simultaneously to the two ears, has been used to probe differences in language processing in the left and right hemispheres. The four patients with right-sided lesions reported almost none of the syllables presented to the left ear, and were unable to modify this massive right ear advantage by directing attention to the left or JON 494 Introduction It is well-known that thalamic lesions may cause severe neuropsychological dysfunction [14, 37]. Language and memory disorders are most frequently reported in the literature [1, 8, 10, 20, 24–26, 28, 31–33], but cases of inattention [38], neglect [15], and “thought disorder” [6] have also been reported. While language and verbal right ear. The patient with a leftsided lesion showed a weaker left ear advantage, and was able to modify his responses by shifting attention, to an extent similar to that of healthy reference individuals. When tested with monaural stimulus presentation, the scores of all patients rose to almost 100 % correct for each ear. The pattern of effects with dichotic stimuli under different instructional conditions cannot be accounted for in purely structural terms, and indicates that lesions in the posterior part of the thalamus, including the pulvinar nucleus and medial geniculate body, produce deficits not only in processing of complex auditory stimuli but also in the allocation of attention to input from one ear or the other. ■ Key words Attentional deficit · Auditory pathways · Dichotic listening · Thalamic haemorrhage · Verbal perception memory deficits are commonly found after left-sided lesions, disorders of non-verbal memory are typically found after right-sided lesions (e. g. Stuss et al. [37]; see also Ojemann [29, 30] using electrical stimulation of thalamic nuclei). Thus, it is commonly believed that thalamic nuclei are functionally organized in a way like that of the left and right cortex (cf. Crosson [9]). Many studies have reported cognitive deficits after lesions in anterior and dorsomedial thalamic nuclei (see 677 Stuss et al. [37]), while fewer studies have reported cognitive deficits after lesions affecting the posterior, particularly the postero-dorsal, region of the thalamus, including the medial geniculate body (cf. Peru & Fabbro [33]; see also Fabbro & Paradis [11]). In a previous case study [19], we reported on a surprising “neglect” effect in a young male patient with a small circumscribed lesion in the right pulvinar region, which is part of the postero-dorsal thalamus. When exposed to different acoustic stimuli, simultaneously presented in the two ears (“dichotic listening”), he failed almost completely to report consonant-vowel syllables presented to the left ear, while his right ear performance was much better than normally found in intact individuals in the same situation (cf. Hugdahl 1995 [18]). Moreover, he was unable to modify this pronounced right ear advantage (REA) when specifically instructed to attend to the left or right ear. His hearing was normal when tested with standard screening audiometry, and when tested monaurally, his left ear scores rose to above 80 % correct. We labelled this particular effect as due to “auditory hemispatial extinction” and suggested that the pulvinar nucleus may play a critical role in gating or tuning auditory input to the cortex (cf. Bhatnagar et al. [3]). The aim of the present study was therefore to expand on the original findings of the previous case study. We report dichotic listening performance to consonantvowel (CV)-syllables in five patients with circumscribed lesions involving the same dorsal posterior thalamic region, including portions of the pulvinar and medial geniculate nuclei. Four of the patients had a right-sided haemorrhage, while the fifth had a similar lesion on the left side. The data are reported as five case studies, and compared with dichotic listening performance in five healthy intact individuals within the same age range as the patients, matched for handedness and gender. Case 1 The patient was a 13-year-old boy who was admitted to the hospital after having experienced an acute right-sided headache.After a while, he felt a numbness in the left side of the body and face, without a motor deficit. Immediate CT showed a haemorrhage in the right posterodorsal thalamus with a diameter of 15–20 mm (Fig. 1). The lesion affected mainly the medial geniculate body as well as the medial and lateral subdivisions of the pulvinar nucleus [36]. Further radiological examination (MRI) failed to disclose any vascular malformations. It was therefore assumed that the bleeding source had been a cavernous haemangioma that was destroyed by the haemorrhage. He was fully awake during the stay in our hospital, and was tested in the dichotic listening test 2 days after the incident. Case 2 The patient was a 70-year-old man who suddenly noticed weakness in his left leg and arm, without losing consciousness. He was admitted to the hospital a few hours later, still with a moderate paresis in his left extremities, and a reduced sensibility in the left side of the face and body. CT showed a haemorrhage involving large portions of the posterior right thalamus, but also extending into more anterior portions of the thalamic complex (Fig. 2). The diameter was ca. 25 mm, and it apparently affected the right internal capsule in addition to the pulvinar and the dorsal thalamic nuclei [36]. His consciousness remained unaffected, and he was tested with dichotic listening 10 days after the incident. Case 3 The patient was a 22-year-old man who was admitted to our hospital 4 years after he sustained a severe head injury in a car accident. Initially, he was unconscious for 10 days, and had a pronounced left hemiparesis that gradually subsided, but was replaced by a severe intentional ataxia in the left arm. He was referred to our department because of this ataxia, and he was later, i. e. after being tested in the di- Patients and methods ■ Patients The patients were five males admitted to the department of neurosurgery with a discrete lesion affecting right (4 patients) or left (1patient) postero-dorsal thalamic regions, including the medial geniculate body. In one patient the lesion was of traumatic origin. In the other four, the lesion was caused by a spontaneous intracerebral haemorrhage. They were all right-handed, as determined from a Norwegian translation of the handedness questionnaire constructed by Raczkowzki et al. [35]. The questionnaire consists of 15 items of manual/pedal activities for which the subject has to indicate hand/foot preference. Four of the patients indicated 15/15 items as preferred with the right hand/foot, and one patient indicated 14/15 items. Three of the patients were tested in an acute stage (2–10 days) after a spontaneous haemorrhage, while two patients were tested in a chronic stage (see below). All the patients gave their informed consent to participate in the study. Fig. 1 Case 1. Axial CT scan showing an acute, discrete haemorrhagic lesion in the right posterodorsal thalamus. 678 medial geniculate body [36]. This patient was the one reported in Hugdahl et al. [19]. Case 4 The patient was a 68-year-old man who, following a physical strain, suddenly noticed a numbness in the left side. Initially, he also had slight ataxia of his left leg and arm, but his consciousness was undisturbed. He was admitted to a local hospital after a few hours, still with a reduced sensibility in the left side of the face and body. CT showed a small haemorrhage in the right postero-dorsal thalamus with a diameter of approximately 10 mm, later confirmed by MRI (Fig. 4). The thalamic lesions seemed to be confined to the pulvinar nucleus and the medial geniculate body [36]. He was transferred to our hospital to investigate possible causes. A vascular malformation was not found. His consciousness remained unaffected, but the numbness in the left side persisted when he was tested with the dichotic listening test 10 days after the incident. Case 5 Fig. 2 Case 2. Axial CT scan showing the maximal extent of an acute haemorrhagic lesion in the right thalamus. The patient was a 23-year-old man who was admitted to our hospital 7 months after he sustained an acute, spontaneous haemorrhage from a small vascular malformation in the pulvinar region of the left thalamus. Fig. 5 shows the MRI appearances shortly after the haemorrhage. The thalamic lesion was confined to the pulvinar nucleus and possibly also the medial geniculate body [36].This patient and his results in the dichotic listening test has previously been reported in Hugdahl and Wester [17] as a case study. In addition to comparing between right- and left-lesions, the patients were also compared with five healthy intact subjects randomly picked from the dichotic listening data pool (n = 692) compiled by Hugdahl [18], matched for age and handedness. ■ Acoustic stimuli and apparatus The dichotic stimuli consisted of the six stop consonants paired with the vowel /a/ to form six consonant-vowel syllables (ba, da, ga, pa, ta, ka). The syllables were paired with each other in all possible combinations, thus giving 36 different syllable pairs. The 36 dichotic pairs were recorded three times on tape with three different randomisations, for each attentional instruction. The tape was played from a Sony Walkman WMDD-II with plug-in type mini headphones. The output from the cassette player was calibrated at a level of 75 dB (A). All subjects were tested for monaural hearing acuity with standard screening audiometry for frequencies between 500 and 6000 Hz in steps of 1000 Hz. ■ Procedure Fig. 3 Case 3. Axial CT scan 4 years after the head injury, showing a discrete area of low attenuation in the right posterodorsal thalamus. chotic listening test, successfully treated with a thalamotomy. CT and MRI showed a small lesion in the right postero-dorsal thalamus (Fig. 3), as well as minor areas of contusion in the right frontal lobe. The thalamic lesions were confined to the pulvinar nucleus and the Four patients were tested bedside in the neurosurgery or neurology department where they had been admitted. The testing situation was made as undisturbed as possible, with the test person sitting beside the patient as the only two persons in the room, and with the cassette player on a small table beside the bed. The fifth patient was tested in an examination room in the neurosurgery department. Each patient was first informed about the dichotic listening procedure, and told that he would hear different “sounds”, like “pa”,“da” etc. He was also shown all six syllables on a sheet of paper, and asked to read them aloud, in order to familiarise him with the sounds. The transducers were put in place and fastened with surgical tape to the ear. Each patient was given a few practice trials before the test proper began. There were three different dichotic listening sessions, with different instructions on how to focus attention. In the first session, the subjects were simply told they would be presented with a list of CV-syllables. Thus no specific instruction regarding attention was 679 Fig. 4 Case 4. Axial and sagittal MRI scans showing an acute, discrete haemorrhagic lesion in the right thalamus, just rostral to the meso-diencephalic junction. same CV-syllables presented to only one ear at a time for 36 randomised presentations. ■ Data scoring and presentation The data were scored as number of correctly reported syllables, from the left and right ears, respectively, excluding the 6 homonymic pairs from the data analysis. The typical finding in healthy individuals is that of more correct syllables being reported from the right ear than from the left ear, i. e. a right ear advantage (REA).An opposite pattern of reports is called a left ear advantage (LEA). In order to facilitate comparisons between different studies, and laboratories, the raw scores were converted to percentage scores in the figures and tables. The data are presented for each patient separately. Results Fig. 5 Case 5. Axial MRI scan 3 weeks after the acute intrathalamic haemorrhage, showing a discrete haemorrhagic lesion in the left pulvinar region. presented. This session is called the Non-Forced (NF) attention condition. The subject’s task was to answer with the syllable he heard on each trial. Thus, the instruction emphasised one response for each trial, even though the subject may have perceived both syllables on some trials. This was done to eliminate the risk of artificial change in ear-advantages due to comparison of double-responses against single response trials. During the Forced-Right (FR) attentional test, the subjects were told to pay close attention to only the right ear syllables, and only to report what they heard in the right ear. During the Forced-Left (FL) attentional test, the subjects were conversely told to pay close attention to the left ear syllables, and only to report what they heard in the left ear. A fourth condition involved monaural listening, with the Fig. 6 shows the number of correctly reported syllables from the right and left ear, respectively, for each patient. As can be seen in Fig. 6, the four patients with lesions in the right thalamus (Case #1–4) showed a marked right ear advantage (REA) for all three attentional conditions. The percentage of correctly reported syllables from the right ear was on the average around 80 %, which is well above the right ear score for the healthy controls (Fig. 7). The corresponding figure for the left ear syllables was abnormally low, around 10 %. Thus, all four patients showed a huge REA of the order of 60–70 %. As can also be seen in Fig. 6, the four patients with right-sided lesions were unable to modify their ear scores as a result of shifting attention to either ear, i. e. the REA remained at the same magnitude for all three attentional conditions. The results for the four patients with lesions in the right thalamus are clearly different from those of the single patient with a left-sided lesion (case 5). As can be 680 Fig. 6 Dichotic listening performance (% correct reports) in the five patients. NF = Non-forced attention, FR = Forced right attention, FL = Forced left attention. seen in Fig. 6 (lower panel), this patient showed a left ear advantage (LEA) during the NF attention condition, which changed to a slight REA during the FR attention condition, and reverted to a large LEA during the FL attention condition. Unlike the patients with right-sided lesions, he was able to use attention to modify his performance. The performance of the patients was compared with the performance of five healthy intact subjects matched for handedness, gender and age (Fig. 7). The healthy subjects showed an expected REA during the NF and FR attention conditions, and a similarly expected LEA during the FL attention condition (see Hugdahl [18] for norms). Comparing the results for the five healthy subjects with the patients revealed that the patients showed more correct reports for the ear ipsilateral to the damaged side (the ipsilesional ear) than with the same side for the reference subjects. This was particularly evident for the four patients with right-sided lesions, who had a REA several times larger than the REA in the reference group, a difference that was significant for the NF and FL 681 Fig. 7 Dichotic listening performance in five healthy intact subjects who were age-, and handedness matched to the five patients. The intact reference subjects were drawn at random from the pool of subjects (n = 692) studied by Hugdahl (1995). conditions when comparing the ear difference between the groups (F(2,14) = 6.035, p < 0.02). A final comparison involved only monaural stimulus presentations, with the left or right transducer removed, but with the same CV-syllables (Figures 6 and 7, far right bars). In this monaural test, all subjects had between 85 and 100 % correct responses from both ears, and there was little difference between the patients and the reference group, or between the patients with lesions in the right or the left thalamus. It is interesting to note the slight ear asymmetry also for the monaural input, favouring the right ear both in the patients and the control individuals. Discussion When presented with conflicting dichotic auditory stimuli, the four patients with right thalamic lesions identified correctly almost all the auditory stimuli presented to the right (ipsilesional) ear, but not those presented to the left (contralesional) ear. However, the patients showed a near-perfect identification from both ears when the stimuli were presented monaurally.Unlike normal individuals, these patients were unable to modify their extreme REA by shifting attention to the left ear when instructed to do so. The results for the single patient with a lesion in the left thalamus were less clear. He also exhibited near-perfect performance with syllables presented monaurally to either ear, but he was clearly able to identify auditory stimuli from both ears when stimulated dichotically. However, he showed a considerably weaker ipsilesional ear advantage than the patients with right thalamic lesions. Unlike the patients with right lesions, but similar to healthy subjects, he was also able to modify his responses by directing attention to one ear or the other. The basic question raised by this pattern of results is whether they reflect lesion-produced changes solely in either attentional or in complex auditory/speech processing mechanisms, or in some combination of the two. If dichotic listening phenomena in general reflect differential allocation of attention to input from one or the other ear when these inputs are different, a simple interpretation of the pattern of effects in healthy righthanded subjects would be that normally (i. e., in the NFattention condition) there is a right-ear bias, in that greater attention is allocated to input from the right ear, but that the relative allocation of attentional resources can be partially modulated (e. g., in response to instructions, as in the FR and FL attention conditions). On this view, the fact that the REA of all four right-lesion patients in the NF condition was substantially (and significantly) greater than that of healthy subjects, and was not affected by instructions to focus attention on either ear, could be interpreted as indicating that the lesion had resulted in a massive reduction in the ability to allocate or shift attentional resources to the left (contralesional) ear. That the patients simply were unable to follow instructions, is not very likely, as all the patients were alert and followed all other instructions well. The observed pattern of effects therefore suggests that the nuclei in the postero-dorsal thalamus affected by the lesions (or the regions to which they project) play a critical role in allowing attention to be differentially allocated between the two ears. Given the known connections between the pulvinar and the parietal lobe [2, 27], it would seem likely that the pulvinar is the relevant structure here, but the possibility that the magnocellular or other divisions of the medial geniculate body might be involved cannot be excluded. This argument cannot, however, be applied so readily to the results for the single patient with a left thalamic lesion.Although the LEA exhibited by this patient could reflect a reduced ability to direct attention to the contralesional (right) ear, this bias was much less extreme than the REA of the right-lesion patients. Contrary to the patients with right thalamic lesions, this patient retained a near-normal ability to modulate the relative allocation of attention to the two ears. Interpretation of this different pattern of effects is, however, qualified by the fact that only one left lesion patient was studied. The difference between the right- and left-lesioned patients could reflect a true laterality difference, and would then imply that the right postero-dorsal thalamus plays a much more important role in the differential allocation of attention to input from the two ears than does the left.However,the difference might also simply be attributable to differences in the extent and/or location of lesions in the right-lesion patients and in the single left-lesion patient. 682 Alternatively, it is possible that the differences between the effects of left and right thalamic lesions might reflect different sensory processing deficits. Traditionally, the REA exhibited by healthy right-handed subjects has been attributed to specialisation of the left hemisphere for the processing of verbal (or, more generally, complex acoustic) stimuli and some form of preferential access of right ear input to the left hemisphere (see, e. g., Geffen and Quinn [12] and Bryden [5] for reviews). The nature of this preferential access remains unclear. Kimura’s [22] original structural model in terms of stronger contralateral projections to the auditory cortex in a given hemisphere and suppression of ipsilateral pathways is not compatible with more recent neurophysiological data (see e. g., Phillips and Gates [34] and Geffen and Quinn [12] for discussion). Auditory cortex in a given hemisphere does, however, contain a stronger excitatory representation of input from the contralateral ear and, as a consequence of binaural interactions, a representation predominantly of contralateral auditory spatial locations (e. g., Brugge and Reale [4]; Clarey et al. [7]). These asymmetries are set up in the brain stem, and thus are also present at the level of the midbrain and thalamus (see e. g., Glendenning et al. [13]; Irvine [21]; Clarey et al. [7]). Furthermore, recent electrophysiological evidence has also indicated an asymmetry in the responses of the MGB to complex acoustic stimuli, including speech sounds, in animals [23]. The pattern of effects exhibited by right- and left-lesion patients in the NF attention condition is basically the same as that seen after temporal lobe lesions in right-handed patients, i. e., right damage leads to a deficit on the left ear, resulting in an exaggerated REA, while left damage leads to a deficit on the right ear, which yields an overall LEA (see Bryden [5] for review). However, while a purely structural model could account for the difference between right- and left-lesion effects in the NF attention condition, a modified structural account incorporating the effects of directed attention would be necessary to account for the modulation of the left-lesion patient’s performance in the forced attention conditions (FR and FL), a modulation that was of similar magnitude to that seen in healthy subjects. Even this modified model does not explain why the REA in the right lesion cases remained unmodulated by attention (i. e., in the FR and FL attention conditions). As with the purely attentional account developed earlier, this difference seems to require the conclusion that right (but not left) postero-dorsal thalamic lesions interfere with the mechanisms that allow attention to be allocated to input from one ear to another. Although our findings relate to the auditory modality, they appear similar to results obtained in the study of visual neglect [16, 27]. 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