Acta psychiatr. scand. 1986:74:178-182 Key words: auditory hallucinations; organic brain symptoms; lateralization phenomenon; superior temporal gyrus; Wernicke’s aphasia; hemorrhagic infarction. Lateralization phenomenon of complex auditory hallucinations H. Tanabe, T. Sawada, H. Asai, J. Okuda and J. Shiraishi Faculty of Health and Sport Sciences, Depts. of Neuropsychiatry and Otorhinolaryngology, Osaka University, and Cerebrovascular Division, Dept. of Internal Medicine, National Cardiovascular Center, Osaka, Japan ABSTRACT - A case is described of a patient who developed a transient verbal hallucination, lateralized to the right ear, and fluent aphasia after a hemorrhagic infarction in the left superior temporal gyrus. On the basis of this patient and the cases in the literature showing unilateral complex auditory hallucinations, the clinical significance of the lateralization phenomenon of complex auditory hallucinations was investigated. As a result, the lateralization phenomenon of complex auditory hallucinations could be considered a significant clinical sign indicating the existence of a lesion in the superior temporal gyrus opposite the hallucination side. Received December 21, 1985; accepted f o r publication February 15, 1986 Auditory hallucinations, as symptoms of organic brain diseases, are much less frequent than visual hallucinations, and have mostly been reported in patients with temporal lobe tumor or epilepsy. Even if the hemispheric lateralization of the auditory hallucinations has been often discussed, the lateralization phenomenon of these hallucinations, namely, the experience of hearing hallucinations in one ear or from one direction, has hardly been mentioned. The reports of the lateralization phenomenon of auditory hallucinations are very few in comparison with those of visual hallucinations. However, we have found a few cases presenting the lateralization phenomenon of complex (verbal or musical) hallucinations in a series of patients (1, 2). The clinical significance of this phenomenon has been referred to briefly by Hecaen & Ropert (1) and Bergman (3). Bergman noted that this phenomenon, which he calls unilateral auditory hallucination, appeared to be a reliable indication of unilateral pathology, with lesion usually on the opposite side. We had the opportunity to examine a patient who developed a transient verbal hallucination lateralized to the right ear, and fluent aphasia after a hemorrhagic infarction in the left superior temporal gyrus. The purpose of this paper is to investigate anew the clinical significance of the lateralization phenomenon of complex auditory hallucinations on the basis of our case and other reported cases. Case report A 64-year-old right-handed woman was examined. She had no prior history of other neurological and psychiatric diseases except for transient global amnesia 7 years ago. On Oct. 10, 1982, she complained of a LATERALIZATION OF AUDITORY HALLUCINATIONS splitting headache after she had been swimming and then carried a heavy bag on her left shoulder. The headache gradually lightened and the following day was concentrated in the temporal region above the left ear. At this time, she suddenly began hearing in her right ear the voice of a female announcer on T.V., and in the background, the noisy voice of her grandson. During the following week the voices were so real that she would turn around to see if someone was actually behind her on the right side and ask her sister if she had said something. She experienced neither auditory illusions, such as changes in quality of sounds heard, nor hallucinations in the other modalities. She did not develop paranoid delusions. She experienced, however, a singular phenomenon which might be considered a kind of auditory illusion as it was an altered interpreta- headache OCt.10.1982. I .... left 11 reglo” “”,lateral audltory hallucination 1verbal.right earl 1 fluent aphasra Oct.20.1982: No”. 1 , 1 9 8 2 : I I I Fig. 1. The clinical course of main symptoms. Fig. 2. EEG. Arrows indicate spike activities in the left temporal region. 179 tion of present experience. She related the experience thus: “While I was talking to someone, I could hear my own spoken words inside my head and, consequently, I could not hear what the other person was saying. On another occasion, the words of another person entered my head and became mixed with my own thoughts, and as a result I got confused.” In addition to these symptoms, she gradually became unable to express what she wanted to say, and was unable to understand immediately what other people were saying. Thus, she was n o longer able to talk to other people. On Oct. 18, her family brought her to us. Although she appeared alert she could only nod, answering “ha ha”, to simple verbal and written questions and requests. Her spontaneous speech was sparse, although she sometimes spoke meaningful sentences such as, “I can do housework. Only my language is a problem.” Her articulation was normal without paraphasia. Two days later, on Oct. 20, she was admitted, and shortly after an injection of contrast medium for CT scan, she felt nausea and her speech became jargon. Afterwards, phonemic and semantic paraphasias were observed, and word-finding difficulty and moderate comprehension disturbance were also confirmed. The symptoms of Wernicke’s aphasia, however, rapidly disappeared, and on Nov. 1 , only mild writing disturbance and some paraphasia were noted. The hallucination and the headache above the left ear, which had continued from the incipient stage, gradually lessened and on about Oct. 28, both disappeared (Fig. 1). The content of the hallucination appeared not to have changed, but she could not recall it precisely. In the course of this illness, she sometimes had a bad dream about being kicked on the right side of her head by her grandson, whose voice had been heard in the verbal hallucination. Routine laboratory findings were normal. Neurological examination revealed no abnormalities. Except for the aphasic symptoms, no apraxic and agnosic signs, including auditory extinction to nonverbal and verbal stimuli (4), were found. On neurological examination performed after Nov. 2, a mild inner-ear hearing loss was present in the left ear, but electrocochleogram and brain stem responses showed no abnormalities. Electroencephalogram, during the illness, showed spike activities and slow waves, predominantly in the left temporal region (Fig. 2), and, after the illness, revealed slow waves confined to the left temporal area (EEG taken 7 years ago was normal). CT scans on Oct. I8 and 20 showed a light low density area, with small high density spots in the left superior temporal gyrus, which was partially enhanced by contrast medium. On Nov. 2, however, this abnormal density area could not be found, and a linear low density area at the lateral edge of the left superior temporal gyrus, and enlargement of 180 H. TANABE ET AL the left sylvian fissure, were noticed (Fig. 3). Left carotid angiograrn disclosed an aneurysm at C3 portion of the left carotid artery. Discussion Semiologically, Hecaen & Ropert (1) divided auditory hallucinations into elementary and complex forms, and further subdivided complex hallucinations into musical and verbal forms. The hallucination of our patient, which consisted of voices of an announcer and a grandson, can be regarded as a verbal form of complex hallucinations. Following the classification of Penfield & Perot ( 2 ) , it may also be regarded as an experiential hallucination, as the content could be considered a re-experiencing of the patient’s past. Our patient could not clearly recollect the content of the hallucination. As pointed out by Hecaen & Ropert ( I ) , this difficulty of recollection might be due to accompanied fluent aphasia. The hallucinations caused by organic brain diseases, gener- ally as an epileptic symptom, have a short duration, but according to our patient, her hallucination appears to have lasted more than 2 weeks (Fig. 1). Referring to the electrocortical stimulation studies of Penfield & Perot (2), the first temporal convolutions, (the stimulation of which produces an experiential hallucination), seem not to be included in the posterior speech area. Thus stimulation of the posterior speech area produces no experiential hallucinations. It is at least clear from the CT scans that the lesion of our patient was situated in the first temporal convolution. Thus, according to the results of Penfield & Perot ( 2 ) , there seems no doubt as to the lesion responsible for her hallucination. Is it possible that the primary or secondary damage to the adjacent posterior speech area produced the transient Wernicke’s aphasia? Does a lesion restricted to the first temporal convolution ever produce Wernicke’s aphasia? The relation between Wernicke’s aphasia and Wernicke’s area Fig. 3. CT scan. A) plain CT on Oct. 18. B) enhanced CT on Oct. 20. C ) plain CT on Nov. 2. White arrows show lesions and black arrow points out the widened left sylvian fissure. LATERALIZATION OF AUDITORY HALLUCINATIONS 181 Table I Reported cases with unilateral complex auditory hallucinations Case Author Content Lateralization Side of lesion F verbal from R-side 23 44 F (case 1) M (case 10) verbal verbal in R-ear in R-ear 23 F (case 14) verbal from R-side 34 M (case 24) musical in L-ear 25 M (case 29) verbal in L-ear L (Cystenbildung im Bereiche der linken Fossa Sylvii) L? (epilepsie a debut crural droit) L (gliome de la partie moyenne de T1 a gauche) L (zone d’aspect inflammatoire a cheval sur le sillon interparietal gauche) R (cicatrix in right parietal and posterior temporal regions due t o a right parietal brain wound) R (AVM in the right fissure of Syl- 46 F (case 45) from R-side vius) L (scarring at tip of left temporal Age Sex Foerster (7) 9 Hecaen & Ropert (1) Penfield & Perot (2) Our patient 64 F + musical verbal verbal has been discussed many times in recent years, but has never been fully elucidated (9,as also the relation between Broca’s aphasia and Broca’s area (6). In this study we have simply presented a patient whose transient verbal hallucination and Wernicke’s aphasia resulted from a hemorrhagic infarction confined to the left first temporal convolution. Table 1 shows reported cases, including our patient, who experienced complex auditory hallucinations lateralized to the right or left ear, or space, i.e. developed unilateral complex auditory hallucinations (3). Only those cases with sufficient data on the content of hallucinations and site of lesion were chosen as subjects of investigation. Hecaen & Ropert (1) considered lateralization of hallucinations as the phenomenon of hearing hallucinations in one of the ears and reported two cases. We followed Bergman’s (3) interpretation of the lateralization phenomenon, thus making a total of three such cases. By examining the cases shown in Table 1, we noted the following: 1) According to the descriptions, all cases spontaneously lateralized their hallucinations to one ear or one side with no question as to localization. 2 ) Although we cannot defi- in R-ear lobe after removal of a meningeal fibroblastoma from lesser wing of left sphenoid bone) L (hemorrhagic infarction in left superior temporal gyrus) nitely conclude that the contents of hallucinations were reproductions of past experiences, they seem to correspond closely to the experiential hallucinations reported by Penfield & Perot ( 2 ) . 3) In all cases, the hallucinations were lateralized to the ear or side opposite the involved hemisphere. 4) Despite Hecaen’s (8) emphasis on the close connection between complex hallucinations and left (dominant) hemispheric lesions, two subjects (Nos. 24 and 29) had right hemispheric lesions. 5 ) Except for one case (No. l), in whom localization of the lesion was not clear, the lesions of the other patients were located around the sylvian fissure and centered on the first temporal convolutions. The last two findings are in accordance with the results of electric stimulation studies by Penfield & Perot (2): “The first temporal convolutions (exclusive of the primary auditory sensory area), when stimulated, give rise to recall of auditory experience with about the same frequency on the two sides. This does not result from stimulation elsewhere.” (p. 688). From the facts described above, we may conclude that the lateralization phenomenon of complex auditory hallucinations could be a significant clinical sign, indicating the existence of a 182 H. TANABE E T AL lesion in the first temporal convolution opposite the side of hallucinations, on condition that the patient spontaneously lateralizes his hallucinations to one ear or to one side. Acknowledgements The authors are indebted to Hiroshi Ohashi, M.D.. a Professor Emeritus ar Kyoto University, for drawing their attention to this problem. References 3 . Bergman P S. Unilateral auditory hallucinations. Trans Am Neurol Assoc 1965:90:226-227. 4. Tanabe H, Nishikawa T, Okuda J, Shiraishi J. Auditory extinction to nonverbal and verbal stimuli. Acta Neurol Scand 1986:73:173-179. 5. Bogen J E, Bogen G M . Wernicke’s region - where is it? Ann NY Acad Sci 1976:28:834-843. 6 . Tanabe H , Obigashi Y . Broca’s area and Broca’s aphasia; based on the observations of two cases with the lesions involving Broca’s area. Brain Nerv (Tokyo) 1982:34:797-804. 7 . Foerster 0. Sensible corticale Felder. In: Bumke et al, eds. Handbuch der Neurologie, Vol. 6 . Berlin: Springer, 1936:358-448. 8. Hecaen H. Introduction a la neuropsychologie. Paris: Larousse, 1972. 1. Hecaen H, Ropert R. Hallucinations auditives au cours de syndromes neurologiques. Ann Med Psycho1 (Paris) 195921 7257-306, 2. Penfield W , Perot P. The brain’s record of auditory and visual experiences; a final summary and discussion. Brain I963 3 6 :595-696. Address Hirotaka Tanabe, M.D. Faculty of Health and Sport Sciences Osaka University 1-1, Machikaneyama-cho, Toyonaka-shi Osaka 560 Japan