Clinical Neurology and Neurosurgery 102 (2000) 156 – 162 www.elsevier.com/locate/clineuro Case report Auditory agnosia restricted to environmental sounds following cortical deafness and generalized auditory agnosia Takayuki Taniwaki a,b,*, Koichi Tagawa a, Fumio Sato a, Kozo Iino a b a Di6ision of Stroke, Department of Internal Medicine, National Fukuoka Higashi Hospital, Chidori 1 -1 -1, Koga, Fukuoka 811 -3113, Japan Department of Clinical Neurophysiology, Neurological Institute, Graduate School of Medical Sciences, Kyushu Uni6ersity 60, 3 -1 -1, Maidashi, Higashi-Ku, Fukuoka 812 -8582, Japan Received 20 January 2102; received in revised form 17 May 2000; accepted 17 May 2000 Abstract We encountered a case of auditory agnosia restricted to environmental sounds, which was associated with the development of bilateral subcortical lesions after suffering a bilateral putaminal hemorrhage. The patient had a history of a putaminal hemorrhage on her left side without any major disability. Three years later, she suffered a putaminal hemorrhage on the other side. The clinical picture started with cortical deafness, then changed to generalized auditory agnosia for verbal and environmental sounds, and finally developed into auditory agnosia confined to the perception of environmental sounds. Her errors in a test of sound recognition were discriminative rather than associative in nature. Neuro-radiological examinations revealed bilateral subcortical lesions involving the fibers from the medial geniculate body to the temporal lobes after bilateral putaminal hemorrhage. This case suggested that the subcortical lesion involving bilateral acoustic radiation could cause either cortical deafness, auditory agnosia of all sounds, or auditory agnosia restricted to environmental sounds. © 1999 Elsevier Science B.V. All rights reserved. Keywords: Auditory agnosia; Cortical deafness; Putaminal hemorrhage; Stroke; Magnetic resonance imaging; Acoustic radiation 1. Introduction Auditory agnosia was originally defined as the selective disorder of recognition in non-verbal sounds and noises, though this term has also been used for patients who had difficulty recognizing all types of sound. Auditory agnosia restricted to non-verbal sounds is a rare condition and we could find only a few such cases in previous literature [1 – 7]. The lesions responsible for auditory agnosia to non-verbal sounds are attributed to cortical lesions including right temporal lobe [1,2,6], left temporal lobe [3] and bilateral insular [7], though only one case was reported to have bilateral subcortical lesions after thalamic hemorrhage [4]. We herein report the second known case of typical auditory agnosia only for environmental sounds. This * Corresponding author. Tel.: +81-92-6425541; fax: + 81-926425545. E-mail address: t – taniwa@neuro.med.kyushu-ac.jp (T. Taniwaki). case is unique in that initially there was generalized cortical deafness which then changed to a generalized auditory agnosia for verbal and nonverbal sounds, and finally developed into auditory agnosia restricted to non-verbal sounds for over one month. No previous case with such unique characteristics has been reported. 2. Case report 2.1. Clinical course A 46-year-old right-handed housewife, with a history of hypertension, suddenly developed right hemiparesis, disturbed consciousness and speech disturbance on March 4, 1992. A computerized tomography (CT) scan disclosed a hematoma in the left putamen. Her symptoms gradually improved, with only mild clumsiness of the right hand remaining and no hearing difficulties or language disturbance. (Neither she nor her family no- 0303-8467/00/$ - see front matter © 1999 Elsevier Science B.V. All rights reserved. PII: S 0 3 0 3 - 8 4 6 7 ( 0 0 ) 0 0 0 9 0 - 1 T. Taniwaki et al. / Clinical Neurology and Neurosurgery 102 (2000) 156–162 ticed hearing difficulties or language disturbance after that). On February 24, 1995, she suddenly developed drowsiness, left hemiparesis, hearing difficulties and dysarthria. She was admitted to a local hospital and a CT brain scan revealed a hyperdense area in the right putamen. After recovering consciousness, left hemiparesis, swallowing difficulties, dysarthria and severe hearing loss remained and she appeared deaf. Two weeks later, she was transferred to our hospital. The patient was a well-nourished woman. General physical examination revealed a normal heart rate and rhythm. Her blood pressure was 129/92 mmHg in both arms. An examination of cranial nerves revealed mild weakness in left facial muscles, severe hearing loss, mild dysphasia and slurred speech. A motor examination revealed moderate weakness in her left limbs. The bilateral tendon reflexes were exaggerated with Babinski response on the left side. A sensory examination revealed mild hypesthesia on both sides. Cerebellar function was normal. Neuropsychologically, the patient was alert, well oriented, attentive and disturbed by her hearing loss. Her speech was moderately slurred but otherwise fluent and grammatically correct. She could not distinguish broad categories of sounds such as speech, music, environmental sounds, however, she could read and write Japanese correctly. Praxis, finger recognition, right-left orientation, calculations, constructional capacity and memory function were all intact. Unilateral spatial neglect and extinction phenomena were absent. On the WAIS-R performed on May 15, her IQ was 80 (verbal), 72 (performance) and 74 (full scale). A brain CT scan on March 13, 1995 revealed a hypodense lesion in the left putamen, which spread to a subcortical lesion of left temporal lobe, and a hyperdense lesion situated in the right putamen, surrounded by a hypodense lesion (Fig. 1). Magnetic resonance imaging (MRI) on May 16, 1995 revealed a linear lesion (hypodense lesion in T1 weighted image and hyperdense lesion 157 in T2 weighted image) from the left putamen to the subcortical lesion of left temporal lobe, apparently involving the fibers from the left medial geniculate body to the left primary auditory cortex (Fig. 2). MRI also revealed a linear lesion (a hypodense lesion on T1 weighted image and hyperdense lesion on T2 weighted image) from the right putamen to the subcortical area of the right temporal lobe, slightly involving auditory fibers. Acoustic radiation seemed to be completely disconnected on the left side, and partially disconnected on the right side. During the clinical course (Table 1), the patient behaved as if she was deaf and showed no response to any kinds of sound or voice from March 10 to April 10 (Stage 1). Thereafter, her hearing loss improved and she could respond to sounds, despite being unable to distinguish speech and environmental sounds from April 11 to April 29 (Stage 2). From April 30 to her discharge on May 30 (Stage 3), she was able to understand speech at normal speed though she still had difficulties in identifying environmental sounds such as footsteps, winds, rainfall, motorcycle. Furthermore, she was afraid of those sounds. After discharge, her ability to recognize environmental sounds gradually improved and she could recognize environmental sounds completely 6 months after the onset. The following investigations were performed at each stage Table 2. 2.2. Neuropsychological assessment Standard pure tone threshold audiometry showed severe bilateral sensorineural hearing loss (55–100 dB at 1000 Hz: Fig. 3A) at the first stage, though it improved in the second (10 dB at 1000 Hz: Fig. 3B) and third stage (0–10 dB at 1000 Hz). The examination of brainstem auditory evoked potentials showed normal wave forms and latencies from wave I to wave V at the first (Fig. 4) and third stage. Fig. 1. Computed tomography of the brain on admission (March 13, 1995) showing two lesions, a hypodense lesion that spread to subcortical lesion of left temporal lobe (arrow head) and a hyperdense lesion suited in the right putamen surrounded by hypodense lesion (arrow). 158 T. Taniwaki et al. / Clinical Neurology and Neurosurgery 102 (2000) 156–162 Fig. 2. MRI image (T2 weighted) on axial section (A) and on coronal section (B) in the stage 3 (May 16, 1995), showing two lesion, a linear lesion from left putamen to subcortical lesion of left temporal lobe, apparently involving the fibers from left medial geniculate body to the left primary auditory cortex (arrow head) and a linear lesion from right putamen to the subcortical area of right temporal lobe, slightly involving auditory fibers (arrow). Acoustic radiation seemed to be completely disconnected on the left side, and to be partially disconnected on the right side. A sound recognition test was conducted using a tape presenting 20 familiar, meaningful non-verbal sounds including the sounds of human voices (man laughing, baby crying, woman singing, the Buddhist scriptures), animal sounds (dog, cat, cow, bird), instrument sounds (piano, telephone, railroad crossing, ambulance car), nature sounds (wind, rain, thunder, water), and various other types of noise (motorcycle, train, saw, steps), requiring the patient to name the sounds (4). The volume of presented stimuli was identical. At the first stage, she could identify no environmental sounds. At stage 2, she could detect only 38% (age matched control; 87.99 13.1; n= 10) of the sounds, and discriminate only 55% (control; 87.89 13.2) at stage 3. She T. Taniwaki et al. / Clinical Neurology and Neurosurgery 102 (2000) 156–162 could easily identify the sounds of human (3/4), animals (4/4) and instruments (3/4), but could hardly detect the sounds of nature (0/4) and noise (1/4) at stage 3. Her errors 159 mainly consisted of names of acoustically similar sounds (e.g. for the sound of thunder or sawing, ‘sound of noise’; for water, ‘crying’, for people laughing, ‘music’). Table 1 Clinical course Stage 1 (Mar 10–Apr 10) Stage 2 (Apr 11–Apr 29) Stage 3 (Apr 30–May 30) Clinical features Deaf Clinical condition Pure tone threshold (1000 Hz) Environmental sounds Auditory comprehension Reading comprehension Cortical deafness R 55 dB Respond to sound, but cannot distinguish speech and sounds Generalized auditory agnosia Understands but cannot distinguish speech environmental sounds Auditory agnosia to environmental sounds 0 dB 0 dB 10 dB 6/16 (37.5%) 10 dB 11/20 (55%) 20–70% 90–100% 90% 100% 67% 100% 56% 100% 74% 95% Normal Vowel identification Phonemic discrimination Token Test BAEPsa a L 100 dB Normal BAEPs, brainstem auditory evoked potentials. Table 2 Recognition of environmental sounds No. 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15. 16. 17. 18. 19. 20. a Stimulus Railroad crossing Dog Baby crying Telephone Water Motorcycle Footsteps People laughing Thunder Cow Piano Cat Train Sawing Buddhist Scriptures Woman singing Wind Ambulance car Bird Rain No. of correct answers Control No response; N.D., not determined. (Category) (Instrument) (Animal) (Human Voice) (Instrument) (Nature) (Noise) (Noise) (Human Voice) (Nature) (Animal) (Instrument) (Animal) (Noise) (Noise) (Human Voice) (Human Voice) (Nature) (Instrument) (Animal) (Nature) 6/16 (37.5%) Response Stage 2 Stage 3 N.D. Dog Baby crying Telephone Crying N.D.a N.D. Baby talk Noise — — Cat Train Bird singing Buddhist Scriptures N.D. — — — — 11/20 (55%) 87.9 9 13.2% Railroad crossing Dog Baby crying Telephone —a — — Music Wind Cow — Cat Train Noise Buddhist Scriptures Woman singing Rain Ambulance car Bird — — 87.8913.2% 160 T. Taniwaki et al. / Clinical Neurology and Neurosurgery 102 (2000) 156–162 The following studies were performed according to the methods as previously reported [9]. All the tests were conducted with a native female Japanese voice at natural speed. In the tests of vowel identification, the patient was required to distinguish between long vowel’s /a/, /e/, /i/, /o/, /u/. She could not identify anything at stage 1. However, she could recognize 67% at stage 2 and 100% at stage 3. In the experiments of phonemic discrimination (stop consonant-vowel discrimination), all the items were combinations of a consonant and the vowel /a/. The initial stop consonants differed according to the place of articulation (labial/b, p/, alveolar/d, t/, or velar/g, k/) or voicing (voiced/b, d, g/, voiceless/p, t, k/). She responded correctly for 56% at stage 2, and 97.5% at stage 3. Her score on the Token test was 74% for oral commands and 98% for written commands at stage 2. At stage 3, her score improved to 95% correct even for oral commands. 3. Discussion In the present case, that of a patient who suffered a bilateral putaminal hemorrhage, pure tone threshold audiometry showed severe bilateral sensorineural hearing loss, though brainstem auditory evoked potentials disclosed normal waveform and latencies from I to V at stage 1. At stage 2, pure tone threshold audiometry revealed that hearing improved sufficiently enough to detect sounds, while the recognition of both verbal and non-verbal sounds remained impaired. At stage 3, recognition for verbal sounds improved in SLTA and on the Token test, while that for non-verbal sounds was still impaired. Although the chance of corrected sound Fig. 3. Pure tone threshold audiometry. (A) Stage 1 (March 20, 1995); (B) stage 2 (April 17, 1995). x=left ear, o= right ear, HL= hearing level. The results of the Standard Language Test for Aphasia [8] are summarized in Table 3. At stage 2, difficulties in language comprehension were observed (word comprehension 70% correct, cut off 100%; sentence comprehension 40% correct, cut off 88%; command comprehension 20%, cut off 90%), although reading comprehension was normal (reading comprehension 90% correct; cut off 90%). At the stage 3, language comprehension improved to normal (word comprehension 100% correct, cut off 100%; sentence comprehension 100% correct, cut off 88%; command comprehension 90%, cut off 90%). Fig. 4. Brainstem auditory evoked potentials at stage 1 (April 2, 1995). Recordings are from Cz to the A1 and A2; 2048 signals were averaged. Waves I – V were intact. T. Taniwaki et al. / Clinical Neurology and Neurosurgery 102 (2000) 156–162 161 Table 3 Results for the standard language test of aphasia (SLTA) Subtest Auditory comprehension Word Sentence Command Speech Confrontation naming Explanation of the action in a picture Explanation of a cartoon Repetition Word Sentence Reading aloud (Sentence, word (Kanji, Kana)) Reading comprehension (Sentence, word written command) (Kanji, Kana), Spontaneous writing With a picture presented (Kanji, Kana) Explanation of a cartoon Dictation Word (Kanji, Kana) Sentence interpretation was corrected in the agnosia test, the value of correction was less than the mean minus 2SD, suggesting that recognition of non-verbal sounds was significantly impaired. It is therefore considered that the present case showed cortical deafness at stage 1, auditory agnosia for verbal and non-verbal sounds at stage 2, and auditory agnosia restricted to non-verbal sounds at stage 3 due to bilateral subcortical lesions after putaminal hemorrhage. To our knowledge, only 3 cases of generalized auditory agnosia have been linked to a subcortical lesion [4,10,11], and only one case changed to auditory agnosia related to environmental sounds [4]. Our present case thus shows aberration which suggests that the subcortical lesions involving bilateral acoustic radiation may cause either cortical deafness, auditory agnosia of all sound, or auditory agnosia restricted to non-verbal sounds. There are two types of auditory agnosia restricted to non-verbal sounds, an impairment in discriminating the acoustic structure of the stimulus, and an inability to associate a well-perceived acoustic pattern with its meaning [12]. Spinnler and Vignolo [13] suggest that acoustic errors reflect a discriminative disorder, and semantic errors an associative disorder. Our patient could not discriminate between acoustically similar sounds, suggesting that her sound recognition disorder was ‘discriminative’ rather than ‘associative’ in nature. Recent neuroimage studies revealed that both the primary auditory cortex and the auditory association cortex are needed to integrate environmental sounds, Score (% of correct) Cut off Stage 2 Stage 3 70 40 20 100 100 90 100 88 90 90 90 100 100 100 100 93 95 85 100 100 100 100 95 92 100 100 95 90 100 90 70 60 100 100 70 60 80 40 100 80 74 50 with a significant rightward asymmetry [14,15]. On the other hand, the auditory association cortex appears important for comprehending speech [16,17]. An animal study showed that the projection fiber from the geniculate body to the primary auditory cortex was separated from that of the auditory association cortex [18]. On the basis of these studies, we speculate that the cortical deafness of our present case at stage 1 was caused by the complete disconnection of the bilateral acoustic radiation, that stretches from the medial geniculate body to the auditory areas including the primary auditory cortex and the auditory association cortex. The MRI findings and the recovery of audiometry at stage 2, suggest that acoustic radiation on the left side was completely disconnected after the first stroke, and that partial disconnection of right acoustic radiation and decreased function, due to the brain edema, caused a complete disconnection of right acoustic radiation. At stage 2, the right acoustic radiation recovered slightly. A partial disconnection from the medial geniculate body to the primary auditory cortex and auditory association cortex might have caused the generalized auditory agnosia at stage 2 in our present case. At stage 3, right acoustic radiation might have improved, and the disconnection from the medial geniculate body to the auditory association cortex recovered. In addition, the disconnection of the fibers from the medial geniculate body to the primary auditory cortex might also have remained, thus inducing the restricted auditory agnosia for nonverbal sounds at stage 3 in our case. 162 T. Taniwaki et al. / Clinical Neurology and Neurosurgery 102 (2000) 156–162 Acknowledgements We would like to thank Brian T. Quinn and ICA company for comments on the manuscript. References [1] Wortis SB, Pfeffer AZ. Unilateral auditory-spatial agnosia. J Nerv Mental Dis 1948;108:181–6. [2] Spreen O, Benton AL, Fincham RW. Auditory agnosia without aphasia. Arch Neurol 1965;13:84–92. [3] Albert ML, Sparks R, von Stockert T, Sax D. A case study of auditory agnosia: linguistic and non-linguistic processing. Cortex 1972;8:427 – 43. [4] Motomura N, Yamadori A, Mori E, Tamaru F. Auditory agnosia; analysis of a case with bilateral subcortical lesions. Brain 1986;109:379 –91. [5] Lambert J, Eustache F, Lechevalier B, Rossa Y, Viader F. Auditory agnosia with relative sparing of speech perception. Cortex 1989;25:71 – 82. [6] Fujii T, Fukatsu R, Watabe S, et al. Auditory sound agnosia without aphasia following a right temporal lobe lesion. Cortex 1990;26:263 – 8. [7] Habib M, Daquin G, Milandre L, et al. Mutism and auditory agnosia due to bilateral insular damage – role of the insular in human communication. Neuropsychologia 1995;33:327 – 39. [8] Tanaka K. Standard language test of aphasia (SLTA): detailed description of construction of aphasia test in Japanese. Adv Neurol Sci (in Japanese) 1977;21:1002–13. . [9] Auerbach SH, Allard T, Naeser M, Alexander MP, Albert ML. Pure word deafness: analysis of a case with bilateral lesions and a defect at the prephonemic level. Brain 1982;105:271 – 300. [10] Kazui S, Naritomi H, Sawada T, Inoue N, Okuda J. Subcortical auditory agnosia. Brain Language 1990;38:476 – 87. [11] Godefroy O, Leys D, Furby A, et al. Psychoacoustical deficits related to bilateral subcortical hemorrhages. A case with apperceptive auditory agnosia. Cortex 1995;31:149 – 59. [12] Vingolo LA. Auditory agnosia. Philos Trans Royal Soc London B 1982;29:847 – 9. [13] Spinnler H, Vignolo L. Impaired recognition of meaningful sounds in aphasia. Cortex 1966;2:337 – 48. [14] Engelien A, Silbersweig D, Stern E, Huber W, Doring W, Frith C, Frackowiak RSJ. The functional anatomy of recovery from auditory agnosia. A PET study of sound categorization in a neurological patient and normal controls. Brain 1995;118:1395 – 409. [15] Tzourio N, Massioui FE, Crivello F, Joliot M, Renault B, Mazoyer B. Functional anatomy of human auditory attention studied with PET. Neuroimage 1997;5:63 – 77. [16] Kojima H, Hirano S, Shoji K, et al. The role of the temporal coding system in the auditory cortex on speech recognition. Neuroreport 1997;8:2395 – 8. [17] Muller RA, Rothermel RD, Behen ME, Muzik O, Mangner TJ, Chugani HT. Receptive and expressive language activations for sentences: a PET study. Neuroreport 1997;8:3767–70. [18] Mesulam MM, Pandya DN. The projections of the medial geniculate complex within the sylvian fissure of the rhesus monkey. Brain Res 1973;60:315 – 33.