GENERALIZED AUDITORY AGNOSIA WITH SPARED MUSIC RECOGNITION IN A LEFT-HANDER. ANALYSIS OF A CASE WITH A RIGHT TEMPORAL STROKE Mario F. Mendez (Departments of Neurology and Psychiatry, University of California at Los Angeles) ABSTRACT After a right temporoparietal stroke, a left-handed man lost the ability to understand speech and environmental sounds but developed greater appreciation for music. The patient had preserved reading and writing but poor verbal comprehension. Slower speech, single syllable words, and minimal written cues greatly facilitated his verbal comprehension. On identifying environmental sounds, he made predominant acoustic errors. Although he failed to name melodies, he could match, describe, and sing them. The patient had normal hearing except for presbyacusis, right-ear dominance for phonemes, and normal discrimination of basic psychoacoustic features and rhythm. Further testing disclosed difficulty distinguishing tone sequences and discriminating two clicks and short-versus-long tones, particularly in the left ear. Together, these findings suggest impairment in a direct route for temporal analysis and auditory word forms in his right hemisphere to Wernicke’s area in his left hemisphere. The findings further suggest a separate and possibly rhythm-based mechanism for music recognition. Key words: auditory agnosia, cortical auditory disorders, amusia, word deafness INTRODUCTION Generalized auditory agnosia, or cortical auditory disorder, is a rare condition usually associated with bilateral temporal lesions (Bauer, 1997). Auditory agnosia refers to an impaired capacity to recognize sounds in the presence of otherwise adequate hearing as measured by standard audiometry. The term has been used broadly to refer to impaired capacity to recognize sounds in general (generalized auditory agnosia) and, in a narrower sense, to a selective deficit in recognizing nonverbal sounds only (selective auditory agnosia). In addition to generalized auditory agnosia, specific lesions can produce other “cortical auditory deficits.” Selective auditory agnosia for meaningful sounds may result from lesions in the right hemisphere, especially the temporoparietal area (Fujii, Fakatsu, Watabe et al., 1990; Nielsen and Sult, 1939; Spreen, Benton and Fincham, 1965; Wortis and Pfeffer, 1948). Isolated verbal agnosia or pure word deafness (PWD) may result from bilateral or from isolated left temporal lesions that presumably disconnect Wernicke’s area (Coslett, Brashear and Heilman, 1984; Shoumaker, Ajax and Schenkenberg, 1977). Patients with PWD cannot understand spoken language but they can read, copy and write spontaneously, and speak in a relatively normal manner Cortex, (2001) 37, 139-150 140 Mario F. Mendez (Buchman, Garron, Trost-Cardamone et al., 1986). Isolated receptive amusia, or the loss of musical ability or appreciation, can follow right, left, or bilateral temporal strokes (Griffiths, Rees, Witton et al., 1997; Mavlov, 1980; Sparr, 1999). These different auditory syndromes imply that lesions in the left temporal region are necessary for agnosia for verbal sounds, lesions in the right temporal region are necessary for agnosia for non-verbal sounds, and either left or rightsided lesions may result in various disturbances in musical ability. This paper presents a left-handed patient whose cortical auditory syndrome deviated from these patterns in several respects. He is unique because of the presence of both verbal and non-verbal auditory agnosia from a stroke involving the right temporal region, along with an increased interest and appreciation of music. The aim of this study was to clarify the underlying mechanism for his unusual combination of neurological auditory manifestations. CASE REPORT NS, a 68-year-old left-handed man, had difficulty understanding speech after a stroke sustained during coronary artery bypass surgery. When he awoke from anesthesia, he could not understand what people were saying, as if they were “speaking too fast or in Chinese.” His own speech was not affected, and he could read and write. In addition, environmental sounds became indistinct and difficult to understand. The initial evaluation did not reveal focal abnormalities on his neurological examination, and his neuroimaging disclosed a right temporoparietal stroke. Over the course of the next twelve years, the patient continued with difficulty comprehending speech and environmental sounds. His wife reported that people resorted to writing notes to him because he could not follow oral conversations. In general, communication was achieved through writing. In this way, NS was able to maintain his lifestyle, including reading multiple newspapers, following the stock market, and maintaining his finances. He gravitated to reading and to “listening” with closed captions to television programs. Moreover, his appreciation of music increased over the years. Previous to his stroke, he had not shown a prominent interest in music. After his stroke, he spend much of his day listening to music. NS and his wife became avid attendees at concerts and other musical performances. Twelve years after his stroke, the patient underwent further evaluation for his auditory disorder. On interview, he was aware of his auditory difficulty and reported that speech still sounded fast and foreign and environmental sounds muffled. He endorsed a greater appreciation of music and would illustrate this by breaking out into song. The patient was a retired accountant who did not smoke and only occasionally used alcohol. He was strongly left-handed all of his life and was “left-footed” in sports. His past medical history was significant for coronary artery disease and benign prostatic hypertrophy, and his family history was negative for known familial illnesses and positive for left-handedness. On examination, this older man appeared much younger than his age. He was alert, attentive, and well oriented to place and time. NS was very talkative and had a slightly empty but otherwise fluent output without paraphasic errors. When spoken to, however, he appeared confused and perplexed. He could not comprehend most simple, verbal, one-step commands or yes/no questions but had no difficulty comprehending written commands. For example, he could not understand the verbal command “touch your chin” but immediately understood it in writing, and when asked “are we in New York?” he replied “Yes, I was born in New York.” Access to lip reading, careful attention to facial expression, and slowing of speech helped his auditory comprehension and allowed him to follow many simple commands. He attempted to visualize spoken words by spelling the words aloud or with his hands. Seeing a spoken word simultaneously written resulted in instantaneous auditory recognition with an expression of sudden discovery. The Token Test confirmed verbal, but Auditory agnosia 141 TABLE I Neuropsychological Tests (Administered with Written Instructions) Mini-Mental State Examination (without the 3-word registration): 24/27 Missed one item on counting backwards by 7’s, one memory item, and the repetition item CERAD* Auditory Verbal Learning Task (10 written words) (approx. within normal limits) Immediate trials: A: 3, B: 6: C: 8 Fifteen minute spontaneous delayed recall: 6/10 and Recognition: 20/20 Rey-Osterieth Complex Figure Copy 33/36 (30.14 ± 5.6)** 3 minute delayed recall: 9 (percent recall: 27%) (8.41 ± 5.9) Trailmaking A: 52” (44th percentile; 0 errors) Raven’s Coloured Progressive Matrices 29/36 A: 10, Ab: 10, B: 9 (95th percentile) Language Tests Verbal Fluency (FAS) 17 (39.08 + 14.17; cut-off 11) Boston Naming Test (BNT) 28/60 (51.56 + 7.0; cut-off 37) h BNT word comprehension (written word-picture match; 4 item multiple choice): 58/60 Original Token Test (very abnormal performance) Part I: Oral 5 Stretched 9 Written 10 Part II: Oral 3 Stretched 6 Written 10 Part III: Oral 0 Stretched 1 Written 10 Part IV: ___________ _________________ Written 10 Part V: ___________ _________________ Written 22 *Consortium to Establish a Registry in Alzheimer’s Disease; Reference tests to Lezak, 1995, and Mutrishina et al., 1999. **Norms and standard deviations. not written, comprehension difficulty with improvement when speech was slowed or “stretched” (Boller and Vignolo, 1966; De Renzi and Vignolo, 1962) (See Table I). Additional language testing was done. On confrontational naming, NS had difficulty producing names on the Boston Naming Test (BNT) (Kaplan, Goodglass and Weintraub, 1978) (see Table I). Because he could not take spoken cues, word comprehension was tested using written words. He was able to correctly match nearly all of the words with one a b Fig. 1 – Magnetic resonance imaging (MRI) disclosed a large area of infarction in the right temporoparietal region. a: T1-weighted horizontal image showing the wedge-shaped infarction. b: T1weighted sagittal view of the right hemisphere showing extension of the infarction along the superior temporal gyrus, Wernicke’s area, and Heschl’s gyrus, and extending posteriorly. The study was done 12 years after his stroke. 142 Mario F. Mendez Fig. 2 – Functional neuroimaging with 18-fluorodeoxyglucose positron emission tomography (PET) showed focal right temporal lobe hypometabolism. No other areas of hypometabolism were present. PET imaging was performed in a resting state. The study was done 12 years after his stroke. of four BNT pictures. Reading and writing were normal, and he could repeat single words perfectly. NS had trouble repeating longer phrases. For example, his attempt at repeating “no ifs ands or buts” was “nose hits blands and the bluffs,” and his attempt at repeating “for whom the bell tolls” was “for whom the spell extols.” His speech inflection and prosody were intact, and he responded to prosody. Finally, NS performed adequately on other neuropsychological tests (Mutrishina, Boone and D’Elia, 1999), although testing was limited because of his pronounced auditory comprehension deficit (see Table I). His general physical and neurological examinations were normal, but neuroimaging confirmed his single right hemisphere stroke. His cranial nerves were intact including clinical screening for hearing impairment. Visual fields were intact and there was no evidence of hemispatial neglect. Coordination, gait, motor, and sensory examinations did not reveal abnormalities. His reflexes were 2+ and symmetrical, and toes were downgoing. No pathologic reflexes were present. The patient had magnetic resonance imaging (MRI) which showed a single, large infarct of the right temporal lobe extending into the parietal region (see Figure 1). Functional neuroimaging with 18-fluorodeoxyglucose positron emission tomography (PET) showed focal right temporal lobe hypometabolism only (see Figure 2). After this evaluation, NS’s course included continued speech therapy with supported conversation. The goal was to improve the quality of his communication with his wife. He also agreed to undergo further audiological and psychoacoustic testing. NEUROLOGICAL INVESTIGATION Audiological and Dichotic Testing On pure tone audiometry, he had presbyacusis with normal hearing in the speech range (see Figure 3). With his eyes closed, NS was able to point to different sound sources (voices, clapping, bells) in the testing room. Finally, the Auditory agnosia 143 Fig. 3 – Pure tone threshold audiogram. X = left ear, 0 = right ear, HL = hearing level. Hearing levels are in dB (ANSI, 1969). There is high frequency hearing compatible with presbyacusis. patient had an assessment of click-fusion threshold by the method of ascending and descending limits, as previously described (Albert and Bear, 1974; Motomura, Yamadori, Mori et al., 1986). Two clicks of 0.1 msec in duration were presented binaurally and monaurally at different intervals. NS reported whether he heard a single click or two clicks. The patient fused these clicks at mean intervals of 16 msec in both ears, 8 msec in the right ear and 92 ms in the left. Prior reports note that normals can distinguish two clicks at 1-3 msec separation (Albert and Bear, 1974; Motomura et al., 1986). Dichotic listening was performed using the VA-CD Tonal and Speech Materials of Auditory Assessment (Nofsinger, Martinez and Wilson, 1994). The initial dichotic test consisted of 30 presentations of different nonsense syllables simultaneously played in each ear after adjusting for volume at about 50-60 db. The patient’s potential responses included 6 possible choices: the right ear phoneme, the left ear phoneme, and four random choices. On this dichotic listening test, he lateralized 20 presentations in the right ear, 3 to the left ear, and 7 were random, demonstrating a right ear advantage for these phonemes. A second dichotic test evaluated the discrimination of tones (1000 Hz) of short duration (250 ms) versus long duration (500 ms) from either ear, masked by 144 Mario F. Mendez tones of varying frequencies in the opposite ear. On this test, he was administered 60 trials of three tones varying in long and short tone sequences (ISI 200 msec). NS had difficulty in both ears, particularly the left: correct responses were 33 in the right ear and 18 in the left ear. Psychoacoustic Test Methods The Speech Sounds Perception Test and the Seashore Rhythm Test are wellknown standardized tests (Lezak, 1995; Mutrishina et al., 1999). Most of the other psychoacoustic tasks were previously described (Mendez and Geehan, 1988) and include pilot control data demonstrating 100% correct responses on these measures. The testing sessions were limited to 60 minutes, and instructions were given in writing. All auditory stimuli were presented binaurally by loudspeakers located 2 feet from the patient. The patient was asked to: (1) Listen to 48 pre-recorded environmental sounds and point to the corresponding picture. Four pictures were presented with each environmental sound. The four choices were either correct, acoustically related, semantically related, or unrelated. (2) Discriminate two environmental sounds as same or different by pointing to one of two response cards marked SAME or DIFFERENT. There were 10 trials. (3) Listen to 48 pre-recorded words and point to the corresponding picture. Four pictures were presented with each spoken word. The four choices were either correct, phonologically related, semantically related, or unrelated. (4) Listen to 48 pre-recorded words and point to the corresponding written word. Four written words were presented with each spoken word. The four choices were either correct, phonologically related, semantically related, or unrelated. (5) Read 48 words and point to the corresponding picture. Four pictures were presented with written word. The four choices were either correct, phonologically related, semantically related, or unrelated. (6) The Speech Sounds Perception Test. The test is composed of 60 spoken single-syllable nonsense words all containing the long “e” vowel sound and differing in beginning and ending consonants. There are four multiple choice options. (7) Listen to 10 common melodies (30 sec. samples) and point to the corresponding picture. Four pictures depicting descriptive scenes (e.g., New Year’s eve celebration with “Auld Lang Syne,” birthday party with “Happy Birthday,” American revolutionary theme with “Yankee Doodle,” Christmas carolers with “Silent Night”). (8) Discriminate as same or different between 10 pairs of melodies. (9) Listen to 10 common melodies (30 sec. samples) and point to the corresponding written name. Four names were presented for each melody. (10) The Seashore Rhythm Test. The test is composed of sequences of 5, 6, and 7 tones set in patterns in different time. The source is a beat-frequency oscillator set at 500 cycles. The subject was to indicate same or different. (11) Discriminate pre-recorded pure tones as same or different with respect Auditory agnosia 145 to differences in frequency, intensity, or duration. The same response cards were used, and there were 10 trials on each task. Parameters, when not an independent variable, were held at 60 dB, 1000 Hz, and 250 ms. Frequencies ranged from 250 to 3000 Hz with a minimum difference of 1000 Hz, intensity test used 70 to 90 dB with a minimum difference of 10 dB, and duration test used 75 to 300 ms with a minimum difference of 150 ms. (12) Discriminate as same or different between pairs comprised of three pure tone which varied either in regularity, in frequency pattern, or in number of tones. In the first 10 trials, three sounds varied in interstimulus intervals of 50-300 ms. In the second 10 trials, three tones varied in frequency patterns. In the third set, they were composed of longer tone sequences of 4-6 tones. Psychoacoustic Test Results Table II summarizes the results of the psychoacoustic tests. Additional observations include the following: (1) Matching environmental sounds-pictures: Of the 21 error responses, 16 were acoustically-related (76%), three were semantically-related (14%), and two were indeterminant (10%) (see Table III). NS focused on the rhythmic aspects of the sounds, and often attempted to repeat the beat of the sounds. (3) Matching of verbal words-pictures: Of the 20 error responses, 4 were phonologically-related (20%), 4 were semantically-related (20%), and 12 were indeterminate (60%). He identified short, single syllable words better than longer, multisyllable words. Otherwise, his responses appeared to be random guesses with a tendency to respond to whatever picture was located in the top right hand corner. TABLE II Psychoacoustic Test Results Test Correct results *1. Matching environmental sounds-pictures 2. Discrimination between two environmental sounds *3. Matching of verbal words-pictures 4. Matching of verbal words-written words 5. Matching of written words-pictures *6. Speech Sounds Perception Test 7. Matching of melodies-pictures 8. Discrimination between two melodies *9. Matching of melodies-written names 10. The Seashore Rhythm Test 11. Discrimination of pure tones based on frequency based on intensity based on duration *12. Discrimination between different tone sequences three tones with varied interstimulus intervals three tones with varied frequency patterns increased number of tones to 4-6 27/48 sounds 10/10 trials 28/48 spoken words 46/48 spoken words 48/48 written words 43/60** 10/10 10/10 trials 5/10 common melodies 24/30*** *NS had an impaired performance on these tests. ** Significantly less than most age-matched normals (Mutrishina et al., 1999). ***Age-adjusted normal mean 24.6 + 3.1; Bak and Greene, 1980. 10/10 trials 10/10 trials 10/10 trials 9/10 trials 8/10 trials 4/10 trials 146 Mario F. Mendez TABLE III Environmental Sound Errors Acoustic errors Baby crying Duck quacking Hand bell Clapping Typing Jack hammer Car Choir Harmonica Electric shaver Hammering Drain Coarse laughter Fire engine Waterfall Toilet for for for for for for for for for for for for for for for for Cat meowing Baby crying Telephone Horse galloping Clapping Sheep baaing Airplane Children’s playground Electric shaver Man humming Boy running Boy slurping Man sawing Church bells Toilet Dishes breaking Semantic errors Singing Alarm clock Man snoring for for for Orchestra Man snoring Man sneezing Indeterminate errors Parade Airplane for for Cow mooing Cash register (4) Matching of verbal words-written words: The presence of even the first few letters of the written word resulted in recognition. (6) Speech Sounds Perception Test: The patient’s errors were 61% on the ending syllable and 39% on the beginning syllable. (7) Matching of melodies-written names: Despite inability to name half of the common melodies, NS could sing all of them and would do so spontaneously. Singing the name helped recognition. Examples of errors including mistaking “Jingle Bells” for “Auld Lang Syne,” “Happy Birthday” for “Silent Night,” and “London Bridge” for “Yankee Doodle.” Despite these errors in naming the tunes, he could describe their usual context, e.g., “Happy Birthday” to celebrate someone’s anniversary. (10) The Seashore Rhythm Test: He would hum the rhythms to himself and would tap the rhythms out on the table. DISCUSSION This patient illustrated impaired auditory comprehension for both words and sounds consequent to a stroke involving the right temporal auditory cortex. Whereas right temporal lesions can produce non-linguistic auditory agnosia, the presence of additional agnosia for spoken language may be due to a dependency on alternative auditory-language pathways in this left-handed person. In addition, NS had an increase in his appreciation of music, so much so that listening to music became his main activity. Generalized auditory agnosia usually results from bilateral lesions affecting posterior temporal lobes (Godefroy, Leys, Furby et al., 1995; Ho, Kileny, Paccioretti et al., 1987; Oppenheimer and Newcombe, 1978), subcortical Auditory agnosia 147 temporal radiations (Hasegawa, Bando, Iwata et al., 1989; Kazui, Naritomi, Sawada et al., 1990; Motomura et al., 1986), inferior colliculi (Johkura, Matsumoto, Hasegawa et al., 1998), and even the insulae (Habib, Daquin, Milandre et al., 1995). Prior PET studies have shown in these patients bilateral temporal changes, albeit with a particular role for the right temporal region (Engelien, Silbersweig, Stern et al., 1995; Nove-Josserand, Fischer, Nighoghossian et al., 1998). In contrast, all prior cases of auditory agnosia from isolated right-sided lesions have been selective for environmental sounds (Fujii et al., 1990; Lambert, Eustache, Lechevalier et al., 1989; Nielsen and Sult, 1939; Spreen et al., 1965; Wortis and Pfeffer, 1948). This is the first patient report of generalized auditory agnosia from a right temporal lesion. Investigators have long proposed two basic mechanisms for the agnosias, an apperceptive (perceptual) one and an associative (semantic) one (Vignolo, 1982). Apperceptive agnosia is impaired recognition from an abnormal percept despite adequate sensory abilities, and associative agnosia is impaired recognition when a normal percept does not arouse meaningful attributes. Although this dichotomy is often indistinct (De Renzi and Lucchelli, 1993), particularly in the auditory modality (Fujii et al., 1990; Spreen et al., 1965), many patients with right temporal lesions have apperceptive features, and those with left-sided lesions have associative ones. Right hemisphere patients tend to make acoustic errors in environmental sounds, and left-hemisphere patients tend to make semantic errors (Schnider, Benson, Alexander et al., 1994; Vignolo, 1982). In environmental sound recognition, NS had predominant acoustic errors consistent with an apperceptive deficit (Buchtel and Stewart, 1989; Ulrich, 1977). The specific apperceptive deficit in generalized auditory agnosia may be a disorder of auditory temporal processing (Buchtel and Stewart, 1989; Godefroy et al., 1995; Kaga, Shindo and Tanaka, 1997). The literature reports abnormalities in temporal duration (Rosati, DeBastiani, Paolino et al., 1982), temporal resolution and summation (Albert and Bear, 1974; Auerbach, Allard, Naeser et al., 1982; Motomura et al., 1986; Tanaka, Yamadori and Mori, 1987), separation of two tones and click-fusion discrimination (Albert and Bear, 1974; Buchtel and Stewart, 1989; Motomura et al., 1986; Chocholle, Chedru, Botte et al. 1975; Kazui et al., 1990), and temporal order and sequencing (Jerger, Weikers, Sharbrough et al., 1969; Mendez and Geehan, 1988). Difficulty in processing brief sounds may impair connected speech and the comprehension of prolonged series of sounds (Buchman et al., 1986; Buchtel and Stewart, 1989; Chocholle et al., 1975). The overall pattern of audiological, dichotic, and psychoacoustic findings in NS points to abnormal temporal processing from his right temporal lesion. This patient’s impaired verbal comprehension resembled PWD in having preserved reading comprehension and a sensation of speech as fast and foreign (Albert and Bear, 1974). In PWD, bilateral lesions of the anterior part of the superior temporal gyri or unilateral subcortical lesions of the left temporal lobe disconnect cortical auditory areas from a relatively intact Wernicke’s area (Auerbach et al., 1982; Buchman et al., 1986; Coslett et al., 1984; Kanter, Day, Heilman et al., 1986). NS’s preserved reading ability and lateralization of phonemes to the right ear suggested a functioning Wernicke’s area in the left 148 Mario F. Mendez hemisphere disconnected from auditory input from his damaged right temporal region. The processing of verbal sounds may require fine temporal discrimination (Blumstein and Cooper, 1974), and most studies of PWD patients show abnormalities in temporal resolution or related processes (Albert and Bear, 1974; Auerbach et al., 1982; Buchman et al., 1986; Chocholle et al., 1975; Jerger et al., 1969; Kanshepolsky, Kelley and Waggener, 1973; Klein, Kurtzberg, Brattson et al., 1995; Mendez and Geehan, 1988; Praamstra, Hagoort, Maassen et al., 1991). In NS, a left-handed man, the fine temporal analysis of verbal sounds may take place in his right auditory cortex rather than his left Heschl’s gyrus, as is usually the case (Breitling, Guenther and Rondot, 1987; Gates and Bradshaw, 1973; Halperin, Nachshon and Carmon, 1973). This patient also had a unique preservation of musical appreciation. Brain lesions can affect separate attributes of music in isolation (Polster and Rose, 1998; Peretz, Belleville and Fontaine, 1997). Bilateral temporal or isolated rightsided lesions can cause amelodia with abnormal sequencing of melodic variations and preserved rhythm (Griffiths et al., 1997; Johkura et al., 1998; Peretz, Kolinky, Tramo et al., 1994; Sparr, 1999). Left hemisphere lesions can cause a “rhythm agnosia” with abnormal recognition of simple rhythm patterns (Assal and Buttet, 1983; Mavlov, 1980). Although impairment of music perception occurs in most cases of auditory agnosia (Gates and Bradshaw, 1973), the musical quality of sound stimuli and musical pleasure may be differentially spared (LeChevalier, Rossa, Eustache et al., 1984). Despite his anomia in naming melodies, NS demonstrated intact perception of the musical quality of sounds and of rhythm. The presence of left-handedness and probable bilateral representation of language complicates the interpretation of this patient’s generalized auditory agnosia. NS had significant anomia on confrontational naming, supporting the participation of the right hemisphere in language production. There was no evidence on either MRI and PET imaging of a second lesion in the left temporal lobe that might otherwise explain his anomia. Furthermore the presence of right ear advantage in dichotic test may reflect right temporal lobe damage more than the integrity of language functions in the left hemisphere. In conclusion, this unusual patient adds to our understanding of generalized auditory agnosia. NS may have a deficit in integrating sounds into a temporal holistic pattern distinct from rhythm and music recognition (Hupfer, Jurgens and Ploog, 1977). As in patients with selective auditory agnosia, his right hemisphere is preferentially involved in acoustically processing environmental sounds. In contrast to most patients, however, his left Wernicke’s area appears to depends on speech input from his damaged right temporal lobe. 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Mendez, Neurobehavior Unit (116AF), V.A. Greater Los Angeles Healthcare System, 11301 Wilshire Blvd., Los Angeles, CA 90073, U.S.A. E-mail: mmendez@ucla.edu (Received 3 April 2000; reviewed 11 May 2000; revised 21 June 2000; accepted 11 July 2000)