Neurocase The Neural Basis of Cognition ISSN: (Print) (Online) Journal homepage: https://www.tandfonline.com/loi/nncs20 Pure word deafness due to bilateral temporal lobe ischemic stroke occurring at different time points over the years: a case report on the insight of brain language network reorganization Ioanna‐Eleni Virvidaki, Lambros Messinis & Grigorios Nasios To cite this article: Ioanna‐Eleni Virvidaki, Lambros Messinis & Grigorios Nasios (2021) Pure word deafness due to bilateral temporal lobe ischemic stroke occurring at different time points over the years: a case report on the insight of brain language network reorganization, Neurocase, 27:1, 106-112, DOI: 10.1080/13554794.2021.1896744 To link to this article: https://doi.org/10.1080/13554794.2021.1896744 Published online: 09 Mar 2021. Submit your article to this journal Article views: 66 View related articles View Crossmark data Full Terms & Conditions of access and use can be found at https://www.tandfonline.com/action/journalInformation?journalCode=nncs20 NEUROCASE 2021, VOL. 27, NO. 1, 106–112 https://doi.org/10.1080/13554794.2021.1896744 Pure word deafness due to bilateral temporal lobe ischemic stroke occurring at different time points over the years: a case report on the insight of brain language network reorganization Ioanna-Eleni Virvidakia, Lambros Messinisb and Grigorios Nasiosa a Department of Speech and Language Therapy, School of Health Sciences, University of Ioannina, Ioannina, Greece; bNeuropsychology Section, Departments of Neurology and Psychiatry, University of Patras Medical School, Patras, Greece ABSTRACT ARTICLE HISTORY Here we present a case of a native Greek male patient who presented clinically with sudden onset pure word deafness after an ischemic stroke in the temporoparietal region of the right hemisphere, but who had suffered an ischemic stroke 9 years previously in an adjacent area of the left hemisphere, causing aphasic symptoms which resolved quickly and almost completely. What makes this case interesting and novel is that it is the first case describing a patient whose ventral language comprehension circuit did not reorganize successfully due to damage of the adjacent right hemisphere language areas at a subsequent time. Received 16 December 2020 Accepted 24 February 2021 KEYWORDS Pure word deafness; stroke; temporal lesions; language comprehension Introduction Pure word deafness (PWD) is a rare, neurological disorder char­ acterized by marked difficulty in comprehending spoken lan­ guage but spared written comprehension and speech production (Kussmaul, 1877; Lichteim, 1885). In its true “pure” form, the coined term has been debated because it presumably should only be applied to patients with isolated auditory impairments for speech sounds (Poeppel, 2001). However, more commonly it has been applied to patients with dispropor­ tionate but not selective deficits in auditory input processing for verbal stimuli and irrespective of coexisting aphasia and/or agraphia (Maffei et al., 2017). In most reported cases, PWD is acquired after bilateral damage to the temporal lobes (Geschwind, 1965; Miceli et al., 2008; Poeppel, 2001; Slotwinski et al., 2020). Less frequently it has been described following subcortical or cortical-subcortical lesions (Hayashi & Hayashi, 2007; Taniwaki et al., 2000) or iso­ lated left temporal lesions (Hayashi & Hayashi, 2007; Maffei et al., 2017; Slevc et al., 2011; Wang et al., 2000) further provid­ ing evidence favoring the disconnection hypothesis of PWD. It is mostly documented in adults with acute stroke or head trauma but has also been reported in children with LandauKleffner syndrome (Baynes et al., 1998) and brain tumor (Chou et al., 2011). Literature also reveals cases of PWD caused by osmotic demyelination syndromes (Garde & Cowey, 1998; Zhu et al., 2010), neurodegenerative diseases (Kim et al., 2011; Lizuka et al., 2007; Otsuki et al., 1998) multiple sclerosis (Tabira et al., 1981; Jónsdóttir et al., 1998), encephalitis (Goldstein, 1974; Arias et al., 1995; Kasselimis et al., 2017) seizures (Fung et al., 2000; Stefanatos et al., 2005), mitochon­ drial encephalomyopathy (Miceli et al., 2008), Creutzfeldt-Jakob CONTACT Grigorios Nasios Ioannina, Greece grigoriosnasios@gmail.com © 2021 Informa UK Limited, trading as Taylor & Francis Group disease (Hillis & Selnes, 1999; Tobias et al., 1994), and drug toxicity (Donaldson et al., 1981). Auditory processing disorders vary in severity, duration, and quality depending on lesion size and location (Maffei et al., 2017). In severe forms of the disorder, patients may not react voluntarily to auditory stimuli and behave as if they were deaf, although they retain some ability to respond reflexively to sounds (Garde & Cowey, 1998). The least impaired patients may voluntarily be able to detect or identify auditory stimuli but present with difficulties in accurately processing these sounds (Ishii et al., 1995; Maffei et al., 2017). Patients’ subjective descriptions are intriguing and seem to also vary in published reports suggesting a continuum of severity (Stefanatos et al., 2005). Some case studies highlight marked impedance in recognizing the acoustic characteristics of a human voice while others have alluded to subtler difficul­ ties mapping the acoustic features of speech to lexical repre­ sentations (Stefanatos et al., 2005). Historically, speech has been described as “a great noise all the time . . . you think you can catch it and it fades away” (Buchman et al., 1986; Coslett et al., 1984), “a hurr or buzzing” (Mendez & Geehan, 1988) “foreign folks speaking in the distance” (Auerbach et al., 1982; Klein & Harper, 1956; Stefanatos et al., 2005) or simply “I can hear you talking but I can’t translate it” (Kanshepolsky et al., 1973) or “does not register” (Saffran et al., 1976). Other patients describe their auditory experience as “words come too quickly” (Albert & Bear, 1974) or “just run together” (Klein & Harper, 1956), reflecting partially intact ability to capture qualitative information from the speaker’s voice but that maybe percep­ tual or cognitive resources cannot keep up with the rate of speech production (Stefanatos, 2008). Department of Speech and Language Therapy, School of Health Sciences, University of Ioannina, NEUROCASE Accumulating evidence suggests that the speech percep­ tion difficulties in PWD reflect underlying deficits in rapid temporal processing (Poeppel, 2001; Slevc et al., 2011; Stefanatos, 2008). This claim is supported by the observation that patients with PWD typically demonstrate difficulties per­ ceiving temporally dynamic features of consonants (especially changes in place of articulation and voicing in stop conso­ nants) rather than steady state stimuli like vowels (Slevc, 2012). Several different explanations have been proposed regarding speech processing and hemispheric specializations. Neuroimaging studies involving patients with temporoparie­ tal damage and non-brain-damaged participants suggest a plausible left hemispheric bias for processing the temporal aspects of sound and a right hemispheric preference for pro­ cessing the spectral aspects of sound (Robin et al., 1990; Scott & Wise, 2004; Slevc, 2012; Warrier et al., 2009). In this study, we present a case of pure word deafness with preexisting cognitive-communication disorder due to stroke and necrosis of the left temporoparietal area which did not threaten the patient’s functional independence in performing daily activities. However, ischemic necrosis of the temporopar­ ietal area in the right hemisphere owing to a second stroke years later, contributed to the clinical presentation we describe and discuss in terms of the functional organization of the language circuitry. Case report 107 Neuropsychological and speech-language evaluations were performed 3 weeks after the onset of his problems in auditory recognition. Both cognition and communication were affected after the second ischemic event, and AM reported his situation frustrating and isolating at times. His general physical condition was normal. Neurological examination revealed no signs of paresis, sensory or visual field deficits. Lack of access to initial clinical assessment data prevented the inclusion of language testing procedures to serve as a baseline for the testing con­ ducted after the second stroke. AM gave permission for his history and medical information to be published. Personal account AM never complained of auditory disorders before his strokes. He displayed an awareness of his deficit in understanding spoken language. The following self-reported perspective is a free trans­ lation from Greek: “this is where I get confused and I cannot make the discrimination-I cannot understand . . . it feels as though “this” (pointing to his brain) is constantly foggy. I cannot perceive mean­ ings, do you understand? I mean I can read, I can do things I used to do, but I cannot listen. I watch TV, I read on the internet. I can understand what I am reading but I cannot recognize what I hear. When I listen to the news, some things are recognized, others are lost. Later in our communicative exchange, he noted, “I can hear the doorbell ring, but I cannot hear you speak . . . and then, I cannot express myself. I hear people talk but I cannot express myself”. He continues (sighing) “we have a long way to go”. Background information AM (initials deliberately changed) is a right-handed, native Greek man who in 2010, at age 60, suffered a heart attack followed by a stroke, involving extensive lesions in the tempor­ oparietal areas of the left hemisphere, with the superior tem­ poral gyrus (STG) identified as the core ischemic lesion site (see Figures 1&2). He had idiopathic hypertension since the age of 50 and was a smoker (40 pack/years, until the myocardial infarction occurred). When hospitalized for a heart attack, he was additionally diagnosed with diabetes mellitus type 2. He is a retired post office employee and lives with his wife. He is also a grandfather with three grandchildren. At the onset, he exhibited signs of a broader aphasic dis­ turbance resembling a severe Broca’s aphasia. His family reports an initial inability to formulate language which rapidly resolved in the first few weeks. Language abilities improved significantly over the course of a few months during which time, the patient also received speech and language therapy services. The 2010 language disorder was diagnosed as expres­ sive in nature although the brain lesion was mainly parietotem­ poral. We did not have access to initial clinical assessment data as the patient was cared for in his hometown, a small town in the Epirus region in northwestern Greece. Retrospectively, one could argue that the aphasic syndrome could be better approached as conduction aphasia. Both the patient and his communication partners highlight that they did not expect such a rapid recovery of language abilities to a state of ade­ quate use of language in every-day functional communication. At the end of 2018, AM suffered a second stroke involving the adjacent temporoparietal region in the right hemisphere. Neuroimaging Magnetic resonance imaging (MRI) performed 3 weeks after his 2018 stroke showed the presence of rather symmetrical lesions involving mainly temporal and parietal perisylvian regions but sparing the frontal lobes. The left-hemispheric lesion character­ istics were chronic in nature, whereas the right lesion was in line with subacute origin. Both sides showed extensive damage to the STG (Figure 1 & Figure 2) Initial clinical setting Pure-tone audiometry testing was initially performed to mea­ sure the level of hearing acuity of our patient. Normal hearing thresholds were revealed. Subsequent neurolinguistic assess­ ment with AM was undertaken in Greek, the only language the patient spoke. We used formal and informal assessment proce­ dures. The entire evaluation was completed in two visits sepa­ rated by 1 week. When AM could not understand a question, written instructions in Greek were provided. The patient was alert and oriented for time, place, and person. His general ability to engage in communication interchange was poor. His comprehension of daily conversation was enhanced when the conversational partner used gestural and excess pro­ sodic cues (such as increased contrastive stress and intonation patterns and slower speech). AM understood his problem and was frustrated by it. He could augment auditory comprehension with lip reading although he could not lip read without hearing the voice. His conversational speech was fluent and grammati­ cally correct with normal phrase length but with occasional 108 I. VIRVIDAKI ET AL. Figure 1. Axonal T2 (left) and T1 MR images (center) and coronal T1 image of the chronic (left) and subacute (right) ischemic lesions of patient AM. Figure 2. MR T2 dark-fluid axonal sequences, revealing bilateral, mainly temporal, ischemic lesions. paraphasic errors. Praxis was normal as assessed via a modified version of the Apraxia Battery for Adults-2 (Dabul, 2000). AM flawlessly and articulately produced automated sequences. Assessment of language Formal assessment of language via the Boston Diagnostic Aphasia Examination-2nd ed (Goodglass & Kaplan, 1972) revealed marked deficits in auditory language comprehension and repetition. Subtests were performed without restrictions on lip reading. His performance on word recognition, body part discrimination, written words to dictation, and repetition dete­ riorated when lip reading was not allowed. AM presented with defective auditory verbal comprehen­ sion. He displayed difficulty following sequential commands (“point to the window and then the door”) and answering biographical/nonbiographical questions requiring a basic yes/ no response. He had better, yet not complete, success in responding to biographic questions. He was able to recognize most body parts, colors, real objects, numbers, and letters (less proficiency with color identification, 2/5). Assessment of sen­ tence-level auditory comprehension revealed more pro­ nounced deficits. AM scored 1/5 (20%) on all respective matching subtests measuring syntactic processing. By contrast, expressive communication ability was relatively preserved. His verbal output in spontaneous speech and pic­ ture description tasks retained fluency, functional content, and adequate prosodic features (intonation, stress, rhythm). Connected narratives of daily life activities included meaningful and grammatically correct sentences. Rare literal paraphasias were noted (e.g., “provavizome” vs “provivazome”) which appeared to be related to periodic lapses in self-monitoring. Similarly, instances of logorrhea or increased speech output were observed at the initiation of tasks that required him to respond non-verbally (e.g., by pointing). Oral reading (reading aloud) ability was intact for all levels of sentences and paragraph complexity. Comprehension of writ­ ten material was intact for simple sentences but displayed impairments for more lengthy, complex sentences and para­ graphs. His ability to correctly repeat single words displayed some accuracy over time (first visit: 1/10, second visit: 6/10 with one repetition allowed). However, repetition was severely impaired at the phrase and sentence level (0/5 correct). His ability to write to dictation was spared up to a word level. AM correctly wrote upon request his name and address, numbers, letters, syllables, and words with four syllables. His “breakdown” appeared to occur at the phrase and sentence level where he relied on more contextual cues and multiple repetitions to pre­ pare his response. He had great difficulty answering situational questions provided through the auditory channel (e.g., what is the weather like outside?). By contrast, he made no mistakes in answering written questions, writing spontaneously, and copying. Performance on the Boston Naming Test, second ed (Kaplan et al., 2001) was moderately impaired. In this confrontation naming task involving 60-line drawings of objects with graded difficulty, AM scored 42/60 (65%). An evaluation of error types and examples of those errors are listed in Table 1. *BNT; Boston naming test It is worth noting that AM produced four more errors (three at the phonological level and one at the semantic level) which he spontaneously self-corrected and thus, was given credit. These errors reflect AM’s difficulties retrieving the target word. Accordingly, lenient scoring was used for two items for which synonyms were provided in a pilot study including normative data on this test for healthy Greek speakers (Patricacou et al., 2007). Finally, performance on sentence completion and responsive speech tasks was poor (20%) secondary to his com­ prehension deficits. NEUROCASE Table 1. An analysis of AM’s observed error types on the BNT*. Error Types No response (3) Misperception (1) Semantic (7) Definition No attempt to name the object Examples “don’t know what this is” for “seahorse” A visual misperception of the “person with legs” for pictured object “Sphinx” a) Production of the category name a) “this is a musical b) Production of a related member instrument” for c) Associated with the concept “harp” b) “seagull” for “pelican” c) “paintbrushes” for “palette” Phonemic (8) Mispronounced word preserving “taniera” for “tenis”, half of the components of the “athimotrio” for target word “arithmitirio” Neologistic (2) Less than 50% of phonemes “femanestra” for common with the target word “siðero”, “valani” for “rhinoceros” Further Assessment of Language Processing/Processing of Verbal Stimuli: Subtests from the Psycholinguistic Assessments of Language in Aphasia (PALPA) (Kay et al., 1992), were adjusted and presented to investigate AM’s ability to carry out auditory input processing at various levels. During all auditory tasks, AM was not allowed to see the examiner’s mouth but was offered written instructions before initiating each task. AM completed auditory lexical decision tasks whereby he was required to make perceptual judgments on 30 pairs of constructed, nonsense words, and meaningful real words by responding with a yes/no response (word/non-word). Half of the pseudowords had a change in a distinctive feature in a single phoneme in a different place of articulation (e.g., “hironas” from “himonas”). The other half was created by mov­ ing a phonemic sequence to a different place in the word (e.g., “patharytho” from “parathyro”). AM’s performance was 67% for words and non-words combined and was marked by some hesitations. AM could not recognize five actual words and five non-words. Healthy controls performed at 97.1% correct. Similarly, AM’s performance on tasks requiring him to use non-lexical routes and repeat nonsense words was remarkably poor. Strict scoring for entirely correct responses provided a 0% score, however, it is interesting to note that his responses revealed partially correct phonemic identification and that all but one mistake involved difficulties perceiving consonants, typically occupying the initial word position (e.g., “kotiri” vs “potiri”). Additionally, a homophone matching task was administered whereby 14 sets of common words were recorded and pre­ sented auditorily for the patient to indicate (verbally or via pointing to two written choices same/different) whether the two words had identical or non-identical pronunciations. AM achieved 57% correct (8/14). Normal controls obtained 100% correct on this task. AM’s performance was poor but above chance. Error analysis again reveals a specific difficulty in dis­ criminating distinctive phonemic features, namely, differences in voicing (voiced/voiceless consonant) and place of articula­ tion (labial, alveolar, and velar). By contrast, 32 words with a CVCV combination were recorded and presented auditorily. Following a 2-s interval, the patient was asked to match the spoken word to one of 109 the two written alternatives, one matching the heard word and one being used as a phonological distracter. AM fared better in this task supported by the visual modality (27/32, 86% correct). Unimpaired participants performed at 98% correct. Finally, AM was required to make semantic judgments with sentences presented initially auditorily and then followed by a task utilizing the same stimuli presented through the visual channel. AM’s performance was 9/15 (60%) and 13/15 (87%) respectively. His ability to access the semantic system via the auditory modality significantly relied on the repetition of the content and more contextual cues (effective speech with allowed pauses). Auditory processing of non-verbal stimuli The ability of AM to process environmental sounds and music was tested in several tasks. Each task was also performed by 10 healthy, age-, and education-matched controls. Our patient was asked to identify a set of 32 recorded environmental sounds corresponding to one of the four sound categories: (1) animal/bird sounds, (2) transport vehicles, (3) household/tool sounds, and (4) recreational/sport activities. The sounds were presented in a randomized order among the tested categories and the patient heard the stimulus twice before identifying it. After hearing each sound, he was asked to point to the corre­ sponding picture in a four-alternative field response paradigm. Each response card included a pictorial representation corre­ sponding to the target, while the three others were semantic foils from the same semantic category. AM’s overall perfor­ mance in sound recognition was 72% correct (23/32). He cor­ rected identified 6/8 animal/bird sounds, 6/8 vehicles, 7/8 household/tool sounds, and 4/8 recreational/sport activities. AM showed difficulty recognizing horseback riding, boating, swimming, and the sound of table tennis. The observed varia­ bility in the latter category may possibly be related to lowintensity sounds. Several ancillary measures of auditory processing of nonverbal stimuli were also administered. AM was asked to name the musical instrument producing a note and to establish if two melodies were the same or different. His performance was not significantly distinguishable from that of healthy volunteers in terms of providing an accurate response but only in terms of the time required to produce a response. AM was also able to discriminate between a male and a female voice and between Greek and non-Greek languages. He could further recognize when the speaker’s voice was emotionally neutral, happy, or angry. Finally, he could discriminate between laughter and crying. Discussion This case study is unique for numerous reasons. To our knowl­ edge, this is the first Greek-speaking person described with clinical manifestations of this syndrome with the etiology of a stroke. One case report has been recently published with herpes simplex encephalitis by Kasselimis et al. (2017) with interestingly similar neural substrates underpinning the audi­ tory comprehension deficits. Another reason is the time interval between the incident ischemic event and the recurrent event which contributed to our patient’s clinical profile. It is worth 110 I. VIRVIDAKI ET AL. noting that AM did not complain of speech, language, or com­ munication difficulties during this lengthy 9-year period. However, lack of access to the initial objective assessment of language abilities constituted a limitation of our study and prevented us from utilizing initial testing procedures as a baseline protocol for the testing performed after the second stroke. AM’s initial clinical presentation of aphasia in 2010, consid­ ered severe, affecting mostly language expression, may be explained partially by the diaschisis theory, which stipulates further clinical encumbrance the first weeks after the destruc­ tive brain damage (Price et al., 2001; Warren et al., 2009). His subsequent rapid recovery may be explained by the gradual obviation of the diaschisis and the functional reorganization of the language circuitry, which to a large extent had escaped necrosis. In fact, the right frontal lobes, a significant portion of the left parietal lobe and the right hemisphere remained intact, and his rapid recovery was grounded on their functional reconnection. This explanation supports and strengthens the dual-stream model of language processing (Hickok & Poeppel, 2007). AM’s frontal and part of the dorsal language network in addition to all the language centers and networks of the bilaterally organized ventral circuit were spared, thereby enhancing the reactivation of those “lost” left hemi­ sphere language areas and functions. The successful func­ tional reorganization of AM’s left anterolateral superior temporal cortex and right anterior superior temporal cortex has been shown to predict a positive language outcome after the incident stroke (Warren et al., 2009). In this regard, our patient remained functionally communicative until he suf­ fered the second ischemic stroke that destroyed the areas in which reorganization was originally based and prompted the severe communication deficit. Our case study adds to the claim of a dual-stream model to language processing and specifically a bilaterally organized ven­ tral stream “running” in both temporal lobes that mediate auditory comprehension (Hickok & Poeppel, 2007). In ΑΜ, when the left temporal lobe was damaged by the first-ever ischemic stroke, language functions were quickly and effectively restored due to the maintenance of the integrity of the right temporal networks. We believe that during the 9-year time-lapse between the incident and recurrent ischemic events, the destroyed left hemisphere areas were “functionally hidden” (Nasios et al., 2019). Necrosis of the right hemisphere areas, in isolation, was not expected to impact the language and communicative abilities of AM, however, severe deficits developed after the second stroke as the brain of AM had no other residual areas to compensate for the new loss. A recently published case report by Slotwinski et al. (2020) pre­ sented a patient with similar brain lesions when compared to our patient AM but occurring with different time order. Specifically, the authors confirmed an initial right temporal lesion that was not associated with speech disturbances, followed by a new, acute, left temporal lesion, revealing a cluster of features that suggested pure word deafness in their patient (Slotwinski et al., 2020). This consideration offers further supporting evidence for the bilateral organization of the ventral networks for language comprehension, supporting the dual-stream model. Similarly, in AM, the maintenance of the right temporal centers was sufficient for the patient to sustain functional communication. However, their sub­ sequent destruction consequently to the second stroke revealed the value of the bilateral organization of the language compre­ hension networks. Moreover, certain other factors tended to improve our patient’s performance. Lip reading offered considerable information for place of articulation. Consonants carry more of the linguistic message than vowels. Consistent with previous reports of PWD (Jacobs & Schneider, 2003; Saffran et al., 1976; Shindo et al., 1991), AM appeared to utilize lip reading to enhance auditory comprehension of the spoken message. Similarly, in agreement with other studies, his comprehension improved when the rate of speech presented to him was slower (Albert & Bear, 1974; Oppenheimer & Newcombe, 1978). This seems to emphasize the importance of the temporal aspects of speech for its processing. Language assessment using the BDAE revealed that he had significant deficits in auditory comprehension, syntactic processing, repetition, writing to dictation, despite the pre­ sence of good reading, fluent speech, and spontaneous writing. He made few paraphasic errors in his spontaneous (running) utterances. This was more pronounced in the confrontation naming task. The presence of aphasic symp­ toms as residua of a left-sided stroke was more likely to be phonemic paraphasias than semantic paraphasias and could be attributed to difficulty decoding and monitoring phonol­ ogy. AM also had semantically coded errors; thus, he also displayed difficulties with accessing semantic knowledge. Evidence of generalized auditory agnosia, i.e., the ability to recognize environmental (nonverbal) sounds was not intact, consistent with most documented reports (Garde & Cowey, 1998; Hurley et al., 2018; Taniwaki et al., 2000; Wang et al., 2000). Concluding comments This is the first case describing a Greek-speaking person, whose ventral language comprehension circuit did not undergo suc­ cessful reorganization due to a second ischemic event 9 years after the incident stroke, which further damaged the adjacent right hemisphere language areas. Our case provides an impor­ tant insight of brain language network reorganization, not only revealing the value of bilateral organization of the language comprehension networks but also serves as further supporting evidence for the “dual contribution of local cortical and path­ way-level function to focal lesion effects on language proces­ sing” (Warren et al., 2009). Acknowledgments We are grateful to AM and his family members for sharing with us the long road of recovery and their permission to publish this paper. Disclosure statement There was no funding source for this study. NEUROCASE Author contributions IEV performed all language testing. GN is the patient’s neurologist. All authors participated in the structuring and reviewing the manuscript. Data availability Original recording, MRI data, and other relevant information are all avail­ able in AM’s medical record file. Informed consent AM gave his permission for publishing his data by signing an informed consent. 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