Neurocase The Neural Basis of Cognition ISSN: (Print) (Online) Journal homepage: https://www.tandfonline.com/loi/nncs20 A case of aphemia following non-dominant subinsular stroke: unveiling the Foix-Chavany-Marie phenomenon Saurav Das, Whitney Postman, Michael A. Haboubi, Ozan Akca, Kerri Remmel, Alexandre R. Carter & Allyson Zazulia To cite this article: Saurav Das, Whitney Postman, Michael A. Haboubi, Ozan Akca, Kerri Remmel, Alexandre R. Carter & Allyson Zazulia (2021): A case of aphemia following nondominant sub-insular stroke: unveiling the Foix-Chavany-Marie phenomenon, Neurocase, DOI: 10.1080/13554794.2021.1933541 To link to this article: https://doi.org/10.1080/13554794.2021.1933541 Published online: 27 Jun 2021. Submit your article to this journal Article views: 51 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 https://doi.org/10.1080/13554794.2021.1933541 A case of aphemia following non-dominant sub-insular stroke: unveiling the FoixChavany-Marie phenomenon Saurav Das a, Whitney Postmanb, Michael A. Haboubic, Ozan Akcad, Kerri Remmele, Alexandre R. Carterf and Allyson Zazuliag a Vascular Neurology Fellow, Washington University School of Medicine, St. Louis, MO, USA; bDirector of Neurorehabilitation and Language Laboratory, Department of Communication Sciences and Disorders, Saint Louis University, St. Louis, MO, USA; cComprehensive Stroke Center and Department of Neurology, University of Louisville School of Medicine, Louisville, KY, USA; dVice Chair for Research and Professor, Department of Anesthesiology and Perioperative Medicine, Director, Stroke ICU, Comprehensive Stroke Center Clinical Research Program (CSCRP, University of Louisville, Louisville, Kentucky, USA; eChair, Department of Neurology, University of Louisville; Director, Comprehensive Stroke Center, Comprehensive Stroke Center Clinical Research Program (CSCRP, University of Louisville Hospital, Louisville, Kentucky, USA; fDivision of Neurorehabilitation, Washington University School of Medicine, St. Louis, MO, USA; gNeurology and Radiology, Associate Dean for Continuing Medical Education, Washington University School of Medicine, St. Louis, MO, USA ABSTRACT ARTICLE HISTORY Aphemia refers to the clinical syndrome of inability to orally produce speech with intact comprehension and written expression. Aphemia has been primarily reported in dominant frontal lobe strokes resulting in apraxia of speech (AoS), and in Foix-Chavany-Marie (FCM) syndrome where bilateral opercular or subopercular lesions result in anarthria due to deafferentation of brainstem nuclei supplying the oro-faciolingual and pharyngeal musculature. Aphemia is not reported in non-dominant sub-insular strokes. Here, we present a case of aphemia following non-dominant sub-insular stroke in a patient who had previously recovered from a homologous dominant sub-insular stroke without any apparent residual deficits. We discuss the accepted definitions, theories and controversies in the use of the terminology – aphemia, apraxia of speech (AoS), anarthria related to FCM syndrome, a concomitant pathology – unilateral upper motor neuron (UUMN) dysarthria, and their neuro-anatomical bases. We also highlight the importance of attributing localization value to sequential homologous lesions of the brain that can unveil symptoms due to a “loss of compensation phenomenon” that we propose be termed as “FCM phenomenon.” These pathological mechanisms may alone or in certain combinations contribute to the clinical syndrome of aphemia included in the diagnostic approach proposed here. The distinction between these mechanisms requires serial careful neurological examination and detailed speech evaluation including in the recovery phase. Received 2 October 2020 Accepted 17 May 2021 Introduction Aphemia refers to the clinical syndrome of inability to orally produce speech with intact comprehension and writ­ ten expression. It has been primarily reported in dominant frontal lobe strokes resulting in apraxia of speech (AoS), and in Foix-Chavany-Marie (FCM) syndrome where bilateral opercular or sub-opercular lesions result in anarthria due to deafferentation of brainstem nuclei supplying the orofacio-lingual and pharyngeal musculature. Here, we pre­ sent a case of aphemia following non-dominant sub-insu­ lar stroke in a patient who had previously recovered from a homologous dominant sub-insular stroke without any apparent residual deficits. We propose a diagnostic approach to a patient with aphemia. This case highlights the importance of attributing localization value to sequen­ tial homologous lesions of the brain that can unveil symp­ toms due to a “loss of compensation phenomenon” that we propose be termed as “FCM phenomenon.” 2019 2009 1998 2012 KEYWORDS Aphemia; Foix-ChavanyMarie syndrome; sub-insular stroke; ischemic stroke; dysarthria; anarthria The existing literature on “aphemia” has used the term synonymously with “apraxia of Speech” as well as with “anar­ thria” from FCM Syndrome, resulting in confusion. The set of seven dysarthrias (flaccid, spastic, hypokinetic, hyperkinetic, ataxic, unilateral upper motor neuron, and mixed) and AoS constitute two distinct classes of motor-speech disorders (Darley et al., 1975). Dysarthria is “a collective name for a group of neurologic speech disorders that reflect abnormal­ ities in the strength, speed, range, steadiness, tone, or accuracy of movements required for the respiratory, phonatory, resona­ tory, articulatory, or prosodic aspects of speech production.” However, AoS is defined as “a neurologic speech disorder that reflects an impaired capacity to plan or program sensorimotor commands necessary for directing movements that result in phonetically and prosodically normal speech” (Duffy, 2012, p. 4). UUMN dysarthria is further characterized by paresis and/ or spasticity of the lower face and tongue contralateral to the damaged upper motor neuron tract, harsh or hoarse vocal quality, reduced vocal intensity, and imprecise articulation CONTACT Saurav Das sauravmed@gmail.com Vascular Neurology Fellow, Washington University School of Medicine, St. Louis, MO, USA On behalf of all authors, the corresponding author states that none of the authors have any disclosures or conflicts of interest. The study did not receive any funding. All authors had access to the patient data, assisted with the manuscript preparation, and agreed with the submission of this manuscript. © 2021 Informa UK Limited, trading as Taylor & Francis Group 2 S. DAS ET AL. Figure 1. Right sub-insular diffusion restriction (A) with ADC correlation (B) representing acute ischemic stroke. T2 FLAIR hyperintensity symmetrically located in bilateral sub-insular cortex representing contralateral lacunar stroke on the left side (C). Image D shows the left sub-insular diffusion restriction on MRI obtained 2 months earlier. with irregular articulatory breakdowns (Duffy, 2012). By con­ trast, AoS that results from strokes affecting dominant premotor cortex is characterized by distorted sound substitutions and additions, syllable segmentation, increased inter-word intervals, articulatory groping, and reduced accuracy with increased utterance length and complexity (Graff-Radford et al., 2014; Duffy et al., 2014). Prosodic abnormalities in AoS are secondary to articulatory timing distortions. An overlapping characteristic of UUMN dysarthria and apraxia is slow rate of speech. Due to absence of a clear framework to approach a patient with aphemia, there is overlap in the terminology used to describe motor speech examination findings in reported cases in the literature adding to the confusion (Ogar et al., 2005). In this case report, we describe a patient with aphemia following non-dominant sub-insular stroke. The case will high­ light how a detailed neurological examination including motor speech assessment, attention to disease progression and recovery, complemented by brain imaging are important to identify underlying mechanism. We will discuss the neuroanatomical basis of the presentation, ambiguity in existing literature and propose a conceptual framework that will be useful in approaching such patients. Materials and methods A 52-year-old Caucasian female with +100 score on the Edinburgh handedness inventory, indicating complete righthandedness, presented to the emergency department around 6 hours after onset of speech difficulty and left upper extremity weakness. Her past medical history was significant for hyper­ tension, uncontrolled diabetes (A1c 11%), hyperlipidemia, and a two-month-old stroke involving the left external capsule. Her presenting symptoms during the prior stroke were right facial droop, mild dysarthria and numbness involving right upper extremity with an initial National Institute of Health Stroke Scale (NIHSS) score of 5. She was discharged on short-term dual antiplatelet therapy (with aspirin 81 mg and clopidogrel 75 mg), pantoprazole, atorvastatin 80 mg, anti-hypertensives and intensive glycemic control. The patient recovered comple­ tely without any residual deficits within a week of discharge and reported no neurological symptoms until her current pre­ sentation. She had no past psychiatric history and no recent psychological stressors reported by family. Her physical examination during day 1 of her readmission revealed complete mutism, bilateral volitional facial paresis with emotional sparing, oro-lingual weakness, and dysphagia with preserved automatic movements like yawning. She had intact comprehension and could express herself accurately by writing and drawing but was unable to phonate, mouth words, count, hum, or sing. Other reflexive speech production capa­ cities such as swearing or reciting the alphabet were not tested. The patient was frustrated by unsuccessful attempts at speech production (Video from day 2 of her hospitalization). At this time, she was unable to enact blowing air, kissing, or pressing her cheeks with her tongue. She had a mild drift in her left upper extremity. Her mood appeared euthymic from her will­ ingness to participate in physical examination, as well as from her use of humor in written communication. There were no signs of catatonia during physical examination. A magnetic resonance imaging (MRI) scan of the brain showed an area of diffusion restriction involving right external capsule and FLAIR hyperintensity in left external capsule indicating her old infarct (Figure 1). The patient was initially started on anti-coagulation due to strokes following multiple vascular territories. After negative transesophageal echocardiogram and CT angiogram of the head and neck except for mild extracranial atherosclero­ sis, she was switched back to dual anti-platelet therapy and received an implantable cardiac monitor to detect occult atrial fibrillation. During her recovery phase, she was able to swallow pureed food and phonate vowel sounds on day 4 of her hospitalization. With speech–language therapy, her speech continued to improve, such that she was able to phonate consonant sounds and bi-syllabic words over the following week. At this time, hypophonia and spastic intonation errors were noted in both propositional speech as well as non-propositional speech such as familiar songs. There was mild hoarseness of voice. However, she did not display other speech errors characteristic of AoS such as distorted sound substitutions or additions, syllable segmentation, or oral groping. Her written language was completely unaf­ fected during this period. She displayed such rapid improvement that within two weeks she was discharged from speech–language therapy services. No residual symp­ toms were observed on neurological examination at her three-month follow up visit. Cardiac monitor had not cap­ tured any atrial fibrillation. NEUROCASE Results This patient’s presentation is a good example of the clinical syndrome of aphemia. It is difficult to attribute such profound oro-facio-lingual and pharyngeal weakness to a small nondominant sub-insular stroke. A stroke in the non-dominant hemisphere is less likely to cause AoS. Additionally, during the recovery phase, this patient did not demonstrate any primary distinguishing features of AoS like distorted sound substitu­ tions or additions, or even features that may be common to AoS and dysarthria like syllable segmentation, lengthened pho­ nemes, or lengthened pauses between phonemes, syllables, words, and phrases. (Strand et al., 2014) She demonstrated intonation errors, hoarseness, etc. during the recovery phase, which are signs of underlying UUMN dysarthria that can be attributed to this patient’s unilateral sub-cortical stroke. However, UUMN dysarthria alone will be insufficient to result in such profound oro-facio-lingual and pharyngeal weakness and mutism at presentation. Therefore, we attributed localiza­ tion value to the presence of homologous sequential subinsular strokes that can cause deafferentation of brain stem nuclei and result in a FCM syndrome-like presentation due to a “loss of compensation” phenomenon. The authors propose this phenomenon be termed as “FCM phenomenon”. This patient’s final diagnosis was clinical syndrome of aphemia arising from a combination of FCM phenomenon and UUMN dysarthria. This approach is summarized in Table 1. Discussion Neuroanatomy and neuroimaging Advanced neuroimaging techniques like functional MRI scans, diffusion tensor imaging (DTI) for white matter tractography and single-photon emission computed tomography (SPECT) scans have discerned the neuro-anatomic underpinnings of these conditions. Pars opercularis of the inferior frontal gyrus is connected with insular cortex by arcuate fasciculus (AF), frontal aslant tract (FAT), and superior longitudinal fasciculus (SAF). Insula is connected to the brain stem nuclei of fifth, seventh, ninth, tenth and twelfth cranial nerves by corticobulbar tracts (Christen et al., 2000). DTI studies have shown reduced volume of these white matter tracts in patients with aphemia (Martino et al., 2012; Yoshii et al., 2019). Of note, it is thought that emotional facial movement reaches the brain stem from the amygdala and lateral hypothalamus via the inner forebrain bundle and outer longitudinal bundle. These projections were intact in previous reports of patients with aphemia (Yoshii et al., 2019). Although most reported cases of aphemia have involved bilateral lesions or left-lateralized damage to motor, premotor, frontal opercular, anterior insular, external or internal capsule, and/or subjacent subcortical areas, right-lateralized damage resulting in this phenomenon has also been attested (Duffau et al., 2003; Martino et al., 2012; Starkstein et al., 1988; Vitali et al., 2004). UUMN dysarthria could be an additional contribu­ tor to deficits in patients following right-sided lesions (Duffy, 2012). Also, brain SPECT has demonstrated bilateral hypometa­ bolism in patients with aphemia following unilateral injury (Kutluay et al., 1996). Due to close interconnectivity of these 3 brain regions, contralateral diaschisis following unilateral brain injury is also possible. Vascular anatomy The insula is buried in the sylvian sulcus. While anterior insula is supplied by branches from superior M3 division of middle cerebral artery (MCA), inferior insula is supplied by branches from inferior M3 division. The sub-insular cortex is the borderzone between three small-vessel vascular territories, namely, lenticulo-striate arteries medially, insular cortical branches of the MCA laterally and cortico-medullary penetrating arteries superiorly. Therefore, stroke etiology in this territory can be from multiple mechanisms including small vessel disease, large vessel disease and cardio-embolic etiology as well as watershed strokes following hemodynamic changes. Of note, sub-insular strokes commonly cause contralateral faciobrachio-crural, brachio-crural, or facio-brachial weakness and dysarthria like in our patient. Sensory loss and dizziness due to vestibular involvement are signs of posterior insular exten­ sion of the sub-insular stroke (Kumral et al., 2004). These signs were absent in our patient. Aphemia vs apraxia of speech Authors who have contributed to research on “aphemia” have conceded that the term is ambiguous at best. Invocations of the historical origins of the term “aphemia” may fail to resolve terminological disagreements, as it was controversial from the moment it was coined by Paul Broca in 1861 (Broca, 1861). By 1865, Armand Trousseau had already replaced it with the term “aphasia” (Tesak & Code, 2008). Schiff et al. offered arguments from the clinical profiles and CT scans of four stroke patients (two cortical, two subcortical affecting the internal capsule) in favor of aphemia being equivalent to profound dysarthria – not AoS – caused by small lesions in the articulatory motor system, specifically the left pars opercularis, ventral precentral gyrus, and/or subjacent white matter (Schiff et al., 1983). They dis­ missed the association of aphemia with AoS: “there is an overall tendency to use the term (apraxia of speech), without further clarification, as the descriptive one for any and all supra-modal motor disturbances. We favor reserving it for learned motor actions that are impaired in some settings but not in others. Within that definition, bucco-facial apraxia is transiently pre­ sent in aphemia. That there is a related apraxic motor distur­ bance underlying abnormal speech in aphemia has not been conclusively shown” (p. 726). Crucially, the work of the 19th and early 20th century pioneers of the study of the brain basis for speech and language preceded major scientific advances in the perceptual, acoustic and physiologic analyses of motor-speech disorders. AoS was not introduced as a diagnostic classification of speech sound disorder until a century later (Darley, 1968). Defined as impairment of motor-planning and motorprogramming for speech, AoS is known to localize to dominant motor and premotor areas and dominant anterior insula (Moser et al., 2016). The specific set of apraxic speech error character­ istics that distinguish them from dysarthric and phonemic para­ phasic errors has been continually refined (Strand et al., 2014). Consequently, the early work of Broca and his contemporaries are of minimal value in disentangling the causes of the disorder 4 S. DAS ET AL. Table 1. Mechanisms underlying the clinical syndrome of aphemia. Sl. Underlying mechanism of Phonatory Articulatory Intonation Errors Recovery phase Aphemia Errors Errors 1 ++ ++ ++ Protracted 2 Profound dysarthria (anarthria) from FCM syndrome Apraxia of Speech - ++ Distorted sound substitutions and additions, Slow rate, Oral groping, Prolongations (intact swallowing integrity) 3 FCM Phenomenon + + ++ secondary to articulatory errors + 4 UUMN Dysarthria + + + 5 FCM Phenomenon+ UUMN Dysarthria ++ ++ ++ 6 FCM Phenomenon+ Apraxia of Speech FCM Phenomenon+ UUMN Dysarthria+ Apraxia of Speech ++ ++ ++ ++ ++ ++ 7 Localization Simultaneous homologous lesions Dominant SMA and premotor cortex Rapid Sequential homologous lesions Dysphonia (harshness, reduced intensity, flat intonation), Unilateral UMN Slow rate, Mild dysphagia lesion (Dominant or non-dominant) Demonstrates characteristics of UUMN dysarthria after acute Unilateral UMN aphemia lesion (Dominant or non-dominant) Demonstrates characteristics of AoS after acute aphemia Dominant side lesions Demonstrates characteristics of both UUMN dysarthria and Dominant side AoS after acute aphemia lesions FCM – Foix Chavany Marie, UUMN- Unilateral Upper Motor Neuron, SMA- Supplementary Motor Area, UMN- Upper Motor Neuron; the number of “+” represents relative severity of the finding, “-” represents absence of the finding. referred to as “aphemia,” as it pre-dated advances in the science of aphasia and motor-speech disorders that inform differentiation between phonemic paraphasias, AoS, and var­ ious types of dysarthria. We propose that use of the term aphemia be restricted to the clinical syndrome of inability to speak with spared comprehension and written expression that may arise due to several causes summarized in Figure 2. These include profound AoS, anarthria of FCM syndrome, FCM phe­ nomenon (discussed subsequently) in conjunction with conco­ mitant UUMN dysarthria, or/and AoS depending upon the localization of the inciting lesion (Table 1). FCM syndrome vs FCM phenomenon Fascination with the phenomenon of severe dysarthria or anarthria resulting from deafferentation of brainstem nuclei, described as FCM syndrome, has engendered a remarkably rich literature, most notable for the heterogeneity of condi­ tions that are associated with them. Attested in the literature are cases of stroke (Fox et al., 2001; Schiff et al., 1983), hematoma from AVM (Ruff & Arbit, 1981), surgical excision of glioma (Duffau et al., 2003), and penetrating head injury (Pellat et al., 1991). The pattern of initial mutism with spared oral and written language comprehension and spared written production, followed by a period of motor-speech production recovery with specific sound errors, reveals the complex nat­ ure of the disorder. It is noteworthy that these cases of FCM syndrome used CT scans to identify large opercular lesions. However, with the advent of MRI, as in the present case, we are now able to identify subtle subcortical lesions and attri­ bute localization value to homology. While the aphemia aris­ ing from simultaneous homologous lesions is termed FCM syndrome, aphemia may also arise from sequential homolo­ gous lesions due to a loss of compensation phenomenon. The authors propose a new term for this phenomenon – “FCM Phenomenon” (Figure 2). FCM phenomenon may exhi­ bit milder speech symptoms and faster recovery (few days) when compared to complete anarthria in FCM syndrome that takes a few weeks to recover. This is possible because one of the two homologous lesions could be in recovery phase during the contralateral stroke. To rephrase, FCM phenom­ enon arises from a unilateral acute stroke in a patient with an old contralateral homologous stroke. Depending upon the laterality of the acute stroke, a concomitant speech pathology may co-exist. For example, AoS may co-exist with FCM phe­ nomenon in dominant hemispheric lesions, and UUMN dysar­ thria may co-exist with FCM phenomenon in either hemispheric lesions. This distinction may be best possible in the recovery phase (Table 1). Unilateral upper motor neuron (UUMN) dysarthria vs apraxia of speech (AoS) Speech and voice abnormalities may also occur following uni­ lateral strokes, falling into the category of UUMN dysarthria (Duffy, 2012). Some strategies for distinguishing UUMN dysar­ thria from AoS are (Strand et al., 2014): (1) Non-propositional (formulaic, overlearned, automatic) utterances and proposi­ tional (novel) utterances are equally affected in UUMN dysar­ thria, whereas in AoS, non-propositional speech should be spared relative to propositional speech, as the burden of motor planning and programming is largely lifted for formulaic, overlearned and automatic speech. (2) Hypophonia, and mono­ tone and monoloud prosody are characteristics of UUMN dys­ arthria. By contrast, AoS disrupts articulation but not phonation, and any prosodic disturbances in AoS are secondary to the articulatory timing disorder of AoS. (3) Slow rate, effortful production, phonemic distortions and selective difficulty with production of consonant blends can be associated with both UUMN dysarthria as well as AoS. Our patient was hypo-phonic, NEUROCASE 5 Figure 2. An approach to a patient with Aphemia. Symptomatology and possible mechanisms. AoS- Apraxia of Speech, UUMN- Unilateral Upper Motor Neuron, FCMFoix-Chavany-Marie. had equal impairment for both propositional and nonpropositional utterances, and had hoarseness during recovery, all indicating a co-existence of UUMN dysarthria accentuating the symptoms from FCM phenomenon. Exclusive AoS or exclusive dysarthria are rare; rather the most recurrent pattern of motor-speech impairment involves a combination of apraxic and dysarthric deficits. The cooccurrence of these deficits should not be surprising, given the proximity and inter-connectivity of neural regions sub ser­ ving motor planning and programming for speech production, direct motor control of muscles for speech production, and control of muscles involved in non-speech oro-facial move­ ments (Pellat et al., 1991; Ruff & Arbit, 1981; Schiff et al., 1983) (Figure 2). Motor speech descriptors and terminological ambiguity A few terms used in discussion of cases of aphemia reported in literature require qualification as a step to ensure uniformity in subsequent usage. (a) The use of “transient word blocking” is ambiguous. It can refer to anomia (pre-word pauses), or dys­ fluency in neurogenic stuttering, or prolongation of initial pho­ nemes and/or oral groping as seen in AoS. (b) “Staccato cadence” is an obscure description and cannot be attributed to either AoS or UUMN dysarthria. This non-technical phrase may have been erroneously applied to segmentation of pho­ nemes, syllables, words and phrases observed in both AoS and dysarthria. (c) “Phonetic disintegration” is an outdated phrase that referred to a set of sound errors now classified as apraxic errors, such as phonemic substitutions and articulation errors at word onsets, most notably with affricate and fricative classes of consonants as well as consonant blends (Darley et al., 1968). (d) “Phoneme transpositions”, schwa (neutral vowel) insertions, irregular articulatory breakdowns, assimilation errors, and repetitive attempts are more typical of AoS. (e) “Contortions” is a term not habitually employed in the field of motor speech disorders, but some authors have attributed it to AoS, likely to refer to the distorted substitutions and additions that are the hallmarks of AoS. Although some of this terminology has remained ambiguous, much confusion can be prevented with application of more rigorous categorizations of observed speech production deficits (Strand et al., 2014). Conclusion In summary, this case and previous reports of FCM syn­ drome indicate that bilateral sub-insular lesions involving the operculum to brainstem projections may result in the clinical syndrome of aphemia despite sparing the opercular cortex responsible for face and mouth control in the motor homunculus (Bakar et al., 1998). The differential diagnoses of aphemia should include FCM syndrome, its sub-cortical variant termed opercular-sub-opercular syndrome as well as dominant frontal lobe lesions. Additionally, unilateral subcortical lesions can contribute further to dysarthria termed as UUMN dysarthria in literature. AoS may be difficult to assess in the co-existence of anarthria or severe dysarthria, and the distinction may only be apparent in the recovery phase. Equivalence in impairment of propositional and nonpropositional utterances, hypophonia, impaired monotone prosody and intonation, hoarseness, are characteristics of dysarthria. Distorted sound substitutions, syllable segmenta­ tion, lengthened inter segment duration, word groping, and effortful speech are common in AoS. This case highlights the importance of attributing localization value to homolo­ gous lesions of the brain and how symptoms can unveil due to a “loss of compensation phenomenon” that the authors 6 S. DAS ET AL. propose be termed as “FCM phenomenon.” A combination of these mechanisms can coexist in the same patient dis­ playing the clinical syndrome of aphemia. Video Legend Focused neurological examination of the patient (.mp4 file). Note the patient is unable to phonate, protrude tongue, count or sing, has bilateral facial weakness sparing automatic movements like yawning, and is able to express by writing. Disclosure of potential conflicts of interest No potential conflict of interest was reported by the author(s). ORCID Saurav Das http://orcid.org/0000-0002-3010-6469 References Bakar, M., Kirshner, H. S., & Niaz, F. (1998). The opercular-subopercular syndrome: Four cases with review of the literature. Behavioural Neurology, 11 (2), 97–103. https://doi.org/10.1155/1998/423645 Broca, P. (1861). Remarques sur le siège de la faculté du langage articulé, suivies d’une observation d’aphémie (perte de la parole). Bulletins et Mémoires de la Société Anatomique de Paris, 36 (6), 330–357. Christen, H. J., Hanefeld, F., Kruse, E., Imhauser, S., Ernst, J. P., & Finkenstaedt, M. (2000). Foix-Chavany-Marie (anterior operculum) syn­ drome in childhood: A reappraisal of worster-drought syndrome. Developmental Medicine & Child Neurology, 42, 122–132. https://doi.org/ 10.1017/s0012162200000232 Darley, F. L. (1968). Apraxia of speech: 107 years of terminological confusion. Paper presented to the American speech and hearing association convention, (unpublished). Darley, F. L., Aronson, A. E., & Brown, J. R. (1968). Motor speech signs in neurologic disease. Medical Clinics of North America, 52, 835–844. https:// doi.org/10.1016/S0025-7125(16)32874-7 Darley, F.L., Aronson, A.E., & Brown, J.R. (1975). Motor Speech Disorders (1st ed.). W.B. Saunders Duffau, H., Karachi, C., Gatignol, P., & Capelle, L. (2003). Transient Foix-ChavanyMarie syndrome after surgical resection of a right insulo-opercular low-grade glioma: Case report. Neurosurgery, 53, 426–431. discussion 431. https://doi.org/10.1227/01.neu.0000073990.94180.54 Duffy, J. (2012). Motor speech disorders: substrates, differential diagnosis, and management (3rd ed.). Elsevier Health Sciences. Duffy, J. R., Strand, E. A., & Josephs, K. A. (2014). Motor speech disorders associated with primary progressive aphasia. Aphasiology, 28, 1004–1017. https://doi.org/10.1080/02687038.2013.869307 Fox, R. J., Kasner, S. E., Chatterjee, A., & Chalela, J. A. (2001). Aphemia: An isolated disorder of articulation. Clinical Neurology and Neurosurgery, 103, 123–126. https://doi.org/10.1016/s0303-8467(01)00126-3 Graff-Radford, J., Jones, D. T., Strand, E. A., Rabinstein, A. A., Duffy, J. R., & Josephs, K. A. (2014). The neuroanatomy of pure apraxia of speech in stroke. Brain and Language, 129, 43–46. https://doi.org/10.1016/j.bandl. 2014.01.004 Kirk, S. T. Check your diagnosis — patient 83 aphemia from an infarct in the left frontal operculum. Baylor College of Medicine. Retrieved April 5 from https://www.bcm.edu/neurology-apps/case_.cfm?Case= 83&Pagename=summary Kumral, E., Ozdemirkiran, T., & Alper, Y. (2004). Strokes in the subin­ sular territory: Clinical, topographical, and etiological patterns. Neurology, 63, 2429–2432. https://doi.org/10.1212/01.WNL. 0000147261.22630.F8 Kutluay, E., Colakoglu, Z., Dirlik, A., & Kumral, K. (1996). Brain SPECT in anterior opercular syndrome due to a unilateral lesion. Journal of Neurology, 243, 427–429. https://doi.org/10.1007/BF00869006 Mantyh, W. G., Chandregowda, A., Fulgham, J. R., Flemming, K. D., Laughlin, R. S., & Jones, D. T. (2019). Teaching video neuroimages: Foix-Chavany-Marie syndrome. Neurology, 92, e2620–e2621. https:// doi.org/10.1212/WNL.0000000000007569 Martino, J., De Lucas, E. M., Ibanez-Plagaro, F. J., Valle-Folgueral, J. M., & Vazquez-Barquero, A. (2012). Foix-Chavany-Marie syndrome caused by a disconnection between the right pars opercularis of the inferior frontal gyrus and the supplementary motor area. Journal of Neurosurgery, 117, 844–850. https://doi.org/10.3171/2012.7.JNS12404 Moser, D., Basilakos, A., Fillmore, P., & Fridriksson, J. (2016). Brain damage associated with apraxia of speech: Evidence from case studies. Neurocase, 22, 346–356. https://doi.org/10.1080/13554794.2016. 1172645 Ogar, J., Slama, H., Dronkers, N., Amici, S., & Gorno-Tempini, M.-L. (2005). Apraxia of speech: An overview. Neurocase, 11, 427–432. https://doi.org/ 10.1080/13554790500263529 Ottomeyer, C., Reuter, B., Jager, T., Rossmanith, C., Hennerici, M. G., & Szabo, K. (2009). Aphemia: An isolated disorder of speech associated with an ischemic lesion of the left precentral gyrus. Journal of Neurology, 256, 1166–1168. https://doi.org/10.1007/s00415-009-5055-0 Pellat, J., Gentil, M., Lyard, G., Vila, A., Tarel, V., Moreau, O., & Benabid, A. L. (1991). Aphemia after a penetrating brain wound: A case study. Brain and Language, 40, 459–470. https://doi.org/10.1016/0093-934x(91) 90143-o Ruff, R. L., & Arbit, E. (1981). Aphemia resulting from a left frontal hematoma. Neurology, 31, 353–356. https://doi.org/10.1212/WNL.31.3. 353 Schiff, H. B., Alexander, M. P., Naeser, M. A., & Galaburda, A. M. (1983). Aphemia. Clinical-anatomic correlations. Archives of Neurology, 40, 720–727. https://doi.org/10.1001/archneur.1983.0405011 0038005 Starkstein, S. E., Berthier, M., & Leiguarda, R. (1988). Bilateral opercular syndrome and crossed aphemia due to a right insular lesion: A clinicopathological study. Brain and Language, 34, 253–261. https:// doi.org/10.1016/0093-934x(88)90137-x Strand, E. A., Duffy, J. R., Clark, H. M., & Josephs, K. (2014). The apraxia of speech rating scale: A tool for diagnosis and description of apraxia of speech. Journal of Communication Disorders, 51, 43–50. https://doi.org/ 10.1016/j.jcomdis.2014.06.008 Tesak, J., & Code, C. (2008). Milestones in the history of aphasia: Theories and protagonists. Psychology Press. Vitali, P., Nobili, F., Raiteri, U., Canfora, M., Rosa, M., Calvini, P., Girtler, N., Regesta, G., & Rodriguez, G. (2004). Right hemispheric dysfunction in a case of pure progressive aphemia: Fusion of multimodal neuroimaging. Psychiatry Research: Neuroimaging, 130, 97–107. https:// doi.org/10.1016/j.pscychresns.2003.04.001 Yoshii, F., Sugiyama, H., Kodama, K., & Irino, T. (2019). Foix-ChavanyMarie syndrome due to unilateral anterior opercular damage with contralateral infarction of corona radiata. Case Reports in Neurology, 11, 319–324. https://doi.org/10.1159/000503856