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Journal of Neurolinguistics
journal homepage:www.elsevier.com/locate/jneuroling
Supplementary motor area aphasia revisited
Alfredo Ardila
Institute of Linguistics and Intercultural Communication, Sechenov University, Moscow, Russia & Psychology Doctoral Program, Albizu University, Miami, FL, USA
A B S T R A C T
Background:Supplementary motor area (SMA) plays a complex role in language. Language disturbances associated with SMA pathology have some times been named as“aphasia of the SMA”or simply“SMA aphasia”. However, this type of aphasia is extremely unusual, that it is not even included in classical aphasia classifications.
Aims:To review the involvement of the SMA in language, in order to suggest if the language disorders observed in SMA pathology should be considered as an aphasia subtype.
Methods & procedures:An extensive literature review was performed using PubMed and Google Scholar.
Outcomes & results:It was found that 45 papers refer to the speech and language disorders associated with SMA damage. Only three of them name this disorder as“aphasia”. It is reported that damage in the SMA results in both speech (posterior SMA, including speech automatization, initiation, timing control, and monitoring speech) and language disorders (pre-SMA, including working memory, word production, lexical disambiguation, context-tracking, monitoring, inhibition of erroneous language representations, and inner language).
Conclusion:Regardless of its rarity, it is evident that damage in the left SMA usually results in a clinical syndrome that clearly corresponds to aphasia. Interpreting this as an aphasia can aid in overcoming the limited idea of a“language zone”located in the perisylvian area of the left hemisphere, that was proposed over one century ago.
1. Introduction
Understanding the specific role of the supplementary motor area (SMA) in language has not been easy. The SMA is located out of the classical language area (Dejerine, 1914;Geschwind, 1970), and as a matter of fact, quite far away. Nonetheless, its involvement in language has been widely supported not only from the clinical, but also from the functional perspective (for an extensive review of the involvement of the SMA in speech and language seeHertrich, Dietrich, and Ackermann, 2016).
1.1. SMA aphasia: Clinical manifestations
Thefirst systematic clinical report of an aphasia due to damage in the SMA was presented by Rubens in 1975, that is, over one century after the classical aphasia syndromes were described. Nonetheless, Rubens considered it as a transcortical motor aphasia because of the preserved ability to repeat, and this naming has continued to be used by several authors (e.g.,Kertesz, 1979;Mendez, 2004). In this pioneer paper, Rubens described two right-handed patients with infarction in the territory of the left anterior cerebral artery presenting a transient aphasia characterized by,“(1) a striking dissociation between intact repetition and grossly disturbed spontaneous conversational speech, (2) an absence of phonemic paraphasia, (3) a lack of speech inhibition and (4) relative pre-servation of confrontation naming and comprehension. Despite the initially profound motor aphasia, serviceable spontaneous con-versational speech returned in two to three months. However, more subtle changes in the form of lack of speech initiative and difficulties in narrating stories and describing complex pictures“remained many months after the onset”(page 239).
https://doi.org/10.1016/j.jneuroling.2020.100888
Received 6 August 2019; Received in revised form 16 December 2019; Accepted 9 January 2020 E-mail address:[email protected].
0911-6044/ © 2020 Elsevier Ltd. All rights reserved.
Rubens (1975)explains that initially thefirst patient did not speak spontaneously, but responses to questions though correct consisted of one-two words answers and were marked by significant effort, false starts, and hesitations. The second patient attempted to communicate but was unable to phonate. In both patients, failures to communicate usually consisted of total inability to answer or perseverations, often with an attempt for self-correcting, resulting in embarrassment and frustration. Naming of objects in thefirst patient although in general correct, presented long latencies and some perseverations; in the second patient naming was correct at about a 60% level, with significant amount of perseverations or total inability to produce the target word. Comprehension was relatively preserved; when using“point to”tasks, answers were correct in 90% in thefirst patient and 80% in the second one. No echolalia or echopraxia was observed.
During the following decades, seemingly, only three published papers have specifically referred to the aphasia of the SMA.Pai (1999)reported a 72-year-old right-handed woman who developed aphasia associated with left SMA infarct. Cognitive deficits were in the initiation of language production. She did not speak spontaneously, but was able to answer with good articulation to questions. Confrontation naming and language repetition were normal. However, the patients had difficulties in reading aloud, writing spon-taneously, and writing to dictation.Masdeu, Schoene and Funkenstein (1978)studied a patient with a single embolic infarct of the left supplementary motor area. Language was characterized by initial mutism, rapid recovery tofluent speech marked by short sentences with normal grammar, persistent severe impairment of writing, and evident anxiety in the performance of verbal tasks. Finally,Katoh et al. (2009)report a case of subarachnoid hemorrhage associated with supplementary motor aphasia. A 52-year-old woman presented a sudden headache. CT scans demonstrated subarachnoid hemorrhage. Fourteen years earlier she had undergone neck clipping of a left vertebral artery aneurysm for subarachnoid hemorrhage. She, then, underwent a new neck clipping of the anterior communicating artery aneurysm. The postoperative course was uneventful and aphasia had disappeared in four weeks. Ardila (1983)reported two cases of damage in the left SMA resulting from tumors, not in a journal paper, but in a conference presentation; the observed language characteristics were basically equivalent to those described by Rubens.
The general clinical characteristics of this aphasia subtype could be summarized in the following way (Ardila, 2014): (1) there is an initial mutism lasting about 2–10 days; (2) later, a virtually total inability to initiate and maintain speech is observed, (3) however, nearly normal speech repetition is evident, (4) language understanding is close to normal, and (5) no echolalia is found. Because these patients have significant difficulties in initiating speech, sometime naming is impossible. Furthermore, due to the speech production difficulties, some phonological paraphasias can be found, resulting in naming errors. It can be conjectured that naming actions should be more impaired than naming objects, but no specific information to support this assumption is currently available. Language understanding for conversational language is normal, but difficulties may be found in complex grammatical sentences (Ardila and Lopez, 1984). A right leg paresis and right leg sensory loss are observed; a mild right shoulder paresis and Babinski sign are also generally found. Language recovery is outstanding and it is usually observed during the following few weeks or months.Table 1is a summary of the basic language characteristics: spontaneous language is limited, but language understanding and language repetition are normal; there is a significant difficulty in initiating and maintaining speech, regardless that the patient makes significant effort to speak; reading aloud is defective, but reading understanding is nearly normal; writing is slow and painstaking.
Right leg hemiparesis represents the most important neurological abnormality. Frequently, an extension of the pathology toward the parietal lobe is found, and hence, some right leg sensory loss is also observed.Table 2is a summary of the associated neurological signs in SMA aphasia.
1.2. SMA and motor control
The SMA has a fundamental role in motor activity, related to the initiation on one hand, and time control, on the other, of motor acts (Hertrich et al., 2016; Nachev, Wydell, O’neill, Husain, & Kennard, 2007; Tanji & Shima, 1994). It is also involved in the automatization of the motor acts and in the planification of actions (Pilgramm et al., 2016). The SMA is particularly active during bimanual movements (Naito, Morita, & Amemiya, 2016), and hence, it is involved in bimanual coordination. Some other motor functions have also been related to the SMA, such as sequence processing (Cona & Semenza, 2017) and modulation of interhemi-spheric interactions during movement preparation (Welniarz et al., 2019). Noteworthy, SMA damage is associated with slow reaction time (Alexander, Stuss, Picton, Shallice, & Gillingham, 2007).
1.3. SMA and cognition
It has been suggested that SMA has a close connectional relationship with the prefrontal cortex and plays a critical role in the
Table 1
Basic language characteristics in SMA aphasia (taken fromArdila, 2014).
Conversational Language Sparse, effortful Language comprehension Normal
Repetition Good to normal
Pointing Normal
Naming Mildly abnormal
Reading: Aloud Defective
updating of verbal representations (Tanaka, Honda, & Sadato, 2005). Neuroimaging studies in humans have demonstrated that the SMA is active when performing various cognitive tasks, such as spatial working memory (Jonides et al., 1993), verbal working memory (Paulesu, Frith, & Frackowiak, 1993), arithmetic tasks (Dehaene et al., 1996;Hanakawa et al., 2002), spatial mental imagery (Mellet et al., 1996), spatial attention (Simon et al., 2002), and word production (Alario, Chainay, Lehericy, & Cohen, 2006). Consequently, the SMA is involved in a variety of not only motor, but also cognitive tasks. Moreover, the anterior and posterior segments seem to be involved in different types of activities (Chung, Han, Jeong, & Jack, 2005). Hence, different SMA sub-areas with different functions may be recognized.
It has been proposed that two different sub-areas can be distinguished in the SMA: (1) pre-SMA, including the mesial frontal cortex rostral to the anterior commissure; it corresponds to Brodmann area BA6 and partially BA8; (2) SMA proper, which is the mesial extension of BA6, caudal to the anterior commissure. Thefirst sub-area seems to be more cognitive. Specifically, it seems involved in higher-order cognitive functions such as lexical disambiguation; the second one is more related to motor control (Hertrich et al., 2016). Furthermore, the SMA represents a crucial area in coordinating the cortical motor zones with other motor related structures, such as the basal ganglia, the cerebellum, and also the thalamus. It receives information from the posterior parietal and frontal association areas, and projects to different brain regions, including the primary motor cortex (Kandel, Schwartz, & Jessell, 1995). Five main connections have been identified in both postmortem dissections and tractography reconstructions:“(1) U-fibres running in the precentral sulcus, connecting the precentral gyrus and the SMA; (2) U-fibres running in the cingulate sulcus, con-necting the SMA with the cingulate gyrus; (3) frontal‘aslant’fascicle, directly connecting the SMA with the pars opercularis of the inferior frontal gyrus; (4) medialfibres connecting the SMA with the striatum; and (5) SMA callosalfibres”(Vergani et al., 2014, p. 1377). Good concordance was observed between postmortem dissections and diffusion tractography.Fig. 1illustrates the location and major connections of the SMA.
1.4. Involvement of the SMA in speech and language
The role of the SMA in motor coordination seems evident, but its role in speech and language control has not been easy to pinpoint. It has been proposed that the SMA seemingly plays a fundamental role in speech automatization, initiation, and timing
Table 2
Associated neurological signs in SMA aphasia (taken fromArdila, 2014).
Motor system Hemiparesis right leg
Articulation Mild defects
Cortical sensory function Right leg sensory loss
Praxis Normal
Visualfield Normal
Visual gnosis Normal
control, as well as monitoring speech and task switching (Hertrich et al., 2016). The linguistic role has been reported to be parti-cularly related to the anterior part of the SMA (pre-SMA) and includes aspects such as“lexical disambiguation, context-tracking, monitoring, or inhibition of erroneous language representations”(Hertrich et al., 2016, p. 603). Simply speaking, the pre-SMA seems to be more language-related, whereas the SMA proper is apparently more speech-related.
The interest in the potential role of the SMA in linguistic processes began toward the middle 20th century. At this historical moment, major aphasia classification systems had been already proposed (e.g.,Goldstein, 1948;Head, 1926;Luria, 1947/1970; Wernicke, 1874) but none of them included the SMA as a language-related area, or referred to an aphasia associated with damage of the SMA. In1940, Brickner reported that electro-cortical stimulation of SMA resulted in continuous perseveration, suggesting its involvement in speech. Some time later,Arseni and Botez (1961)reported speech disturbances caused by tumors of the SMA.Jonas (1981)referred to the participation of the SMA in speech emission. During the following years, a diversity of papers reporting speech and language-related abnormalities associated with left SMA pathology were published (e.g.,Ardila, 1983;Pai, 1999;Ziegler, Kilian, & Deger, 1997). Later, with the introduction of the contemporary neuroradiological techniques, it was also observed that SMA becomes activated in a diversity of language tasks, such as word production (Alario et al., 2006).
Furthermore, from a evolutionary perspective,MacNeilage (1998)proposed that the syllable“frames”and content components of speech probably evolved into separate realizations within two motor control systems: (a) a motivation-related medial“intrinsic” system, including the anterior cingulate cortex and the SMA, responsible for ancestral vocalization control and currently also re-sponsible for frames, and (b) a lateral“extrinsic”system, including Broca's area and surrounding regions, as well as Wernicke's area, which are involved in response to external input and are more responsible for content. Hence, SMA is clearly involved in speech.
Brendel et al. (2010)suggested that the brain network of speech motor control can be subdivided into at least three functio-nal–neuroanatomical subsystems: (a) thefirst one is involved in planning movement sequences, and relates to the premotor ven-trolateral–frontal cortex as well as the anterior insula, (b) the second one participates in preparedness for as well as initiation of verbal utterances; this system is based in the SMA; andfinally (c) execution of the motor act, which depends on the corticobulbar system, but also on the basal ganglia and the cerebellum. The fundamental role of the SMA would be related to planning and initiating speech.
After reviewing the available evidence regarding the involvement of the SMA in speech and language processing,Hertrich et al. (2016) concluded that its contribution refers to the use of inner speech mechanisms during language encoding, lexical dis-ambiguation, syntax, and prosody integration, andfinally, context-tracking. Other speech-related abnormalities observed in SMA pathology include“foreign accent syndrome”(Berthier et al., 2015) and speech dysfluency (Alm, 2011). Furthermore, it has been suggested that stuttering can be understood as a type offluency disorder due to abnormal connectivity between the SMA and the basal ganglia (Lu et al., 2010). It should be emphasized that the SMA has a direct monosynaptic connection with the lateral inferior frontal gyrus (Broca's area) that is known as“frontal aslant tract” (Dick, Garic, Graziano, & Tremblay, 2018). Hence, it is not surprising tofind not only motor speech disturbances, but also language abnormalities (aphasia) in cases of SMA pathology. It has been further proposed that this frontal aslant tract underlies speechfluency abnormalities in persistent developmental stuttering (Kronfeld-Duenias, Amir, Ezrati-Vinacour, Civier, & Ben-Shachar, 2016;Neef, Anwander, & Friederici, 2015).
Consequently, it seems evident that the SMA should be included in the brain language area (Ardila, Bernal, & Rosselli, 2016; Binder et al., 1997;Riecker, Brendel, Ziegler, Erb, & Ackermann, 2008). Nonetheless, most classifications of aphasia syndromes do not include the language disturbances associated with SMA pathology. Probably the only classification overtly recognizing the aphasia of the SMA isArdila's (2010)classification of aphasia syndromes. Furthermore, even the largest series of aphasia patients reported in the literature does not include the aphasia of the SMA subtype (e.g.,Lahiri et al.,unpublished;Pedersen, Vinter, & Olsen, 2004).
Reviewing the literature about the speech and language disturbances observed in SMA pathology, it is found that the term “aphasia”is ocassionaly used to refer to these language disturbances (e.g.,Katoh et al., 2009; Masdeu, Schoene, & Funkenstein, 1978; Pai, 1999). More frequently however, it is not used (e.g.,Chivukula, Pikul, Black, Pouratian, & Bookheimer, 2018;Hertrich et al., 2016;Krainik et al., 2003), the latter suggesting that, regardless of evident language disturbances associated with SMA pathology, these disturbances should not be named as“aphasia”, probably because they do not really correspond to the classically recognized aphasia syndromes.
1.5. Is there an aphasia of the supplementary motor area?
Penfield and Welch (1951) observed arrest of speech associated with stimulation of this cortical region. However, language disturbances associated with SMA pathology were reported relatively late in the aphasia literature. Clinical characteristics of this type of aphasia were only described during the 1970s byRubens (1975,1976); he assumed that these language disturbances correspond to a transcortical aphasia (TMA), considering the preserved repetition. This point of view has been shared up to-date by different authors (e.g.,Alexander & Schmitt, 1980;Kertesz, 1979;Mendez, 2004).Ardila and Lopez (1984), however, proposed that this type of aphasia was different from the prefrontal transcortical motor aphasia (Berthier, 1999), and represents quite a different syndrome, not only from the anatomical but also from the clinical point of view.Table 3presents the similarities and differences between the transcortical motor aphasia and the aphasia of the SMA.
are observed in the SMA aphasia, but not in transcortical motor aphasia. Additionally, it has been proposed that the SMA plays a basic role in speech automatization, initiation, and timing control (Hertrich et al., 2016). These are not characteristics of the transcortical motor aphasia, which is generally associated with left prefrontal pathology, and hence, disturbances in executive functions. Ac-cording toHertrich et al. (2016)the contribution of the SMA to language refers to use of inner speech mechanisms during language encoding, and also lexical disambiguation, syntax, prosody integration, andfinally, context-tracking. Furthermore, both types of aphasia–transcortical motor aphasia and SMA aphasia–are due to quite different neuroanatomical substrates: transcortical motor aphasia is due to prefrontal pathology, whereas the SMA is a pre-motor area.
Ardila (2010)proposed that the SMA aphasia does not represent a“primary”(or“central”) aphasia, but–together with con-duction aphasia—it is a“secondary”(or“peripheral”) aphasia. The language system is not impaired, but the mechanisms of language production. Transcortical motor aphasia was interpreted, on the other hand, as a“dysexecutive aphasia”, resulting from a defect in the executive control of the language.
Freedman, Alexander, and Naeser (1984)proposed that transcortical motor aphasia is due to disruption of connections between the supplementary motor area and the frontal perisylvian speech area. If the lesion is extended, poor articulation, impaired auditory, or stuttering can be observed. These authors assume that this explanation potentially can unify three syndromes: classical trans-cortical motor aphasia, the language disturbances observed after left medial frontal infarction, and transtrans-cortical motor aphasia during recovery from Broca's aphasia. In a certain way, they are anticipating that a tract connecting the supplementary motor area and the Broca's area should be responsible for the language abnormalities associated with SMA damage. This recently described connection is known as“frontal aslant tract”(Dick et al., 2018).
Clinical reports of speech and language disturbances associated with SMA pathology are limited and usually they are single case reports. The only exception to this is probablyKrainik et al.’s (2003)paper that reported 12 patients undergoing surgical resection of medial frontal lesions; six of them presented speech disorders characterized by a global reduction in spontaneous speech, ranging from a complete mutism to a less severe speech reduction; this defect recovered within a few weeks or months. The occurrence of the deficit was related to the resection the left SMA.
Furthermore, the clinical diagnosis of “SMA aphasia” is extremely unusual (Ardila, 2017). According to the Director of the “Fundación Argentina de Afasia”(Argentinian Aphasia Foundation), out of the several hundred patients they have received during the last 30 years, none have ever had this diagnosis (Silvia Rubio-Bruno, personal communication). In my personal experience, amid over 10 years at the Neurological Institute of Colombia, out of over 2000 aphasia patients, I only witnessed three patients with SMA aphasia.
There are several possibilities potentially accounting for the rarity of the diagnosis“aphasia of the SMA”: (1) the two major etiologies of aphasia of the SMA are cerebrovascular accidents of the left anterior cerebral artery and brain tumors. Cerebrovascular accidents of the anterior cerebral artery are extremely rare, and represent only 0.3%–4.4% of the total number of strokes (Kang & Kim, 2008;Kumral, Bayulkem, Evyapan, & Yunten, 2002). Tumors in this area are usually gliomas (Russell & Kelly, 2003;Satoer, Kloet, Vincent, Dirven, & Visch-Brink, 2014); (2) because SMA is not included in most aphasia classifications, it tends to overlook or simply avoid the term“aphasia in its description; as a matter of fact, a language disorder is frequently reported and acknowledged, but the disorder is not labeled as“aphasia”(e.g.,Ziegler et al., 1997); and (3) because the language defect tends to rapidly recover, it may be assumed that it is not a“real”aphasia, but just a transient language disorder. Most likely, the reason for such a low diagnosis of“aphasia of the SMA”or“SMA aphasia”is a combination of these three factors.
According to PubMed and Scholar Google, only three published papers overtly refer to the SMA aphasia, out of several thousands of papers reporting aphasic disturbances.
1.6. Why does aphasia spontaneously and rapidly dissapear?
Since the initial reports about language disturbances associated with SMA pathology (e.g.,Rubens, 1975), it has been observed that language recovery is fast, usually taking weeks or months. This is a most important observation to understand the underlying mechanisms of the type of aphasia. It suggests the possibility that other brain areas assume the SMA functions; or, as observed in general with aphasia rehabilitation, that the contralateral right area assumes the functions of the damaged left SMA (Coppens & Table 3
Similarities and differences between the transcortical motor aphasia and the aphasia of the supplementary motor area (adapted fromArdila & Lopez, 1984).
Transcortical Motor Aphasia SMA Aphasia
Conversational speech Patient does not try to communicate Patientdoestry to communicate Speech speed Close to normal Considerably decreased
Grammar Appropriate Appropriate
Articulation Normal Effortful
Phonemic paraphasias Absent Sometimes
Language comprehension Relatively normal Relatively normal
Repetition Good Some phonemic paraphasias
Naming Some mistakes due to perseveration Close to normal
Patterson, 2017). This rapid recovery has been extensively documented (e.g.,Krainik et al., 2003,2004). The aslant tract connecting the SMA with the Broca's area may at least partially account not only to the language defects observed in cases of damage of the SMA but also to the rapid recovery of aphasia, considering that there is a crossed frontal aslant tract (Baker et al., 2018).
In the aphasia of the SMA, typically an initial speech reduction and even mutism is observed; recovery is initially fast, and progressively slower; some long-term reduction in spontaneous speech can be observed. It has been suggested that the rapid recovery can be due to the fact that there are bilateral projections traversing the periventricular white matter, and controlling the left lateral frontal cortex. Because of being bilateral, it could explain the successful functional compensation (Alario et al., 2006).Baker et al. (2018)explicitaly refer to the crossed frontal aslant tract as a possible pathway involved in the recovery of SMA aphasia.
Chivukula et al. (2018)studied two patients with tumors in the left SMA. Thefirst patient underwent resection of an astrocytoma and presented mutism postoperatively, with a full recovery 14 months later. fMRI 32 months after the surgery demonstrated a migration of speech SMA to homologous contralateral hemispheric regional tissue. The second patient had an oligodendroglioma in the left SMA, and postoperatively experienced long latency and poorfluency associated with speech hesitancy, which gradually resolved over 18 months. fMRI performed at 64 months after surgery also demonstrated a reorganization of speech SMA to the contralateral hemisphere.
2. Conclusions
Regardless of the limited amount of reports, and its rapid recovery, it is evident that damage in the left SMA is typically associated with a significant, not only speech, but also language disorder. There is no reason to consider that this language disorder is not a real aphasia, even though the major defect can be found at the level of speech production. Rarity is not a reason to ignore it. For instance, so-called“mixed transcortical aphasia” is also extremely rare (Berthier, 1999), and has not only attracted an immense interest (Raymer & Rothi, 2017), but is also considered to significantly contribute to the understanding of the brain organization of language. Furthermore, interpreting this disorder as an aphasia can aid in overcoming the limited and“old-fashioned”idea of a“language zone”located in the perisylvian area of the left hemisphere, that was proposed over one century ago (Dejerine, 1914). Contemporary interpretation of the brain organization of language tend to refer to brain circuits or brain systems, involving diverse cortical and also subcortical areas (e.g.,Ardila et al., 2016;Tremblay and Dick, 2016).
Appendix A. Supplementary data
Supplementary data to this article can be found online athttps://doi.org/10.1016/j.jneuroling.2020.100888.
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