Behavioural Neurology

Behavioural Neurology / 2014 / Article

Research Article | Open Access

Volume 2014 |Article ID 230578 | 8 pages | https://doi.org/10.1155/2014/230578

Syntactic Comprehension in Patients with Amyotrophic Lateral Sclerosis

Academic Editor: Frederic Blanc
Received22 Aug 2012
Revised16 Feb 2013
Accepted18 Feb 2014
Published06 Apr 2014

Abstract

Recent neuropsychological studies of patients with amyotrophic lateral sclerosis (ALS) have demonstrated that some patients have aphasic symptoms, including impaired syntactic comprehension. However, it is not known if syntactic comprehension disorder is related to executive and visuospatial dysfunction. In this study, we evaluated syntactic comprehension using the Syntax Test for Aphasia (STA) auditory comprehension task, frontal executive function using the Frontal Assessment Battery (FAB), visuospatial function using Raven’s Coloured Progressive Matrices (RCPM), and dementia using the Hasegawa Dementia Scale-Revised (HDS-R) in 25 patients with ALS. Of the 25 patients, 18 (72%) had syntactic comprehension disorder (STA score < IV), nine (36%) had frontal executive dysfunction (FAB score < 14), six (24%) had visuospatial dysfunction (RCPM score < 24), and none had dementia (HDS-R score < 20). Nine of the 18 patients with syntactic comprehension disorder (50%) passed the FAB and RCPM. Although sample size was small, these patients had a low STA score but normal FAB and RCPM score. All patients with bulbar onset ALS had syntactic comprehension disorder. These results indicate that it might be necessary to assess syntactic comprehension in patients with bulbar onset ALS. The implications of these findings are discussed in relation to the pathological continuum of ALS.

1. Introduction

Amyotrophic lateral sclerosis (ALS) has historically been considered a neurodegenerative disease characterized by the progressive involvement of upper and lower motor neurons at the bulbar and spinal level. However, the consensus criteria have changed, and ALS is now considered a multisystem disorder in which motor system deficits are prominent but nonmotor deficits can also be observed [1]. Phukan et al. [2] reported that, of 160 patients with ALS, 14% fulfilled the Neary criteria for frontotemporal dementia, 21% had executive dysfunction without dementia, and 14% had cognitive impairment without dementia or executive dysfunction.

The frontal lobe contributes to executive function, language function, and elementary motor function. Executive function refers to higher-level cognitive functions that contribute to the control and direction of lower-level functions such as language, cognition, behavior, and memory [3]. There have been many reports of executive function in patients with ALS, and they have consistently shown that fluency, set-shifting, attention, inhibition, and working memory are impaired [46].

Patients with motor neuron disease (MND) and ALS also exhibit language dysfunction, including aphasic symptoms, such as Broca’s aphasia, due to frontal lobe deterioration [711]. A Japanese account written by Watanabe described paragraphia of an aphasic nature in bulbar onset ALS [12, 13]. In Japan, there were some other reports about writing errors in patients with ALS [1417]. Cobble [18] assessed nine MND patients on a range of standardized language assessments and found deficits on tasks involving naming, auditory comprehension of complex sentences, semantics, and spelling. In particular, there was a highly significant difference in the auditory comprehension of complex sentences between MND patients and healthy control subjects. Indeed, there are several reports of syntactic comprehension disorder in patients with MND [1921]. Bak et al. [20] reported that five of six patients with MND had impaired syntactic comprehension, and comprehension of verbs was consistently more impaired than that of nouns. Postmortem examination confirmed the clinical diagnosis of MND-dementia in three of these patients, and the verb disadvantage was associated with prominent pathological changes in Brodmann areas 44 and 45 (Broca’s area). It is known that the inferior frontal gyrus (Broca’s area) is important for syntactic comprehension [22, 23], and it has been suggested that a neural network including the parietal-temporal region may also be important [24, 25].

Bak et al. [20] reported that visuospatial skills, tested through copying drawings and the visual object and space perception battery, were relatively well preserved in MND, and Neary et al. [26] reported that spatial disorder was absent in three of four MND patients, including two with advanced disease.

Despite these reports, it remains unclear how syntactic comprehension disorder is related to executive and visuospatial dysfunction in ALS. The purpose of this study was to investigate the prevalence and profile of syntactic comprehension in ALS and to investigate the relation of syntactic comprehension with executive and visuospatial function. In addition, single-photon emission computed tomography (SPECT) was performed for two patients to investigate the pathological continuum of ALS.

2. Methods

2.1. Participants

Seventy-five Japanese ALS patients visited the Department of Speech Therapy at Kitasato University East Hospital from May 1, 2010, to August 31, 2011. All fulfilled the El Escorial criteria for definite ALS [27]. Exclusion criteria included past history of neurological, psychiatric, or mental disorder, including schizophrenic disorder and manic-depressive psychosis. Patients were also excluded if they had dysarthria or upper limb impairments that were severe enough to prevent completion of the neuropsychological assessments. There were only 25 patients from the total of 75 who met the inclusion criteria (Figure 1). Patients gave informed consent according to the Helsinki Declaration and the Ethics Committee at Kitasato University School of Medicine approved this study.

2.2. Patient Characteristics

Patients were classified with bulbar, upper limb, or lower limb onset ALS by a neurologist according to self-reported initial symptoms. Subscales of the Japanese version of the revised ALS functional rating scale (ALSFRS-R) [28] were used to estimate the severity of dysarthria (ALSFRS-R1, speech subscale) and upper limb impairments (ALSFRS-R5a, cutting food and handling subscale).

2.3. Neuropsychological Assessment

We evaluated syntactic comprehension, frontal executive function, visuospatial function, and dementia in all patients. Each of the tests used is characterized by brevity and was selected to minimize the burden on participants.

Syntactic Comprehension. There is a hierarchy of syntactic comprehension in patients with aphasia, not only in English-speaking countries but also in Japan [2931]. We evaluated syntactic comprehension using the Test of Syntactic Processing in Aphasia (Syntax Test for Aphasia; STA) [32], which was designed to assess syntactic aspects of language in patients with aphasia in Japan. The STA consists of an auditory comprehension task, a reading comprehension task, and a sentence production task. We used only the auditory comprehension task, which is designed to assess comprehension of active and passive sentences with regular and nonregular word order and to determine the use of word meaning, word order, or particles.

The STA auditory comprehension task includes four levels, with eight sentences in each level. Level I consists of nonreversible, active sentences with regular word order; Level II consists of reversible, active sentences with regular word order; Level III consists of reversible, active sentences with regular and nonregular word order; and Level IV consists of reversible, passive sentences with regular and nonregular word order (Table 1).


LevelStrategyDefinitionSample of Japanese (English)

IThe meaning of a wordNonreversible, active sentences in regular word order otokonoko (n) ga (p) aruiteiru (v)
(The boy is walking.)
okasan (n) ga (p) teburu (n) wo (p) fuiteiru (v)
(The mother is wiping the table.)

IIThe word orderReversible, active sentences in regular word orderonnanoko (n) ga (p) otosan (n) ni (p) purezento (n) wo (p) ageteiru (v)
(The girl is giving a present to the father.)
okasan (n) ga (p) otokonoko (n) wo (p) ositeiru (v)
(The mother is pushing the boy.)

IIIThe particle without complementizerReversible, active sentences in regular and nonregular word orderotousan (n) wo (p) onnanoko (n) ga (p) ositeiru (v)
(The father is pushed by the girl.)
otousan (n) ga (p) onnanoko (n) wo (p) ositeiru (v)
(The father pushed the girl.)

IVThe particle with complementizerReversible, passive sentences in regular and nonregular word order otosan (n) ga (p) onnanoko (n) ni (p) rinngo (n) wo (p) moratteiru (v)
(The father is given an apple from the girl.)
otosan (n) ni (p) onnanoko (n) ga (p) rinngo (n) wo (p) moratteiru (v)
(The girl is given an apple from the father.)

(n): noun; (v): verb; (p): particle.

For each sentence, patients are presented with four to six pictures and are required to point to the picture that corresponds to the sentence read by the examiner. Seven sentences within a level have to be answered correctly to pass that level. Failure to pass all four levels (STA score < IV) was classed as failure of the STA auditory comprehension task and was considered indicative of syntactic comprehension disorder.

In Japanese grammar, particles are short words that follow the modified noun, verb, or adjective and can indicate various functions and meanings within a sentence. Some particles are equivalent to English prepositions, but others have a unique usage that is not found in English. For example, the sentences in Level III (Table 1) show that substitution of particles such as “ga” and “wo” makes reversible meaning.

Frontal Executive Function. The Frontal Assessment Battery (FAB) is a short battery of tests that assess frontal executive function [33]. It has six subtests: conceptualization, mental flexibility, motor programming, sensitivity to interference, inhibitory control, and environmental autonomy. Terada et al. reported that the mean ± standard deviation total score for normal healthy adults (mean age, 64.4 ± 8.3 years) was 14.7 ± 1.3 [34]. Therefore, a score less than 14 out of 18 was classed as failure of the FAB test and was considered indicative of frontal executive dysfunction.

Visuospatial Function. Raven’s Coloured Progressive Matrices (RCPM) are a standardized tool for both geriatric and pediatric populations [35] and were used to assess visuospatial function. In RCPM, patients are required to select one picture out of six that is the same in pattern. We used three picture sets (A, AB, and B) that each included 12 pictures, for a total of 36 pictures. A score of less than 24 out of 36 was classed as failure of the RCPM test and was considered indicative of visuospatial dysfunction. The RCPM requires the ability to analyze color, form, and linear slope. These visual processing tasks take place in different subdivisions of the visual association areas (primarily the occipital lobe) [36].

Dementia. The Hasegawa Dementia Scale-Revised (HDS-R) is a screening test for patients with dementia in Japan that is similar to Mini-Mental State Examination and correlates well with Mini-Mental State Examination [37]. A score of less than 20 out of 30 was classed as failure of the HDS-R and considered indicative of dementia.

2.4. Neuroimaging

In two patients (patients 7 and 22) who had consented to go through neuroimaging test in writing, we performed 123I-isopropyl amphetamine SPECT (IMP-SPECT). Both patients selected for IMP-SPECT had similar clinical characteristics: they were both women aged between 70 and 80 years with upper limb onset ALS. The disease duration was between 1 and 2 years. Regional cerebral blood flow (r-CBF) was assessed using three-dimensional stereotactic surface projection.

2.5. Statistical Analysis

Relations between syntactic comprehension (STA auditory comprehension score), frontal executive function (FAB score), visuospatial function (RCPM score) and demographic variables (age, disease duration, severity of dysarthria (ALSFRS-R1 score), and severity of upper limb impairment (ALSFRS-R5a score) were assessed using Pearson’s correlation. Correlations among the neuropsychological tests (STA auditory comprehension, FAB, RCPM, and HDS-R) were calculated with Spearman rank correlation coefficient. All analyses were performed using SPSS version 10.0 J software for Windows. Data are presented as mean ± standard deviation unless otherwise stated.

3. Results

3.1. Patient Characteristics

Results are presented from 25 patients (16 men, 9 women) aged 67.9 ± 9.0 years. Disease duration was 23.9 ± 15.5 months (range, 6–61 months). The ALSFRS-R1 score was 3.5 ± 0.8 and the ALSFRS-R5a score was 3.6 ± 0.5. Eleven patients were classified with bulbar onset ALS, 10 with upper limb onset ALS, and four with lower limb onset ALS. The clinical and neuropsychological characteristics of patients are summarized in Table 2.


Patient
number
Age
(years)
GenderhandednessSubtypeDisease duration (months)ALS FRS-R1
score
ALS FRS-R5a score HDS-R
score
STA achieved
highest stage
FAB
score
RCPM
score

153FRSpinal (u)413430IV1830
279FRSpinal (l)63329IV1627
361MRSpinal (u)244330IV1735
459MRSpinal (l)594330IV1832
548MRSpinal (u)324330IV1732
650MRSpinal (l)94430IV1833
774FRSpinal (u)213329IV1627
873MRSpinal (u)244329III1830
974MRBulbar184422III1630
1074MRSpinal (l)124428III1634
1174MRBulbar104428III1734
1268MRBulbar144328III1730
1359MRSpinal (u)334330III1636
1471MRBulbar94430III1729
1571MRBulbar612427III1634
1673FLBulbar202429III1431
1775FRBulbar263429II1125
1863FRBulbar464323III1326
1972MRBulbar102430II1125
2068FRSpinal (u)104425III1324
2159FRSpinal (u)114425II1218
2275FRSpinal (u)134326I1124
2382MRBulbar413422III1224
2473MRBulbar282423I823
2569MRSpinal (u)204421I514

Average67.923.93.53.627.3 14.428.2
SD9.0    15.50.80.53.0  3.55.4

ALS FRS-R: revised amyotrophic lateral sclerosis functional rating scale; HDS-R: Hasegawa Dementia Scale-revised; STA: Syntax Test for Aphasia; FAB: Frontal Assessment Battery; RCPM: Raven’s Coloured Progressive Matrices; R: right; L: left; (u): upper limb; (l): lower limb.

3.2. Neuropsychological Assessment

Eighteen out of the 25 patients (72%) failed to complete all four levels of the STA auditory comprehension task (score < IV; Table 2) and were classed as having syntactic comprehension disorder. Of the 18 patients, 12 (66.8%) failed to comprehend reversible, passive sentences with regular and nonregular word order and were classed at level III. Three (16.6%) of the 18 patients failed to comprehend reversible, active sentences with regular and nonregular word order and were classed at level II. Other 3 (16.6%) of the 18 patients failed to comprehend reversible, active sentences with regular word order, and were classed at level I. There were more errors for reversible sentences than for nonreversible sentences, and more errors for passive sentences than for active sentences. The FAB score was 14.4 ± 3.5 (range, 4–18). Nine out of the 25 patients (36%) failed the FAB (score < 14; Table 2) and were classed as having frontal executive dysfunction. The RCPM score was 28.2 ± 5.4 (range, 14–36). Six out of the 25 patients (24%) failed the RCPM (score < 24; Table 2) and were classed as having visuospatial dysfunction. Mean HDS-R score was 27.3 ± 3.0, which is within normal limits. No patient scored less than 20 on the HDS-R; therefore, no patients were classed as having dementia (Table 2). Of the 18 patients who failed the STA auditory comprehension task, nine (50%) also failed the FAB and six (33%) failed both the FAB and the RCPM.

Patients were divided into four groups (Table 3). Group A passed all four tests (); Group B failed the STA auditory comprehension task but passed the FAB, the RCPM, and the HDS-R (); Group C failed the STA auditory comprehension task and the FAB but passed the RCPM and the HDS-R (); and Group D failed the STA, the FAB, and the RCPM (). Of the seven patients in Group A, four had upper limb onset ALS and three had lower limb onset ALS. Of the nine patients in Group B, one had upper limb onset ALS, two had lower limb onset ALS, and six had bulbar onset ALS. All three patients in Group C had bulbar onset ALS. Of the six patients in Group D, four had upper limb onset ALS and two had bulbar onset ALS. All patients with bulbar onset ALS failed the STA auditory comprehension task (Table 3).


GroupInitial symptoms
Upper limbLower limbBulbar

A (STA+, FAB+, RCPM+)430
B (STA−, FAB+, RCPM+)216
C (STA−, FAB−, RCPM+)003
D (STA−, FAB−, RCPM−)402

STA: Syntax Test for Aphasia; FAB: Frontal Assessment Battery; RCPM: Raven’s Coloured Progressive Matrices; +: pass, −: failure.

The scores on the STA auditory comprehension task, the FAB, and the RCPM were not correlated with age, disease duration, ALSFRS-R1 score, or ALSFRS-R5a score (Table 4). The STA auditory comprehension score had strong positive correlation with the FAB score (, ) but moderate positive correlation with the RCPM score (, ), and the FAB score also showed strong positive correlation with the RCPM score (, ) (Table 5).


Pearson’s correlation

Age
 STA score−0.390
 FAB score−0.311
 RCPM score−0.258
Disease duration
 STA score0.199
 FAB score0.123
 RCPM score0.210
ALSFRS-R1 score
 STA score0.168
 FAB score0.258
 RCPM score0.087
ALSFRS-R5a score
 STA score−0.332
 FAB score−0.348
 RCPM score−0.251

ALS FRS-R: revised amyotrophic lateral sclerosis functional rating scale; STA: Syntax Test for Aphasia; FAB: Frontal Assessment Battery; RCPM: Raven’s Coloured Progressive Matrices.

rsP value

STA score
 FAB score0.791<0.05
 RCPM score0.600<0.05
 HDS-R score0.574<0.05
FAB score
 RCPM score0.734<0.05
 HDS-R score0.637<0.05
RCPM score
 HDS-R score0.565n.s.

STA: Syntax Test for Aphasia; FAB: Frontal Assessment Battery; RCPM: Raven’s Coloured Progressive Matrices; HDS-R: Hasegawa Dementia Scale-revised; n.s.: not significant.

3.3. Neuroimaging

Patient 7 passed all four levels of the STA auditory comprehension task and passed the FAB, the RCPM, and the HDS-R (Group A). IMP-SPECT revealed that she had mildly reduced r-CBF in the bilateral frontal lobes. Patient 22 passed the HDS-R but failed the STA auditory comprehension task, the FAB, and the RCPM (Group D) and had moderately reduced r-CBF in the bilateral frontotemporal lobes (Figure 2).

4. Discussion

The majority (72.0%) of ALS patients tested in this study had syntactic comprehension disorder, which is one of the linguistic characteristics of ALS with aphasic symptoms [1821]. However, we decided to exclude the patients with severe dysarthria. We should take into account that we might have underestimated the frequency of syntactic comprehension disorder, because the language disorders are often associated with the bulbar presentation. The prevalence of syntactic comprehension disorder in MND or ALS patients varies across the literature, ranging from 27.8% to 83.3% (Table 6). Rakowicz and Hodges [19] reported that four out of 15 patients with bulbar onset MND had syntactic comprehension disorder. Cobble [18] reported a single patient with bulbar onset MND who had syntactic comprehension disorder, and Bak et al. [20] reported that five out of six patients with bulbar onset MND had syntactic comprehension disorder. In our cohort, all patients with bulbar onset ALS had syntactic comprehension disorder, and it is therefore possible that bulbar onset ALS is associated with syntactic comprehension disorder.


StudyTestsFrequency

Doran et al. (1995) [8]The test of the reception of grammar (TROG) and the shortened version of the token test 3/5 (60.0%)
Rakowicz and Hodges (1998) [19]The test of the reception of grammar (TROG)5/18 (27.8%)
Cobble (1998) [18]The test of auditory comprehension of sentences (PALPA) 5/9 (55.6%)
Bak et al. (2001) [20]The test of the reception of grammar (TROG) 5/6 (83.3%)
Taylor et al. (2013) [47]The test of the reception of grammar (TROG)18/51 (35.3%)
Current resultsSyntax test for aphasia (STA)18/25 (72.0%)

The syntax test used in this study evaluated the strategy level (use of word meaning, word order, or particle) of syntactic comprehension [38]. Patients with syntactic comprehension disorder were more impaired at the level of use of particle (Level III) than use of word meaning (Level I) and word order (Level II). The errors depended on the complexity of syntax. This pattern of errors is similar to that observed in aphasic patients [39, 40]. ALS patients progressively develop disorders of verbal and literal expression due to dysarthria or upper limb weakness, and syntactic comprehension disorder might therefore be concealed when not specifically tested for in clinical settings.

Bak et al. [20] reported that visuospatial skills were relatively well preserved in MND patients who had impaired syntactic comprehension. Moreover, Phukan et al. [2] reported that of 19 ALS patients who had multidomain executive impairment, only nine had visuospatial impairment. In our cohort, all patients who failed the RCPM or the FAB also failed the STA auditory comprehension task. Bak et al. [20, 41, 42] reported that MND with aphasic symptoms and MND with dementia were extremes on a nosological continuum with a varying degree of overlap between them. According to this theory, our data (Table 5) might indicate that ALS also represents a continuum including aphasia, executive dysfunction, and visuospatial dysfunction. However, the present study included some ALS patients with aphasic symptoms who did not show executive dysfunction or visuospatial dysfunction.

Neuropsychological and neuroimaging studies have reported that Broca’s area (left inferior frontal gyrus, Brodmann’s areas 44 and 45) is involved in the processing of sentence structure [4346]. We found a moderate reduction in r-CBF in the bilateral frontal lobes of a patient who failed the STA auditory comprehension task, the FAB, and the RCPM but only a mild reduction in a patient who passed these tests. This may indicate that neurodegeneration in the bilateral frontal lobes underlies the results of our neuropsychological evaluations. However, there is no evidence of a relation between neuroimaging data and syntactic comprehension in present study, and further research of r-CBF in ALS patients is needed.

Broca’s area is adjacent to the lower precentral gyrus, which is the motor center for the face, lips, tongue, and pharynx. Therefore, we propose that, in patients with bulbar onset ALS, neurodegeneration may have progressed from the medulla oblongata and pons to the precentral gyrus and inferior frontal gyrus. Six of 10 (60.0%) patients with upper limb onset ALS had syntactic comprehension disorder, and 1 of 4 (25.0%) patients with lower limb onset ALS had syntactic comprehension disorder (Table 3). If neurodegeneration first progressed from the medulla oblongata and pons to the upper prefrontal gyrus and Broca’s area, then neurodegeneration might have occurred in some patients with upper or lower limb onset type ALS.

Taylor et al. [47] found language domain impairment in 43% of patients with ALS, and executive domain impairment in 31%. They concluded that although the two domains were strongly associated, executive dysfunction did not fully account for the language impairment observed. These were similar to our results. In our cohort, there was strong correlation between the score of the STA auditory comprehension task and the FAB. On the other hand, there were 9 patients who failed level IV on the STA auditory comprehension task but passed the FAB and RCPM (Group B). This may indicate that neurodegeneration was limited to Broca’s area and had not progressed to the prefrontal lobe. Furthermore there were 3 patients who failed the STA auditory comprehension task and the FAB but passed the RCPM (Group C). In addition, there were no patients who failed the FAB and/or the RCPM but passed the STA auditory comprehension task and who failed the RCPM but passed the FAB. These results raise the possibility that neurodegeneration in ALS may sequentially progress from Broca’s area to the prefrontal lobe and occipital lobe. Longitudinal studies on the relation between neuropsychological evaluations and neuroimaging data, including IMP-SPECT, in patients with ALS are required. These will help to elucidate the mechanisms by which neurodegeneration progresses in ALS.

Ichikawa et al. [14] reported that, of 15 patients with bulbar onset type ALS who had writing errors, six showed grammatical errors. However, evaluation of the abilities of syntactic comprehension and writing at the same time has not yet been performed. Further studies are needed in order to confirm the relation between writing errors and syntactic comprehension disorder.

5. Conclusion

In this study we investigated the prevalence and profile of syntactic comprehension in ALS and the relation of syntactic comprehension with executive and visuospatial function. There was a high prevalence of syntactic comprehension disorder, especially in patents with bulbar onset ALS. These results raise the possibility that neurodegeneration in ALS may sequentially progress from Broca’s area to the prefrontal lobe and occipital lobe.

Conflict of Interests

The authors declare that there is no conflict of interests regarding the publication of this paper.

Acknowledgment

The authors would like to acknowledge all the patients who kindly agreed to participate in this study.

References

  1. M. J. Strong, G. M. Grace, M. Freedman et al., “Consensus criteria for the diagnosis of frontotemporal cognitive and behavioural syndromes in amyotrophic lateral sclerosis,” Amyotrophic Lateral Sclerosis, vol. 10, no. 3, pp. 131–146, 2009. View at: Publisher Site | Google Scholar
  2. J. Phukan, M. Elamin, P. Bede et al., “The syndrome of cognitive impairment in amyotrophic lateral sclerosis: a population-based study,” Journal of Neurology, Neurosurgery and Psychiatry, vol. 83, no. 1, pp. 102–108, 2012. View at: Publisher Site | Google Scholar
  3. D. T. Stuss and B. Levine, “Adult clinical neuropsychology: lessons from studies of the frontal lobes,” Annual Review of Psychology, vol. 53, pp. 401–433, 2002. View at: Publisher Site | Google Scholar
  4. S. Abrahams, P. N. Leigh, A. Harvey, G. N. Vythelingum, D. Grisé, and L. H. Goldstein, “Verbal fluency and executive dysfunction in amyotrophic lateral sclerosis (ALS),” Neuropsychologia, vol. 38, no. 6, pp. 734–747, 2000. View at: Publisher Site | Google Scholar
  5. S. Abrahams, L. H. Goldstein, A. Simmons et al., “Word retrieval in amyotrophic lateral sclerosis: a functional magnetic resonance imaging study,” Brain, vol. 127, no. 7, pp. 1507–1517, 2004. View at: Publisher Site | Google Scholar
  6. C. Volpato, F. Piccione, S. Silvoni et al., “Working memory in amyotrophic lateral sclerosis: auditory event-related potentials and neuropsychological evidence,” Journal of Clinical Neurophysiology, vol. 27, no. 3, pp. 198–206, 2010. View at: Publisher Site | Google Scholar
  7. R. J. Caselli, A. J. Windebank, R. C. Petersen et al., “Rapidly progressive aphasic dementia and motor neuron disease,” Annals of Neurology, vol. 33, no. 2, pp. 200–207, 1993. View at: Publisher Site | Google Scholar
  8. M. Doran, J. Xuereb, and J. R. Hodges, “Rapidly progressive aphasia with bulbar motor neurone disease: a clinical and neuropsychological study,” Behavioural Neurology, vol. 8, no. 3-4, pp. 169–180, 1995. View at: Google Scholar
  9. A. Roberts-South, K. Findlater, M. Strong, and J. B. Orange, “Longitudinal changes in discourse prouction in amyotrophic lateral sclerosis,” Seminars in Speech and Language, vol. 33, no. 1, pp. 79–94, 2012. View at: Publisher Site | Google Scholar
  10. A. E. Hillis, S. Oh, and L. Ken, “Deterioration of naming nouns versus verbs in primary progressive aphasia,” Annals of Neurology, vol. 55, no. 2, pp. 268–275, 2004. View at: Publisher Site | Google Scholar
  11. S. Tsuji-Akimoto, S. Hamada, I. Yabe et al., “Writing errors as a result of frontal dysfunction in Japanese patients with amyotrophic lateral sclerosis,” Journal of Neurology, vol. 257, no. 12, pp. 2071–2077, 2010. View at: Publisher Site | Google Scholar
  12. E. Watanabe, Journal of Okayama Medical Association, vol. 5, pp. 138–144, 1893.
  13. H. Ichikawa, M. W. Miller, and M. Kawamura, “Amyotrophic lateral sclerosis and language dysfunction: Kana, kanji and a prescient report in Japanese by Watanabe (1893),” European Neurology, vol. 65, no. 3, pp. 144–149, 2011. View at: Publisher Site | Google Scholar
  14. H. Ichikawa, N. Takahashi, S. Hieda, H. Ohno, and M. Kawamura, “Agraphia in bulbar-onset amyotrophic lateral sclerosis: not merely a consequence of dementia or aphasia,” Behavioural Neurology, vol. 20, no. 3-4, pp. 91–99, 2008. View at: Publisher Site | Google Scholar
  15. H. Ichikawa, S. Koyama, H. Ohno, K. Ishihara, K. Nagumo, and M. Kawamura, “Writing errors and anosognosia in amyotrophic lateral sclerosis with dementia,” Behavioural Neurology, vol. 19, no. 3, pp. 107–116, 2008. View at: Google Scholar
  16. H. Ichikawa, H. Ohno, H. Murakami, Y. Ohnaka, and M. Kawamura, “Writing error may be a predictive sign for impending brain atrophy progression in amyotrophic lateral sclerosis: a preliminary study using X-ray computed tomography,” European Neurology, vol. 65, no. 6, pp. 346–351, 2011. View at: Publisher Site | Google Scholar
  17. M. Satoh, K. Takeda, and S. Kuzuhara, “Agraphia in intellectually normal Japanese patients with ALS: omission of kana letters,” Journal of Neurology, vol. 256, no. 9, pp. 1455–1460, 2009. View at: Publisher Site | Google Scholar
  18. M. Cobble, “Language impairment in motor neurone disease,” Journal of the Neurological Sciences, vol. 160, supplement 1, pp. S47–S52, 1998. View at: Publisher Site | Google Scholar
  19. W. P. Rakowicz and J. R. Hodges, “Dementia and aphasia in motor neuron disease: an underrecognised association?” Journal of Neurology Neurosurgery and Psychiatry, vol. 65, no. 6, pp. 881–889, 1998. View at: Google Scholar
  20. T. H. Bak, D. G. O'Donovan, J. H. Xuereb, S. Boniface, and J. R. Hodges, “Selective impairment of verb processing associated with pathological changes in Brodmann areas 44 and 45 in the motor neurone disease-dementia-aphasia syndrome,” Brain, vol. 124, no. 1, pp. 103–120, 2001. View at: Google Scholar
  21. P. Bongioanni, G. Buoiano, and M. Magoni, “Language impairments in ALS/MND,” Amyotrophic Lateral Sclerosis/Motor Neuron Disease, 2002. View at: Google Scholar
  22. A. R. Damasio and D. Tranel, “Nouns and verbs are retrieved with differently distributed neural systems,” Proceedings of the National Academy of Sciences of the United States of America, vol. 90, no. 11, pp. 4957–4960, 1993. View at: Google Scholar
  23. A. D. Friederici, A. Hahne, and D. Saddy, “Distinct neurophysiological patterns reflecting aspects of syntactic complexity and syntactic repair,” Journal of Psycholinguistic Research, vol. 31, no. 1, pp. 45–63, 2002. View at: Publisher Site | Google Scholar
  24. N. F. Dronkers, D. P. Wilkins, R. D. van Valin Jr., B. B. Redfern, and J. J. Jaeger, “Lesion analysis of the brain areas involved in language comprehension,” Cognition, vol. 92, no. 1-2, pp. 145–177, 2004. View at: Publisher Site | Google Scholar
  25. L. K. Tyler, W. D. Marslen-Wilson, B. Randall et al., “Left inferior frontal cortex and syntax: function, structure and behaviour in patients with left hemisphere damage,” Brain, vol. 134, no. 2, pp. 415–431, 2011. View at: Publisher Site | Google Scholar
  26. D. Neary, J. S. Snowden, L. Gustafson et al., “Frontotemporal lobar degeneration: a consensus on clinical diagnostic criteria,” Neurology, vol. 51, no. 6, pp. 1546–1554, 1998. View at: Google Scholar
  27. B. R. Brooks, R. G. Miller, M. Swash, and T. L. Munsat, “El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis,” Amyotrophic Lateral Sclerosis, vol. 1, no. 5, pp. 293–299, 2000. View at: Publisher Site | Google Scholar
  28. Y. Ohashi, K. Tashiro, Y. Itoyama et al., “Study of functional rating scale for amyotrophic lateral sclerosis: revised ALSFRS(ALSFRS-R) Japanese version,” Brain and Nerve, vol. 53, no. 4, pp. 346–355, 2001. View at: Google Scholar
  29. A. Caramazza, R. S. Berndt, A. G. Basili, and J. J. Koller, “Syntactic processing deficits in aphasia,” Cortex, vol. 17, no. 3, pp. 333–348, 1981. View at: Google Scholar
  30. S. Sasanuma, “Agrammatism in Japanese—a cross-language approach,” Journal of Neurolinguistics, vol. 4, no. 2, pp. 233–242, 1989. View at: Google Scholar
  31. D. Caplan, G. Waters, G. Dede, J. Michaud, and A. Reddy, “A study of syntactic processing in aphasia I: behavioral (psycholinguistic) aspects,” Brain and Language, vol. 101, no. 2, pp. 103–150, 2007. View at: Publisher Site | Google Scholar
  32. I. Fujita, “Treatment programme for sentence processing deficits in aphasia,” Higher Brain Function Research, vol. 16, pp. 214–220, 1996 (Japanese). View at: Google Scholar
  33. B. Dubois, A. Slachevsky, I. Litvan, and B. Pillon, “The FAB: a frontal assessment battery at bedside,” Neurology, vol. 55, no. 11, pp. 1621–1626, 2000. View at: Google Scholar
  34. T. Terada, T. Obi, H. Miyajima, and K. Mizoguchi, “Assessing frontal lobe function in patients with amyotrophic lateral sclerosis by frontal assessment battery,” Clinical Neurology, vol. 50, no. 6, pp. 379–384, 2010. View at: Google Scholar
  35. M. Sugishita and K. Yamazaki, Japanese Raven's Colored Progressive Matrices, Nihon Bunka Kagakusya, Tokyo, Japan, 1993 (Japanese).
  36. V. Prabhakaran, J. A. L. Smith, J. E. Desmond, G. H. Glover, and J. D. E. Gabrieli, “Neural substrates of fluid reasoning: an fMRI study of neocortical activation during performance of the Raven's progressive matrices test,” Cognitive Psychology, vol. 33, no. 1, pp. 43–63, 1997. View at: Google Scholar
  37. T. Hosokawa, Y. Yamada, A. Isagoda, and R. Nakamura, “Psychometric equivalence of the hasegawa dementia scale-revised with the mini-mental state examination in stroke patients,” Perceptual and Motor Skills, vol. 79, no. 1, pp. 664–666, 1994. View at: Google Scholar
  38. I. Fujita and M. Tateishi, “The standard series of language, speech and hearing pathology,” in Aphasiology, Igakusyoin, Tokyo, Japan, 2009 (Japanese). View at: Google Scholar
  39. A. Caramazza and E. B. Zurif, “Dissociation of algorithmic and heuristic processes in language comprehension: evidence from aphasia,” Brain and Language, vol. 3, no. 4, pp. 572–582, 1976. View at: Google Scholar
  40. I. Fujita, T. Miyake, Y. Takahashi, K. Sakai, and M. Akitake, “Syntactic recognition in aphasics,” The Japan Journal of Logopedics and Phoniatrics, vol. 18, pp. 6–13, 1977 (Japanese). View at: Google Scholar
  41. T. H. Bak and J. R. Hodges, “Cognition, language and behaviour in motor neurone disease: evidence of frontotemporal dysfunction,” Dementia and Geriatric Cognitive Disorders, vol. 10, no. 1, pp. 29–32, 1999. View at: Publisher Site | Google Scholar
  42. T. H. Bak and J. R. Hodges, “Motor neurone disease, dementia and aphasia: coincidence, co-occurrence or continuum?” Journal of Neurology, vol. 248, no. 4, pp. 260–270, 2001. View at: Publisher Site | Google Scholar
  43. D. Swinney, E. Zurif, P. Prather, and T. Love, “Neurological distribution of processing resources underlying language comprehension,” Journal of Cognitive Neuroscience, vol. 8, no. 2, pp. 174–184, 1996. View at: Google Scholar
  44. I. Wartenburger, H. R. Heekeren, F. Burchert, S. Heinemann, R. de Bleser, and A. Villringer, “Neural correlates of syntactic transformations,” Human Brain Mapping, vol. 22, no. 1, pp. 72–81, 2004. View at: Publisher Site | Google Scholar
  45. C. J. Fiebach, M. Schlesewsky, G. Lohmann, D. Y. von Cramon, and A. D. Friederici, “Revisiting the role of Broca's area in sentence processing: syntactic integration versus syntactic working memory,” Human Brain Mapping, vol. 24, no. 2, pp. 79–91, 2005. View at: Publisher Site | Google Scholar
  46. K. Ogawa, M. Ohba, and T. Inui, “Neural basis of syntactic processing of simple sentences in Japanese,” NeuroReport, vol. 18, no. 14, pp. 1437–1441, 2007. View at: Publisher Site | Google Scholar
  47. L. J. Taylor, R. G. Brown, S. Tsermentseli et al., “Is language impairment more common than executive dysfunction in amyotrophic lateral sclerosis?” Journal of Neurology, Neurosurgery and Psychiatry, vol. 84, no. 5, pp. 494–498, 2013. View at: Publisher Site | Google Scholar

Copyright © 2014 Kentarou Yoshizawa et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

1039 Views | 503 Downloads | 20 Citations
 PDF  Download Citation  Citation
 Download other formatsMore
 Order printed copiesOrder

We are committed to sharing findings related to COVID-19 as quickly and safely as possible. Any author submitting a COVID-19 paper should notify us at help@hindawi.com to ensure their research is fast-tracked and made available on a preprint server as soon as possible. We will be providing unlimited waivers of publication charges for accepted articles related to COVID-19. Sign up here as a reviewer to help fast-track new submissions.