Behavioral Neurology in Language and Aphasia

REVIEW ARTICLE
Behavioral Neurology in Language and Aphasia:
From Basic Studies to Clinical Applications
Kenichi Meguro
Department of Geriatric Behavioral Neurology, Tohoku University Faculty of Medicine 2-1, Seiryo-machi,
Aoba-ku, 980-8575 Sendai, Japan. Correspondence mail: k-meg@umin.ac.jp.
ABSTRAK
Seiring dengan meningkatnya populasi usia lanjut, penurunan fungsi kognisi akibat penyakit neurodegeneratif atau stroke semakin umum ditemukan dan dianggap tidak dapat dihindari seperti halnya proses
menua. Pada demensia dan stroke, gangguan komunikasi akibat penurunan kualitas berbahasa merupakan
salah satu masalah utama. Neurologi perilaku bertujuan untuk menjelaskan hubungan antara fungsi otak dan
perilaku; penurunan kualitas berbahasa merupakan salah satu target utamanya, dan aplikasi klinisnya sungguh
bermanfaat dalam membantu membangun pemahaman yang lebih baik bagi pasien.
Bahasa merupakan serangkaian suara atau karakter yang membawa makna dalam komunikasi. Berdasarkan
perspektif evolusi, “bahasa” dapat dianggap berkaitan dengan struktur otak tertentu bagaikan anjing pemburu
yang mampu menunjukkan mangsanya dengan tepat. Struktur otak yang dimaksud adalah ganglia basalis dan
singulata anterior, serta talamus dan korteks serebri yang menjadi latar belakang neurobiologis. Manusia dapat
memanfaatkan bahasa. Area bahasa merupakan area otak yang baru berkembang dalam evolusi dan terutama
terletak di hemisfer otak sebelah kiri. Memori semantik juga telah berkembang pada manusia. Ada dua rute
memori, yakni memori permukaan dan memori dalam. Memori dalam berkaitan dengan arti dan melibatkan
tiga area otak, yakni area peri-silvian, area peri-peri-Silvian dan hemisfer kanan.
Dengan menggunakan prinsip tersebut, gejala bahasa pada demensia yang disertai afasia tak lancar
yang progresifn/(PA), demensia semantik/Semantic Dementia (SD) dan penyakit Alzheimer/Alzheimer Disease
(AD) serta demensia vaskular/vascular dementia (VaD) dapat dimengerti. Gejala PA dapat dipahami dengan
mempelajari disfungsi area bahasa peri-Silvian, sedangkan SD dan AD pada area bahasa peri-peri-Silvian dan
beberapa kasus VaD dan AD pada hemisfer kanan.
Kata kunci: bahasa, afasia progresif tak lancar, demensia semantic, penyakit Alzheimer, demensia vascular.
ABSTRACT
With increasing aging population, cognitive deteriorations due to neuro- degenerative diseases or stroke are
so commonly observed that it is thought to be inevitable with aging. For dementia and stroke, a communication
disorder due to language deterioration is one of the main problems. Behavioral neurology aims to clarify the
relationship between brain function and behavior; language deterioration is one of the main targets, and its
clinical applications are really useful for making better understanding of patients.
Language is sequences of sound or characters that carry meanings for communication. From the evolutionary
perspective, “language” can be thought about by considering birds and dogs: the basal ganglia and anterior
cingulate, and the thalamus and cerebral cortex are thought to provide the neurobiological background,
respectively. Humans can use language. The language area is a newly developed brain area in evolution and
is mainly localized in the left cerebral hemisphere. Semantic memory has also developed in humans. There are
two routes, the superficial and deep routes, with the latter associated with meaning, and three brain areas are
involved: the peri-Sylvian area, per-peri-Sylvian area, and right hemisphere. Using these principles, language
symptoms of dementia with progressive non-fluent aphasia (PA), semantic dementia (SD), Alzheimer’s disease
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Acta Med Indones-Indones J Intern Med
(AD), and vascular dementia (VaD) can be understood. Namely, the symptoms of PA is understood by the
dysfunction of peri-Sylvian language area, those of SD and AD by that of peri-peri-Sylvian language area, and
those of some VaD cases and AD cases by that of right hemisphere.
Key words: language, progressive non-fluent aphasia, semantic dementia, Alzheimer’s disease, vascular
dementia.
INTRODUCTION
Rules of Language
With increasing aging population, cognitive
deteriorations due to neuro-degenerative diseases
or stroke are so commonly observed in older
adults that it is thought to be inevitable with
aging. This situation leads us to perform
comprehensive approach for the geriatric ward1
or preventing stroke.2 For dementia and stroke,
a communication disorder due to language
deterioration is one of the main problems.
Behavioral neurology aims to clarify the
relationship between brain function and human
behavior through medical approach to patients
with neurodegenerative diseases or stroke.
Language deterioration is one of the main
targets of behavioral neurology, and its clinical
applications are really useful for making better
understanding of dementia or stroke patients.
In this review, we will present basic principles
and clinical applications of behavioral neurology
especially on language deterioration, together
with some clinical cases.
As shown in Figure 1, language, and
especially a word, is a sequence of sounds or
written characters that carries a meaning. There
is a relationship between the sequence and the
meaning; for example, the sequence of sounds
“A RI GA TO” in Japanese has the meaning of
“thank you.” The meaning can also be affected
in a pragmatic way; the tone of sounds or a facial
expression can demonstrate even an opposite
meaning, despite use of the same sequence of
sounds. People can say “thank you” to indicate
gratitude or with an ironical meaning.
BASIC PRINCIPLES
Evolution
From the evolutionary perspective,
“language” can be thought about by considering
birds, dogs, and humans. Birds can repeat
human “words”; however; they clearly cannot
understand the language, and can only produce
sounds. Neurobiologically, the basal ganglia and
anterior cingulate are thought to be associated
with this mechanism.3 Mammals such as dogs
can perform “attention-related sound learning".
Thus, a dog can discriminate sounds and show
“body language” by shaking its tail. The thalamus
and cerebral cortex are thought to provide the
neurobiological background. Finally, humans
can use “language” The language area is a
newly developed brain area in evolution and is
mainly localized in the left cerebral hemisphere.
Semantic memory has also developed in humans.
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Figure 1. Basic principle 2: Rules of language
Dual Route
Language is a process of auditory or visual
input for the affecter, and speech or writing output
from the effecter, as shown in Figure 2. This
process is possible with or without accessing
the semantic system. Speaking or reading aloud
the sequence of sounds or written characters
is possible without knowing the meaning. For
example, German language can be easily read
aloud according to the regular pronunciation
rules; however, it may be difficult to understand.
This is equivalent to repetition of human words
by a bird.
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Figure 2. Basic principle 3: Dual route
THREE BRAIN AREAS ASSOCIATED WITH
LANGUAGE
Figure 3 illustrates the three brain areas
associated with language, with reference to basic
principles.4 The first language area comprises
multiple brain regions associated with the
sequence of sounds (or written characters) (basic
principle 1) and the affecter/effecter (basic
principle 2). This area is called the “peri-Sylvian
language area,” since it surrounds the Sylvian
fissure, and includes the Broca and Wernicke
areas, supramarginal and post central sulci, and
precentral and postcentral sulci (regions 1-4 in
Figure 3). The second language area comprises
multiple brain regions associated with meaning
(basic principle 1) and the semantic system (basic
principle 2). This area surrounds the peri-Sylvian
language area, and thus is called the “peri-periSylvian language area”. The area includes the
angular gyrus, posterior temporal and anterior
temporal lobes, precentral sulcus, and frontal
association area (regions 5-9 in Figure 3). The
third language area is the right hemisphere
(region 10 in Figure 3). This area is associated
with the pragmatic system (basic principles 1
and 2).
Figure 3. Three brain areas associated with language
Behavioral neurology in language and aphasia
Early anatomically based models of language
consisted of an arcuate tract connecting Broca's
speech and Wernicke's comprehension centers;
a lesion of the tract resulted in conduction
aphasia. However, the heterogeneous clinical
presentations of conduction aphasia suggest a
greater complexity of peri-sylvian anatomical
connections than allowed for in the classical
anatomical model.
A study using the diffusion tensor MRI5
demonstrated the classical arcuate pathway
connecting Broca's and Wernicke's areas, and
showed the anatomical findings relevant to
provide a framework for Lichtheim's symptombased neurological model of aphasia. The
classic types of aphasia (Broca, transcortical
motor, conduction, Wernicke, and transcortical
sensory aphasia) are characterized by patterns
of dysfunction in the first language area, as
summarized in Table 1.
Table 1. Classic model of aphasia associated with perisylvian language area
Fluency
Comprehension
Repetition
Broca
X
O
X
Transcortical
motor
X
O
O
Conduction
O
O
X
Wernicke
O
X
X
Transcortical
sensory
O
X
O
A S S O C I AT I O N O F T H E J A PA N E S E
LANGUAGE WITH THE DUAL ROUTE
Two Different Scripts: Kanji and Kana
There are two kinds of scripts in
Japanese writing: Kanji (logogram) and Kana
(morphogram). Generally, Kanji words are
thought to correspond to irregular words in
Western languages, whereas Kana words are
considered to be regular words. Regular words
have a “regular” rule of pronunciation. As
shown in Table 2, Kana characters are learned
at home, whereas Kanji characters, which are
more complex, are taught at elementary school.
The angular gyrus is considered to be associated
with character recall for both Kana and Kanji,
while the posterior inferior temporal (PIT) lobe
is additionally related to Kanji recall.6
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Table 2. Neuropsychological background of Kanji and Kana
Kana
Kanji
Education
Home
School
Complexity
+
+++
Character recall
“Form” recall
Reading System
Figure 4 illustrates a schema of a reading
system, including three subsystems: letterby-letter reading, lexical reading without knowing
the meaning, and lexical reading with knowledge
of the meaning. Reading letter-by-letter (arrow
A in Figure 4) is possible independent of the
lexicon and semantic systems. Reading of the
lexicon is also possible without knowing the
meaning (arrow B in Figure 4), or reading can
be performed with knowledge of the meaning
(arrow C in Figure 4).
In contrast to Taiwanese or Chinese, speakers
of Japanese can use a Kanji character to express
a sound without a meaning; i.e., “on”-reading
of Kanji. For example, “Indonesia” is written as
印度尼支亜 in Kanji, since the respective
characters are pronounced as IN-DO-NE-SHI-A.
There is no relationship with the respective
meanings of each character: stamp-degreenun-support-“A”.
Figure 4. Reading system
330
Writing System
For a writing system, there are also three
routes: phoneme-by-phoneme writing, lexical
writing without knowing the meaning, and lexical
writing with knowledge of the meaning. In Kanji
and Kana writing, Kana is used more frequently,
but Kanji has more “form” information and
semantic information.
Maeshima et al. 7 reported the case of
a 61-year-old woman with a left thalamic
hemorrhage causing agraphia of Kanji. She had
a decrease in the blood flow in the left thalamus
as well as in the frontal lobe. The agraphia in
this case may be due to the thalamic lesion itself,
but the SPECT findings strongly suggest that a
secondary cortical lesion may be involved in
producing the higher cognitive disorder.
CLINICAL APPLICATIONS
Dysfunction of the Peri-Sylvian Language
Area: Progressive Non-fluent Aphasia
Frontotemporal lobar degeneration (FTLD)
encompasses a heterogeneous group of clinical
syndromes that include frontotemporal dementia
(FTD), progressive non-fluent aphasia (PNFA),
semantic dementia (SD), etc.8
Previous review 9 reported the clinical,
neuroimaging, and neuropathologic features of
PNFA, a rare neurodegenerative syndrome most
notable for its distinct language disturbance.
Longitudinal observations of 3 patients revealed
progressively telegraphic speech and writing,
followed by gradual deterioration of sentence
comprehension, and finally, preterminal mutism
and dementia. Magnetic Resonance Imaging
(MRI) revealed cortical atrophy most pronounced
in anterior regions of the left hemisphere.
Functional neuroimaging demonstrated reduced
cerebral activity most prominently in left frontal
and temporal regions.
We present a case of progressive non-fluent
aphasia with lacunar infarction is presented as
an example of dysfunction in the peri-Sylvian
language area. The patient was an 87-year-old,
right handed man who had dysarthria, but could
communicate with his family. His mother and
brother had similar dysarthria.
The patient had suffered a stroke in 1997 and
subsequently his dysarthria progressed. He also
showed amnesia. Delusion of theft, delirium at
night, and aggressiveness were noted in 2001.
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He could not communicate well due to dysarthria
and dementia. He was admitted to the hospital for
further evaluation and rehabilitation.
Neurological examination disclosed no
remarkable findings except for dysarthria. He
had no buccofacial apraxia. Language skills
included relatively good comprehension and
good ability at naming daily items. He could
repeat a word, but not a sentence. The MiniMental State Examination (MMSE)10 score was 3
and the Cognitive Abilities Screening Instrument
(CASI)11 score was 13, with a perfect score
(10/10) on the Figure copying (double pentagon)
domain.
An MRI examination disclosed a lacunar
infarction in the right basal ganglia region with
white matter changes. The frontal and temporal
lobes showed atrophic changes. Since the lacunar
infarction was not associated with dysarthria,
we evaluated the atrophy in detail. The voxelbased specific regional analysis system for
AD (VSRAD) 12 images comparing the two
hemispheres are shown in Figure 5. The left
precentral gyrus had significantly greater atrophic
changes compared with the right side. This area
is considered to be associated with speech output.
Dysarthria is classified as congenital
(functional/organic) or acquired, with the
latter class including cerebrovascular diseases,
progressive non-fluent aphasia, frontotemporal
lobar degeneration, and amyotrophic lateral
sclerosis. The clinical course and the location
of stroke supported the diagnosis of progressive
non-fluent aphasia with lacunar infarction.
Figure 5. MRI findings (VSRAD)
Dysfunction of the Peri-Peri-Sylvian Language
Area: Semantic Dementia and Alzheimer
Aphasia
A clinicopathologic review on FTLD 13
reported that clinical phenotype is often assumed
Behavioral neurology in language and aphasia
to be a poor predictor of underlying histopathology.
They classified pathological material from
79 FTLD brains, blind to clinical diagnosis,
according to topography of brain atrophy. There
were highly significant relationships to clinical
syndrome. Atrophy was predominantly frontal
and anterior temporal in FTD, frontal markedly
asymmetric peri-sylvian in PNFA, asymmetric
bitemporal in SD. The findings demonstrate
predictable relationships between clinical
phenotype and both topographical distribution
of brain atrophy. The findings emphasize the
importance of refined delineation of both
clinical and pathological phenotype in furthering
understanding of FTLD.
We here in present a case of SD and data
from patients with Alzheimer’s disease (AD)
are discussed as examples of dysfunction of the
peri-peri-Sylvian language area.
SD involves brain regions associated with
meaning (basic principle 1) and the semantic
system (basic principle 2). Areas 6 (posterior
temporal lobe), 7 (anterior temporal lobe), and 9
(frontal association area) (Figure 3) are mainly
degenerated.
We previously reported a case of SD with
multilingualism in a 75-year-old right-handed
Taiwanese woman.14 She had worked as a tailor
before her illness, and had been able to speak
Taiwanese, Japanese and Chinese fluently until
5 years ago. She gradually had symptoms of
profound anomia and word-finding difficulty.
Her mother language was Taiwanese and she
had learned Japanese as her first symbolized
language. Although she had used Chinese for
most of her life, she depended on Japanese for
writing and reading, such as reading a newspaper
and keeping accounts. At the time of examination,
she could speak only very simple Taiwanese
and Japanese, and she could recognize simple
Japanese characters. We speculated that reading
and writing in Japanese seemed to have had a
greater impact on the semantic system in this
case.
It is well known that AD as per the NINCDSADRDA diagnostic criteria15 involves mainly
posterior brain regions16 associated with meaning
(basic principle 2), the semantic system (basic
principle 3), and the pragmatic system (basic
principles 2 and 3). Areas 5 (angular gyrus),
6 (posterior temporal lobe), and 10 (right
hemisphere) (Figure 3) are mainly degenerated.
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Figure 6. Thirty elements in picture description task18
Alzheimer’s speech is referred to as ‘empty’,
since patients speak fluently but with abundant
pronouns due to word finding difficulties. The
Picture Description Task.17 (Figure 6) is useful
for evaluation of language function in a narrative
fashion. The picture contains 30 basic elements,
which are shown as words on the figure (girl,
telephone, call, etc.). Three variables can be
analyzed: Variable 1: the amount of information
conveyed, Variable 2: the number of relevant
and irrelevant descriptions, and Variable 3: the
efficacy of the description (the ratio of the number
of relevant descriptions to the total number of
descriptions).
We have found that AD patients show
significantly lower scores for Variable 1 and
Variable 3, and that regional cerebral blood flows
in the occipital lobes and thalamus are correlated
with Variable 1. This suggests that visual
searching (occipital lobes) and the thalamocortical network are part of the neurobiological
background.18
The left thalamo-cortical network has been
implicated in successful speech separation and
identification.19 Recently, the cortico-striatothalamo-cortical network has been proposed as
a new thalamo-cortical network, in association
with syntactic integration of lexical elements
in grammatical structure.20 This caused us to
re-analyze our previous data from a syntactic
perspective. The Picture Description Task
contains 7 verbs: call, smoke, watch, do, have,
play, and lie. Among the 14 AD patients, 4
showed decreased blood flow in the thalamus and
5 showed decreased blood flow in the striatum.
One patient had decreases in both brain regions
and showed impaired syntactic errors, i.e.,
impaired connections between nouns and verbs
(p<0.05 by chi-square test).
In writing disturbance, AD alexia has been
thought of as having a surface alexia pattern
due to a deteriorated semantic system. That is,
the semantic system is damaged. However, our
systematic investigation suggested that several
patterns may occur, rather than the surface
dyslexia pattern alone, with predominance of
Kanji errors, as shown in Table 3.21
Dysfunction of the Right Hemisphere:
Vascular Dementia and Alzheimer Disease
Results from cases of vascular dementia
(VaD) as per the diagnosis of NINDS-AIREN22
and AD are presented as examples of dysfunction
of the right hemisphere. It is clinically well known
that patients with right hemisphere damage
showed overestimation of self-reported physical
activities23 but also manifest communication
disability, despite having no apparent language
disability. We prepared an original scale, the
Daily Communication Assessment Scale,
and compared patients with right hemisphere
damage to those with left hemisphere damage
with similar MMSE scores.24 The patients with
left hemisphere damage had coarse speech
patterns, whereas those with right hemisphere
damage showed a “deviant” pattern of language,
including limited information, circuitry and
Table 3. Alzheimer’s alexia
Task
Reading task
Semantic task
Items
AD patients
Moderate
Severe
D
Kana characters
46
えい
O
Kana transcribed words
122
いえ
O
D
Kanji words
122
家
D
D ~ X
Matching with objects
122
D
X ~ D
The signs ‘O’, ‘X’, and ‘triangle’ mean “OK”, “poor”, “partly OK”.
332
Sample
Vol 44 • Number 4 • October 2012
redundancy, excessive utterance, and disjointed
conversation.
We recently reported a 79-year-old patient
with chronic severe aphasia.25 Singing therapy
was effective since her right hemisphere was
relatively preserved. Interventions 1, 2, and 3
were to practice singing a song that the patient
knew, to practice singing a song with a therapist,
and to practice saying a greeting using a song
with lyrics, respectively. After intervention 1,
the patient could sing spontaneously and repeat
lyrics. After intervention 2, she could sing with
the therapist, and sing spontaneously and repeat
lyrics. After intervention 3, she could memorize
words with meaning, say the words in context,
and use them. These suggest that rehabilitation
therapy can still be used in patients with severe
cognitive impairment.
We examined 40 AD patients using the
Binet-V test and positron emission tomography
(PET).26 The questions on illogical sentences
included sentences such as, “A man saw a horse
carrying a heavy bag. He felt pity, so he took the
bag on his back, and rode on the horse.” Patients
were asked to state what is illogical. Illogical
pictures in the test (Figure 7) included 1) a girl
eating curry and rice with the opposite side of the
spoon, 2) a businessman walking with different
shoes on his right and left feet, 3) a family holding
a barbeque in the garden in the rain, and 4) a boy
giving water to a flower garden using a hose, but
the opposite end is not connected with the water.
We found that the scores on verbal illogical
questions were correlated with regional
glucose metabolism in the right angular gyrus
and the bilateral temporal and parietal lobes
Figure 7. Illogical pictures in binet-V test
Behavioral neurology in language and aphasia
(neurobiologically meaningful findings), and
those on illogical pictures were correlated with
regional glucose metabolism in the right angular
gyrus.
CONCLUSION
Language is sequences of sound or characters
that carry meanings for communication. There
are two routes, the superficial and deep routes,
with the latter associated with meaning, and three
brain areas are involved: the peri-Sylvian area,
per-peri-Sylvian area, and right hemisphere.
Using these principles, language symptoms of
cases of dementia with progressive non-fluent
aphasia, semantic dementia, Alzheimer’s disease,
and vascular dementia can be understood.
ACKNOWLEDGEMENTS
The author is grateful to Professor Anam
Ong, President of the 4th Asian Society Against
Dementia (ASAD) (Bali, 2010), for inviting me
to write on this topic. The assistance colleagues
Ms. K. Akanuma, M. Meguro, H. Ishii, and S.
Yamaguchi is also appreciated.
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