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Brain Injury
ISSN: 0269-9052 (Print) 1362-301X (Online) Journal homepage: http://www.tandfonline.com/loi/ibij20
Neurological impressions on the organization of
language networks in the human brain
Fabricio Ferreira de Oliveira, Sheilla de Medeiros Correia Marin & Paulo
Henrique Ferreira Bertolucci
To cite this article: Fabricio Ferreira de Oliveira, Sheilla de Medeiros Correia Marin & Paulo
Henrique Ferreira Bertolucci (2016): Neurological impressions on the organization of language
networks in the human brain, Brain Injury, DOI: 10.1080/02699052.2016.1199914
To link to this article: http://dx.doi.org/10.1080/02699052.2016.1199914
Published online: 14 Oct 2016.
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Date: 31 October 2016, At: 01:01
http://tandfonline.com/ibij
ISSN: 0269-9052 (print), 1362-301X (electronic)
Brain Inj, Early Online: 1–11
© 2016 Taylor & Francis Group, LLC. DOI: 10.1080/02699052.2016.1199914
REVIEW ARTICLE
Neurological impressions on the organization of language networks in
the human brain
Fabricio Ferreira de Oliveira
, Sheilla de Medeiros Correia Marin
, & Paulo Henrique Ferreira Bertolucci
Department of Neurology and Neurosurgery, Escola Paulista de Medicina, Federal University of São Paulo (UNIFESP), São Paulo, SP, Brazil
Abstract
Keywords
Background: More than 95% of right-handed individuals, as well as almost 80% of left-handed
individuals, have left hemisphere dominance for language. The perisylvian networks of the
dominant hemisphere tend to be the most important language systems in human brains,
usually connected by bidirectional fibres originated from the superior longitudinal fascicle/
arcuate fascicle system and potentially modifiable by learning. Neuroplasticity mechanisms
take place to preserve neural functions after brain injuries. Language is dependent on a
hierarchical interlinkage of serial and parallel processing areas in distinct brain regions considered to be elementary processing units. Whereas aphasic syndromes typically result from
injuries to the dominant hemisphere, the extent of the distribution of language functions
seems to be variable for each individual. Method: Review of the literature Results: Several
theories try to explain the organization of language networks in the human brain from a
point of view that involves either modular or distributed processing or sometimes both. The
most important evidence for each approach is discussed under the light of modern theories of
organization of neural networks. Conclusions: Understanding the connectivity patterns of
language networks may provide deeper insights into language functions, supporting evidence-based rehabilitation strategies that focus on the enhancement of language organization
for patients with aphasic syndromes.
Linguistics, aphasia, language, speech,
disability evaluation, neural networks
Towards a better understanding of language
lateralization
Lateralization of language functions
Language is dependent on an hierarchical interlinkage of
serial and parallel processing areas in distinct brain regions
considered to be elementary processing units [1,2]; therefore,
language processing takes place mostly in the dominant hemisphere, which is usually the left one. Development of hemisphere dominance for language processing is related to the
specificity of synaptic connections established before and
after birth, but it is still unknown if a specific linguistic
specialization based on experience is required for the functional separation of the hemispheres [1].
The first historical evidence for localization of higher brain
functions arose from studies of language disorders. Since the
end of the nineteenth century, aphasic syndromes had been
considered to be mostly mediated by specialized areas of the
dominant hemisphere of the brain [2]. While localization of
language functions shows little inter-individual variability, it
Correspondence: Fabricio Ferreira de Oliveira, MD, MSc, PhD,
Universidade Federal de São Paulo (UNIFESP), Escola Paulista de
Medicina, Departamento de Neurologia e Neurocirurgia, Rua Botucatu
740, Vila Clementino, CEP 04023-900, São Paulo, SP, Brazil. E-mail:
[email protected]
Color versions of one or more of the figures in the article can be found
online at www.tandfonline.com/ibij.
History
Received 26 May 2015
Revised 22 March 2016
Accepted 6 June 2016
Published online 14 October 2016
is currently known that both hemispheres are functionally
complementary, considering that several brain areas are bilaterally activated when a language task is undertaken [3–5].
Ambidextrous individuals usually have bilateral language
dominance, while those with left, bilateral or right hemisphere language representation do not differ significantly
with respect to verbal fluency, linguistic processing or intelligence, as well as with regard to the homology of anatomical
and functional organization of language networks in either
hemisphere [6]. More than 95% of right-handed individuals,
as well as almost 80% of left-handed individuals, have left
hemisphere dominance for language [7]. Women tend to perform better on language tasks and have bilateral language
representation more often than men, who usually excel in
visual-spatial abilities [8]. Whereas aphasic syndromes typically result from injuries to the dominant hemisphere [9], the
extent of the distribution of language functions seems to be
variable for each individual brain.
A native language and a second language that shares its
universal grammar can assume different region-specific processing rules according to the time when they were learned.
Language lateralization seems to depend on the bilingual
status of the individuals, with bilateral hemispheric involvement for both languages of early bilinguals (who learned such
languages during early infancy), left hemisphere dominance
for language of monolinguals and also left hemisphere dominance for both languages of late bilinguals [10]. If both
2
F. F. de Oliveira et al.
Brain Inj, Early Online: 1–11
languages are learned during infancy, their fluency tends to
activate indistinguishable sites in Broca’s area; however, if
the second language is acquired during adulthood, it is usually
represented in a separate region in Broca’s area [3,11].
The neuroanatomy of language
Three large networks interact to connect language with conceptual information [1]. Broca’s and Wernicke’s areas, the
insular cortex, the head of the caudate nucleus and the putamen in the dominant hemisphere form the language implementation system, which analyses auditory signals to activate
conceptual knowledge and support phonemic and grammatical construction while controlling production of speech. This
system is surrounded by a mediational system, composed of
several regions distributed among the parietal, frontal and
temporal association areas, acting as brokers between the
language implementation system and the so called conceptual
system, a group of regions spread throughout the association
areas. It is remarkable that bidirectionality is an important
attribute of the arcuate fascicle, which connects areas of the
sensory cortex (including Wernicke’s area) with prefrontal
and premotor areas (including Broca’s area) in the dominant
hemisphere [9].
Language networks may be allocated into two different
streams [12]. The dorsal stream for language is composed
by the superior longitudinal fascicle/arcuate fascicle system,
the most important pathway for syntactic analysis and auditory-motor transcoding in the brain [13], which is sometimes
divided into a lexical-semantic pathway and a phonological
pathway, but is currently considered to be domain-general
rather than specialized for language [3,14]. The ventral stream
for language is largely bilaterally organized for parallel processing [15], formed by the uncinate fascicle (involved in
semantic processing and sound recognition), the extreme
capsule (involved in the long-term storage of semantic information and phonological working memory), the middle longitudinal fascicle (involved in phonological and semantic
processing) and the inferior longitudinal fascicle (involved
in object recognition, face processing and visual semantic
memory) [14]. The currently accepted distribution of language networks, along with trajectories of subcortical fascicles may be viewed in a simplified model (Figure 1).
Subcortical structures are also known to contribute to the
organization of language in view of their reciprocal connections with cortical language areas through networks that may
be modified by learning [1,16]. This is particularly true for
the lexical-semantic processing in inferior, lateral and posterior thalamic nuclei and also for the phonetic processing for
fluency in the striatal structures of the dominant hemisphere
[16]. Also, attention and executive functions may be affected
when the thalamus in the dominant hemisphere is injured and
visual-spatial orientation may be particularly impaired when
lesions occur in the thalamic nuclei of the non-dominant
hemisphere [17]; such impairments may affect the linguistic
performance of patients after brain injuries. Disconnection
syndromes may result when lesions involve the thalamus
and the basal nuclei, implicating in subcortical aphasias.
Spoken language is only one of several language skills
mediated by the dominant hemisphere. Contrariwise, affective
Figure 1. Approximate distribution of language networks in the cortex of
the dominant hemisphere with simplified trajectories of subcortical fascicles. AC, primary auditory cortex; AG, angular gyrus; B, Broca’s area; M,
motor networks in the precentral gyrus; PF, prefrontal networks; S, sensory
networks in the postcentral gyrus; SM, supramarginal gyrus; T, inferior
temporal networks and temporal pole; W, Wernicke’s area.
aspects of language such as intonation (prosody) are processed
in the non-dominant hemisphere, mirroring the logical organization of language content in the dominant hemisphere [7]. Irony,
musical interests, metaphors and intentions can only be appreciated when the non-dominant hemisphere is intact [1].
Homologue areas in the non-dominant hemisphere contribute to
‘emotional’ aspects of language, such as the inferior frontal gyrus
of the non-dominant hemisphere for expression of emotions and
the homologue of Wernicke’s area in the non-dominant hemisphere, which acts in the interpretation of human emotions. The
abilities for elaboration of discourse macrostructure and for contextual integration of information are basically non-dominant
hemisphere functions, particularly related to the frontal lobe
[17], as well as the ability for single word reading in patients
recovering from aphasia. Incidentally, even though spatial orienting is usually a function of the visually inspired non-dominant
hemisphere, neglect may also result from acute damage to areas
of the dominant hemisphere that typically serve language functions, namely the superior and middle temporal gyri, the inferior
parietal lobule and the insula [18]; these patients may present both
contralateral neglect and aphasia.
Definition of aphasia
Aphasia is defined as an acquired impairment in language
production and comprehension and in other cognitive processes that underlie language, causing problems with any or
all of the following: speaking, listening, reading, writing and
gesturing abilities [3]. These problems may be characterized
by: impaired fluency; difficulty to understand and/or produce
words; substitution or addition of speech sounds or exchange
of semantically-related words (phonemic or semantic paraphasias, respectively); difficulty to name objects (anomia) or
to recall words during conversation; and impairment in social
Neurological organization of language networks
DOI: 10.1080/02699052.2016.1199914
communication skills (pragmatic language). Reading and
writing are usually affected in patients with aphasia, while
phono-articulatory function and consciousness are relatively
preserved. The most important aphasic syndromes are shown
in Table I, as well as the most likely brain injury sites to result
in these language disturbances [2,19].
Plasticity in the human brain and the benefits of
neurological rehabilitation
Mechanisms of language recovery after injuries to the dominant
hemisphere seem to be relatively stereotyped. There are
increased activations of homologues of language areas in the
non-dominant hemisphere and of perilesional areas of the dominant hemisphere, including compensatory recruitment of new
areas and of language areas that were spared [20]. Sometimes,
there may also be dysfunctional activation of the non-dominant
hemisphere interfering with language recovery due to increased
and deleterious transcallosal inhibition of the already damaged
dominant hemisphere [21]. Nevertheless, uninjured language
areas in the dominant hemisphere seem to present a continuously increased activation, while non-dominant hemisphere
3
homologue areas have a biphasic course with earlier increased
and later decreased activation that is dependent on the amount of
pre-morbid language lateralization [15]. It seems that the areas
recruited for a particular language task change over the course of
recovery, with minimal elicited activation (or haemodynamic
response) during the language task in the acute stage, predominant non-dominant hemisphere activation in the sub-acute stage
and a return to predominant dominant hemisphere activation in
chronic stages for patients who show good recovery of the
task [4,21].
Ictal evaluation of language may be able to localize complex
partial seizure commencement in patients with epilepsy [22] and
some studies with patients who had infancy or adolescence onset
of epilepsy have shown evidence of plastic processes affecting
language lateralization. While speech processes activate bilateral superior temporal regions, there may be convergence to a
right hemisphere dominant pattern for language in some patients
with left mesial temporal sclerosis or neoplastic diseases (interhemispheric reorganization), contrary to what usually happens
in the uninjured brains of right-handed individuals that have
developed left hemisphere dominance [23,24]. In some patients
with epilepsy, reorganization of language results in receptive
Table I. Traditional classification of aphasic syndromes.
Type of aphasia
Spontaneous speech
Fluency
Comprehension Repetition
impaired
preserved
preserved
impaired
Conduction Aphasia normal (phonemic
mistakes)
Global Aphasia
poor (mutism),
restricted to simple
verbal stereotypes
preserved
preserved
impaired
impaired
Semantic Aphasia
preserved
preserved
impaired
preserved
preserved
impaired
Broca’s Aphasia
Wernicke’s Aphasia
Transcortical Motor
Aphasia
Transcortical
Sensory Aphasia
poor, with effort,
paraphasias,
agrammatism
logorrheic, with
paraphasias and
neologisms
normal (difficulty
finding words)
poor (mutism), with
great latency at
responses, echolalia,
perseveration
normal (semantic
jargon)
Mixed Transcortical
Aphasia
mutism
impaired
impaired
Verbal Deafness
normal
preserved
impaired
Thalamic Aphasia
normal or with
paraphasias
preserved
preserved or
discretely
impaired
preserved
Subcortical Aphasia poor, with great latency preserved
(non-thalamic)
at responses, echolalia,
perseveration
impaired
Naming
Other signs
impaired
hemiparesis,
apraxia of mouth
and hand
impaired impaired homonymous
hemianopia,
apraxia,
anosognosia
impaired preserved hemi-hypoesthesia,
apraxia, hemianopia
impaired impaired hemiparesis,
hemianopia, hemihypoesthesia,
apraxia
preserved impaired homonymous
hemianopia
preserved impaired eventually
hemiparesis (crural
involvement) and
grasp reflex
preserved impaired eventually
hemianopia and
visual agnosia
preserved impaired eventually
hemianopia, visual
agnosia and
hemiparesis
impaired preserved absent
Lesion localization
(dominant hemisphere)
posterior-inferior frontal
posterior-superior temporal
arcuate fascicle—
supramarginal gyrus
perisylvian region (middle
cerebral artery territory)
inferior parietal (angular
gyrus)
anterior and superior to
Broca’s area
(supplementary motor area)
preserved impaired
dysarthria, initially
with mutism
watershed areas of middle
cerebral artery and
posterior cerebral artery
watershed areas of middle
cerebral, anterior cerebral
and posterior cerebral
arteries
middle third of superior
temporal gyrus
thalamus in the dominant
hemisphere
preserved impaired
dysarthria,
hypophonia
basal nuclei in the
dominant hemisphere
4
F. F. de Oliveira et al.
and expressive functions showing divergent hemispheric dominance [23], while in others a perilesional (intra-hemispheric)
reorganization may also be seen [24].
Considering that functional communication usually
improves spontaneously over the first months after an acute
brain injury [25], the benefits of early aphasia rehabilitation
are still uncertain. The fact that some patients show better
response to speech and language therapy than others might be
indicative of some unidentified cognitive impairments that
impact their ability to recover from aphasia. Insight into the
processes that underlie recovery from brain injuries is essential for diagnostic and therapeutic approaches, resting on the
need for a deeper understanding of the organization of language networks in the brain.
Several theories try to explain the organization of language
networks in the human brain from a point of view that
involves either modular or distributed processing or sometimes both. The most important evidences for each approach
are briefly summarized in Table II. The aim of this review is
to describe and confront the available theories on this subject,
with the final goal to reach a clearer explanation of the inner
workings of language networks.
Evidence for modularity of language functions
Focal brain lesions affecting language functions
Many brain functions are organized on the basis of modular
localization and activation, such as the localization of function
in sensory and motor systems. Human languages are structured
according to universal principles as well; therefore, why should
language not follow the same modular rules as sensory and
motor systems? In evolutionary terms, modularity of brain
functions allows for the optimization of task performance in
view of faster neural processing of information, but there is
some relativity to the modularity of linguistic processes, even
though they are independent from thought and reason.
Regardless of aetiology, focal brain lesions are the most
important models for the study of correlations between structural changes and linguistic functions. Some focal lesions may
cause aphasia while preserving other cognitive domains, thus
justifying the modular views. Whereas some patients present
with lesions of language areas without aphasia [2], strategic
lesions may produce aphasic syndromes regardless of the injury
size. The angular gyrus in the dominant hemisphere integrates
functions from several other areas of the brain, accounting for
left–right orientation, constructional praxis, naming, reading
and writing (the spatial representation of words), calculations
and finger recognition [26]. A structural asymmetry leads to an
almost 15% greater cortical volume of the dominant angular
gyrus in comparison with the non-dominant one, with extensive
bilateral training-induced neuroplasticity when learning new
skills that require spatial co-ordination and verbal memory or
theory of mind tasks [27]. Calculations are usually associated
with the ability to spontaneously write sentences, while these
functions are usually impaired at the same time in patients with
Alzheimer’s disease dementia, possibly due to dominant angular
gyrus dysfunction [28]. While lesions to the angular gyrus may
result in semantic aphasia, patients with brain lesions often show
double dissociations between their abilities to name objects and
Brain Inj, Early Online: 1–11
actions, suggesting that entity and event knowledge are mediated
by different neural networks [29]. The angular gyrus is involved
in phonemic discrimination and semantic feature knowledge, but
not in mapping from semantics to phonology (a role of inferior
temporal areas) or in reading in the absence of semantic associations [27].
Functional impairment of the insula or subinsular area of
the dominant hemisphere tends to produce phonemic disintegration and disturb speech fluency, resulting in apraxia of
speech and transcortical motor aphasia [30]. Apraxia of
speech has always been described with lesions to the dominant hemisphere, more specifically the left superior precentral
gyrus of the insula, and usually follows non-fluent aphasic
syndromes rather than being a sole finding, but tends to be
more severe when premotor and supplementary motor areas
of the same hemisphere are also involved [31].
Alexia without agraphia refers to impaired reading in the
presence of spared writing and relatively spared recognition of
words spelled aloud, often resulting from a combination of lesions
in the left occipital cortex resulting in right homonymous hemianopia (such that all visual information is initially processed in the
right occipital cortex) and in the splenium of the corpus callosum
preventing visual information in the right hemisphere from being
transferred to the left hemisphere language networks [4]. Lesions
usually include connections of the visual word form area, a
modular area located in the lateral occipitotemporal sulcus of
the dominant hemisphere near the visual object form area, mostly
responsible for orthographic reading-specific processes of the
brain independently of spatial location and partially selective for
written strings relative to other categories such as line drawings
[32,33]. Abilities involved in the rapid parallel letter processing
that is required for skilled reading are lost, but patients may
recover the ability to read short familiar words by way of visual
inputs to the occipital cortex connected to dominant hemisphere
motor and premotor regions via activity in a central part of the
dominant superior temporal sulcus [34]. Many of these patients
are also unable to name visual stimuli, although they can name the
same items from tactile exploration or in response to verbal
description, a pattern known as ‘optic aphasia’ [4] (although not
exactly classified as an aphasic syndrome). Overall, different networks of the dominant hemisphere are responsible for the recognition of orthographic and phonologic stimuli, with predominant
activation of middle temporal and fusiform gyri during reading
tasks (as well as higher connectivity of Broca’s area and of the
fusiform gyrus with the parietal cortex) and of the superior
temporal gyrus during oral language tasks (with higher connectivity of Broca’s area and of the fusiform gyrus with the temporal
cortex) [35].
In cases of lesions in the non-dominant hemisphere, patients
often produce inappropriately stressed speech, with awkward
timing and intonation, and flattened emotionality. These
patients also have difficulty to interpret the mood and emotional
cues in the speech of others and their narrative is usually
incoherent when ordering sentences [1]. Even though dominant
hemisphere involvement is the most important predictor for
aphasia, dysarthria may develop when weakness is present
and may be associated with dysphagia in stroke patients who
are not alert, regardless of the affected hemisphere [36].
Likewise, dysphagia tends to follow communication difficulties
in patients with primary progressive aphasia [37].
DOI: 10.1080/02699052.2016.1199914
Neurological organization of language networks
5
Table II. Evidences for the organization of language functions.
Evidence for modular organization
The dominant hemisphere is specialized in language, while the nondominant hemisphere is skilled for visual-spatial functions.
Individuals with left, bilateral or right hemisphere language representation
do not differ significantly with respect to the anatomical and functional
organization of language.
Aphasic syndromes result from injuries to the dominant hemisphere for
language, whereas some focal lesions may cause aphasia while
preserving cognitive functions.
The superior longitudinal fascicle/arcuate fascicle system connects Broca’s
and Wernicke’s areas and the localization of such structures is relatively
invariant among individuals.
Topographic organization of cortical language areas is reproduced in subcortical structures, such as the thalamus.
Human languages develop according to universal principles that mimic the
localization of function in sensory and motor systems.
Development of hemisphere dominance invariably depends on the
specificity of synaptic connections established before and after birth.
When two languages are learned during infancy, their fluency tends to
activate indistinguishable sites in Broca’s area.
Plasticity of language structures is critical only during infancy and early
adolescence, characterized by its magnitude and by the ease of its
triggering, while stability overcomes flexibility in the adult brain.
The non-dominant hemisphere is recruited only in the sub-acute stage after
an injury to the dominant hemisphere, returning to predominant
dominant hemisphere activation in chronic stages.
The processing of visual information is divided between a dorsal and a
ventral stream that integrate modular structures and the same
mechanisms may be found for the processing of auditory language.
The compensatory potential of the non-dominant inferior frontal gyrus
after brain injuries is less effective than in patients who recover inferior
frontal gyrus function in the dominant hemisphere.
A structural asymmetry leads to an almost 15% greater cortical volume of
the dominant angular gyrus in relation to the non-dominant one.
Different areas of the dominant hemisphere are responsible for the
recognition of orthographic and phonologic stimuli.
The visual word form area and the visual object form area are modularly
involved in reading and semantic processing of visual information,
respectively.
Patients with brain injuries often show double dissociations between their
abilities to name objects and actions, suggesting that entity and event
knowledge are mediated by different modular systems.
Modularity of brain functions permits the optimization of neural
performance in view of faster processing of information.
Linguistic processes are independent from thought and reason in the same
way that musical features are independent from spoken language and
speech, bringing about some patients with non-fluent aphasia being able
to sing while unable to speak.
Language dysfunction in patients with primary progressive aphasias or
Alzheimer’s disease depends on specific structures that are affected by
neurodegeneration.
In general, a direct relationship exists between lesion size and both
language recovery and mortality, whereas strategic lesions may result in
aphasic syndromes, regardless of lesion size.
Evidence for distributed processing
Commissures connect both hemispheres leading to the formation of a wide
network in which functional inter-dependence supplants lateralization.
Converting handedness induces plasticity mechanisms that lead to
re-organization of specific brain areas, while approaches that involve both
hemispheres during language rehabilitation may be more efficacious.
Language networks are distributed throughout both hemispheres in a
complementary rather than in an independent fashion.
Information processing in the superior longitudinal fascicle/arcuate
fascicle system is bidirectional, while motor and sensory aphasias may
sometimes result from injuries to areas that are not primarily involved in
language.
The organization of language networks, as well as reciprocal connections
involving hubs and fibres, may be modified by learning.
Neural networks involved in any function interact in a parallel distribution
while preserving their independence.
Post-natal neuronal plasticity directs the variable formation and
maintenance of active neural connections while pruning the aberrant ones.
If a second language is learned during adulthood, it is usually represented
in a separate region in Broca’s area.
Neuroplasticity may develop in adulthood due to activation of perilesional
areas and to disinhibition of the non-dominant hemisphere when brain
injuries affect the dominant hemisphere.
Activation of the non-dominant hemisphere after an injury to the dominant
hemisphere may be dysfunctional and interfere with language recovery,
suggesting that networks of the non-dominant hemisphere are also
important for language functions.
The streams for processing of visual and auditory information are
distributed along a network of elementary processing units that are interdependent rather that isolated for integration of neural signals.
Recruitment of the non-dominant inferior frontal gyrus reflects the
activation of mirror neurons which are apparently concentrated in the
inferior frontal gyri of both hemispheres.
The non-dominant angular gyrus mimics the organization of the dominant
one and integrates its functions during learning of new skills that require
spatial co-ordination and verbal memory or theory of mind tasks.
Recognition of orthographic and phonologic stimuli depends on the
organization of language networks according to the distribution of specific
hubs and fibres.
Lesions of the inferior longitudinal fascicle that affect object recognition
or orthographic processes are usually temporary and compensated by
neuroplasticity mechanisms.
Improvements in naming and comprehension may be susceptible to
performance in non-linguistic domains such as attention, abstraction and
visual-spatial working memory, translating into multiple brain regions
being simultaneously required for language functions.
Performance in neural tasks is related to the connectivity between key
cortical regions and a network of parallel processing areas that act in an
integrated form to support the hierarchical organization of language.
Rhythmic acoustic and social cues mediated by the mirror neuron system
may be responsible for the enhancement of speech networks in patients
with aphasia.
Connectivity disruption is the primary mechanism leading to language
dysfunction in neurodegenerative diseases.
Even though the reduced functional segregation in the ageing brain may
result in greater susceptibility to functional impairment, language
performance after brain injuries is modulated by mechanisms related to the
formation of a ‘linguistic reserve’ (such as education and bilingualism).
Patients with injuries to the dominant hemisphere specifically present with The enhancement of emotional behaviours with social communicative
an increased visceral-autonomic response to stimuli.
purposes is mediated by the interaction between both hemispheres.
6
F. F. de Oliveira et al.
Processing of visual and auditory signals
It has been shown that the processing of visual information is
divided into two main streams: the ‘what’ pathway, a ventral
occipital to temporal stream specialized in object identification
and lexical activation for familiar words; and the ‘where’ and
‘how’ pathways, composing a dorsal sub-lexical stream that
examines spatial positions, motion and translations of spelling
to sounds for less familiar letter strings. The dorsal stream is
divided into a pathway for spatial processing (occipital to
superior dorsal parietal) and another pathway that represents
semantic information about person–object interactions (occipital to middle dorsal parietal and frontal). In other words, object
identification modularly activates the parahippocampal and
occipitotemporal gyri, while lexical-based reading modularly
activates the lingual, lateral occipital and posterior inferior
temporal gyri—basically, modular activation of single structures with little shared activation in the ventral stream (dominant posterior inferior frontal gyrus); on the other hand, object
interaction processing and phonetic decoding largely activate
modular dorsal regions in both hemispheres, as well as several
shared distributed processing regions (precentral gyri, superior
posterior temporal gyri and the following regions in the dominant hemisphere: inferior frontal cortex, postcentral gyrus and
lateral occipital cortex) [38]. Analogically, the following dual
stream model for auditory language processing has been suggested: a dorsal phonological stream in the superior longitudinal fascicle/arcuate fascicle system between superior temporal
and prefrontal regions in the dominant hemisphere is the most
relevant pathway for production of speech (mapping sound to
articulation), while a ventral semantic stream in the extreme
capsule connecting the middle temporal lobe with the ventrolateral prefrontal cortex is relevant for comprehension (mapping sound to lexical concepts) [14,18].
Audiovisual speech comprehension is an interactive process that results from the integration of auditory and visual
signals progressively constrained by stimulus intelligibility
along the superior temporal structures of the dominant hemisphere in conjunction with a spectrotemporal structure in a
dorsal frontotemporal circuitry [39]. Furthermore, the inferior
longitudinal fascicle links the visual cortex with the visual
object form area, a modular area located within the basal
occipitotemporal region which is involved in object recognition, but language disturbances due to lesions of this fascicle
are usually temporary and compensated by neuroplasticity
mechanisms [40].
Neurodegenerative mechanisms underlying modular
systems
The presentation of neurodegenerative diseases usually comprises language disturbances as a major feature. Visual confrontation naming, reading comprehension and auditory
comprehension are usually impaired in mild stages of
Alzheimer’s disease dementia, further leading to fluency deficits and eventually mutism in late stages [41]. Verb production deficits in Alzheimer’s disease dementia are more driven
by semantic than by executive impairment, with double dissociation between verb (frontal) and noun (temporal) production [42]. Whereas lower frequency words and pseudowords
Brain Inj, Early Online: 1–11
tend to elicit larger parietal activities [43], a correlation
between cognitive decline and the loss of integrity of microstructural white matter connectivity involving the superior
longitudinal fascicle has been established in patients with
Alzheimer’s disease [44]. Still, posterior cortical atrophy is
a focal presentation of Alzheimer’s disease with occipitotemporal hypometabolism that, when involving the dominant
hemisphere, may be clinically characterized by progressive
fluent aphasia with prominent visual-spatial deficits and loss
of insight [45].
Primary progressive aphasias constitute models that tend
to support the modular theories of language organization.
These syndromes are characterized by progressive loss of
language functions with initial sparing of other cognitive
domains, resulting from a circumscribed atrophic process in
language areas leading to connectivity disruption involving
white matter and grey matter loss [46] and are classified
into the following variants: agrammatic, semantic or logopenic [47]. The logopenic variant of primary progressive
aphasia, with hesitant anomic speech, word retrieval and
sentence repetition deficits, features left posterior perisylvian or parietal atrophy, endorsing the role of the inferior
parietal cortex in phonological loop functions and usually
evolves to Alzheimer’s disease dementia in advanced stages
[48]. In comparison, apraxia of speech is one of the initial
features of agrammatic primary progressive aphasia, which
typically involves the left posterior frontoinsular region, is a
better predictor of a tauopathy and may evolve to frontotemporal dementia and corticobasal degeneration in later
stages [49], with initial impairments in phonological processing further leading to severe aphasia [50]. The semantic
variant of primary progressive aphasia leads to early involvement of the anterior temporal lobes (predominantly in the
left), is associated with ubiquitinated inclusions and usually
evolves to the classical form of semantic dementia or to
behavioural variant frontotemporal dementia [51]. Lexicalsemantic impairment is associated with greater atrophy of
the dominant hemisphere, whereas a degradation of knowledge about people, including progressive prosopagnosia,
has been seen in patients with more widespread temporal
atrophy in the non-dominant hemisphere [52]. Features that
differentiate the variants of primary progressive aphasia in
early stages may lose their distinctiveness as the degeneration spreads [53].
Right posterior superior temporal sulcus structures have
increased activity both in patients with primary progressive
aphasia and in those with Alzheimer’s disease dementia,
correlating positively with performance in language tasks
[54]. However, in view of the underlying neurodegenerative
mechanisms, the effectiveness of rehabilitation strategies
tends to be very limited.
Prognostic implications
Language networks are so important for daily living that a
direct relationship exists between lesion size and both language recovery and mortality [21,25,55–57]. Global aphasia
is usually a stronger predictor of mortality for stroke patients
when present in the acute phase than other language disorders
DOI: 10.1080/02699052.2016.1199914
[55], also bringing an unfavourable prognosis to post-stroke
mobility recovery, something that could be phylogenetically
related to the simultaneous development of language networks and motor gesture activity in earlier primates
[25,55,58].
Age, education, depression, lesions in the dominant hemisphere and cortical injuries are other important prognostic factors for language recovery after a first stroke [25,57,59,60],
leading to some variability in language impairments according
to lesion topography. Although healthy ageing shifts from a
more distributed (in young adulthood) to a more localized topological organization of language networks [61], older people
display reduced modularity of neural networks that may be
indicative of reduced functional segregation in the ageing
brain, with diminished connectivity in modules corresponding
to executive functions and the default mode network [62], resulting in greater susceptibility to functional impairment after brain
injuries. On the other hand, education may lead to distinct
communication forms that allow some high schooling patients
with aphasia to communicate better than low schooling individuals without brain injuries. Along with other environmental
and cultural influences, schooling might modify brain organization and connections between cortical structures in both hemispheres, leading to better performance in language tests and also
protecting patients from post-stroke dementia. Bilingualism is
able to delay the onset of various forms of dementia by more
than 4 years independently of education [63], probably due to
stronger requirements from executive functions and attentional
networks that lead to greater cognitive reserve. It has also been
demonstrated that the better the response to language tests
involving writing, the likelier it is for a patient with a non-fluent
aphasia to have a good evolution [64].
When patients with aphasia present with cerebrovascular
subcortical injuries, prognosis is much more favourable the
less likely one is to find that there has been cortical hypoperfusion [25,60]. Lesion size and cortical hypoperfusion in
the acute phase are significant risk factors for bad prognosis
of aphasia. Even though lesion size is an important prognostic
factor for depression and language recovery [25], more notably if there is salvageable tissue (penumbra) involved [65],
lacunar infarctions and leukaraiosis are also able to aggravate
language dysfunction [66].
It is believed that recovery of language after stroke is
primarily produced by arterial recanalization or expansion
of collaterals, giving rise to an enhanced flow in the hypoperfused cortical penumbra [67] and secondarily by mechanisms related to the disinhibition of the uninjured hemisphere
[68]. Nevertheless, the speed of language rehabilitation in
adults is much slower than in children, since structural stability overcomes plasticity in the adult brain [69]. Despite the
critical role of reperfusion of ischaemic brain tissue in the
restoration of normal function [7], it can paradoxically result
in reperfusion injury [70]. The dominant hemisphere supposedly modulates the inhibition of the activation of arousal
systems by the non-dominant hemisphere and enhances emotional behaviours with social communicative purposes, so that
patients with injuries to the dominant hemisphere have an
increased visceral-autonomic response to stimuli, more specifically if aphasic syndromes are present; this leads to phenomena such as the catastrophic reaction, an emotional
Neurological organization of language networks
7
outburst which is almost exclusively present in the acute
stroke phase when the dominant hemisphere is injured and
aphasia is present [71].
According to the ‘modular’ view, the distributed patterns
of brain activity that are observed in some studies could be
explained by the fact that other areas unoriginally related to
language would respond to linguistic stimuli in an incidental
way, echoing the neural processing of information with no
functional contribution to language. Nonetheless, the hierarchical distribution of linguistic processing of information
seems to be the only model to be able to integrate all data in a
timely manner for human comprehension and expression.
Evidence for distribution of language functions
Shared network functioning for language
Is language acquisition innate or merely the learning of lexical and constructional forms of communication? It is possible that the principles that organize language in the brain are
shared with other cognitive domains, thus allowing for a more
distributed network of processing units that are integrated by
way of such principles. For instance, individual reading performance may be related to the connectivity between key
cortical regions both in upstream visual association areas
(defining shapes of words) and in downstream visual association cortical areas (defining the lexical identity of words) and
a network of parallel processing areas that act in an integrated
form to define the meanings of words and support the hierarchical organization of language [35]. It has been proposed
that the ventral and dorsal processing streams for networks
involved in visual and in auditory processing interact in a
parallel distribution while preserving their dual independence [72].
Logical inference recruits neural networks that are independent of the dominant perisylvian regions traditionally
associated with language, leading to deductive reasoning;
nonetheless, some general ‘support’ areas in the frontoparietal
cortex of both hemispheres tend to be commonly recruited as
well [73]. Superior parietal regions are examples of such
‘support’ areas, usually associated with executive functions
related to information update, maintenance of order relations
and spatial attention, particularly when multi-element processing is required, and possibly being implicated in representations of the structure of arguments, whereas the left superior
parietal lobule contributes to letter string (identity) processing
along with the left ventral occipitotemporal area [73,74].
The meanings of words and sentences seem to be
grounded in functional networks for action and perception.
Somatotopic activation of the precentral gyrus has been
described when subjects perceive words and sentences
semantically related to bodily actions involving the face,
arms or legs, whereas semantic information about constituent
parts of sentences (especially action verbs) is manifest in the
brain response, suggesting that these elements contribute to
the meaning of the whole sentence [75]. A double dissociation seems to exist between syntactic gender and naming
processing, the former involving the dominant inferior frontal
and posterior middle temporal gyri, while a sub-part of the
dominant superior longitudinal fascicle lateral to the caudate
8
F. F. de Oliveira et al.
nucleus underlies a distributed cortical–subcortical circuit
which might selectively subserve grammatical gender processing [76]. Serial and parallel processing seem to be involved
in the neurophysiological indexes of lexical-syntactic, semantic and deep syntactic processes emerging both in sequence
and at times near simultaneously in written and spoken language processing [77].
Studies in different languages are useful for a better understanding of word processing systems. It has been suggested
that morpheme selection and word selection overlap in time
and influence each other in the Chinese language, while
imageability does not impact the performance of patients
with brain injuries, leading to the conclusion that there is a
morphological level of representation in the Chinese word
production system with non-semantic routes for reading
[78]. A study with Japanese morphograms (kanji) and syllabograms (kana) showed that alexia is complete only when the
lesion involves the dominant angular gyrus together with the
adjacent lateral occipital gyri; while transposition errors suggested disrupted sequential phonological processing from the
angular and lateral occipital gyri to the supramarginal gyrus,
substitution errors suggested impaired allographic conversion
between characters attributable to dysfunction in the angular
or lateral occipital gyri [79]. In any language, it seems that the
dominant occipitotemporal region (the ventral pathway for
reading) is specialized in automatic parallel word recognition,
whereas the dominant parietal lobe (the dorsal pathway) is
specialized in serial letter-by-letter reading and both pathways
are modulated by character spacing [80]. While imagery
impacts single-letter production, the contextual production
of words may rely mostly on retrieval of learned scripts.
The study of letter position dyslexia in Arabic (an orthography in which letters have different forms in different positions
of each word) has shown that letter form in this alphabet is
part of the information encoded in the identity of the abstract
letter, affecting processes for recognition of words [81]. Thus,
reading and writing seem to rely upon different neural networks that act in concert for such linguistic abilities.
Plasticity mechanisms and rehabilitation
Converting handedness tends to induce plasticity mechanisms
that lead to reorganization of specific brain areas. When forced
to use the right hand, left-handers show an increase in movement-related activity in the primary sensorimotor hand areas and
posterior premotor cortex of the left hemisphere associated with
the relative left-to-right shift in hand preference [82]. During
skill learning, involvement of the ipsilateral hemisphere may
influence the magnitude of inter-manual transfer, regardless of
the degree of handedness, which suggests that approaches that
involve both hemispheres during language rehabilitation may be
more efficacious [83]. Occupation-based approaches, matching
what is trained with what the person has to do in daily situations, also tend to be more cost-effective [84]. Similarly,
patients with traumatic brain injuries seem to benefit in
reading efficiency when simultaneously listening to and
reading written passages (text-to-speech technology), combining reading and comprehension performances [85].
Improvements in naming and comprehension may be susceptible to performance in non-linguistic domains such as
Brain Inj, Early Online: 1–11
attention, abstraction and visual-spatial working memory
[86], translating into multiple brain regions being simultaneously required for language functions, even though verbal
and spatial domains activate different hemispheres when
memory tasks are undertaken (dominant and non-dominant
hemispheres, respectively).
The dominant fusiform gyrus was previously directed to
specialize in object processing for children, who learn to read
by way of the recycling hypothesis: according to this hypothesis, plastic neuronal changes leading to word representations
in the dominant fusiform gyrus occur in the context of strong
restrictions that were evolutionarily imposed to this cortical
area [33]. For patients with aphasia, it is possible that such
mechanisms might also develop in the adult non-dominant
hemisphere when it is exposed to rehabilitation therapy.
Aphasia is caused by stroke in more than 80% of all cases
[2]. Recovery and reorganization of language networks is usedependent and must be achieved by the active participation of
patients as much as possible [87].
Sub-acute and chronic plasticity mechanisms may be
detected in patients with insidiously evolving brain tumours.
Tumour invasion, surgical stress, radiation and chemotherapy
are triggers for neural reorganization that may elicit perilesional or mostly contralateral hemisphere recruitment, with
chronic reshaping of language networks [88]. Plasticity of
white matter language networks has also been described
following anterior temporal lobe resections in patients with
refractory epilepsy [89].
Musical features are usually processed in brain areas
which are different from the ones related to spoken language
and speech, bringing about some patients with non-fluent
aphasia being able to sing, while unable to speak [90].
Melodic intonation therapy results in an increase in white
matter fibres and volume in the non-dominant arcuate fascicle
correlating with patient improvement [21]. Rhythmic acoustic
and social cues may be responsible for the enhancement of
speech networks for such patients, possibly involving the
mirror neuron system in the context of neural networks distributed throughout the non-dominant hemisphere [90,91].
The non-dominant hemisphere for language has a critical role
during recovery from aphasia, probably related to the lexical
learning itself present in healthy subjects and to mechanisms of
brain plasticity; recruitment of networks in the non-dominant
hemisphere is believed to occur concurrently with attempts to
repair the damaged original language networks in patients with
aphasia [5,55]. It is generally accepted that there is greater
activity in the non-dominant hemisphere in post-stroke aphasia
compared to healthy subjects, subject to modulation by therapy
and verbal learning. Nevertheless, it has been shown that the
supplementary motor area in both hemispheres, traditionally
involved in preparatory processing, is particularly activated
when patients try to speak aloud auditorily presented stimuli or
even during silent verb generation, suggesting that this area is
part of a language network that includes a sub-vocal rehearsal
system and a phonological store [5]. The additional activation of
non-dominant hemisphere regions may be interpreted as further
involvement of functionally connected and parallel processing
networks which, while holding some importance for speech, are
usually not needed for language processing in the uninjured
brain.
Neurological organization of language networks
DOI: 10.1080/02699052.2016.1199914
Concerning rehabilitation strategies, the theory of the mirror neuron system implies in understanding others’ actions by
means of an automatic matching process that links observed
and performed actions. Mirror neurons discharge during the
execution of goal-directed manual and oral actions, as well as
during the observation of the same actions undertaken by
other individuals [58]. The most important areas in which
mirror neurons seem to be located in humans are those that
are activated during observation and execution of speech,
such as the inferior precentral gyrus, the inferior parietal
lobule and the pars opercularis of the inferior frontal gyrus
[92]. In view of the fact that words whose retrieval is facilitated by gestures are more likely to be analogically encoded in
a multimodal representation including sensorimotor features
that involve both brain hemispheres, it is likely that action
observation leads to organizational changes in the brain and
may participate, via the mirror neuron system, in the relearning of language fluency and comprehension [58,92].
The inferior frontal gyrus is an important element for
language recovery after a stroke. Activation of the non-dominant inferior frontal gyrus seems to be essential for word
retrieval from long-term memory for some patients with
vascular aphasic syndromes and also for lexical learning in
individuals without brain injuries [93], although its compensatory potential appears to be less effective than in patients
who recover inferior frontal gyrus function in the dominant
hemisphere [94]. This could reflect the activation of mirror
neurons which are apparently concentrated in the inferior
frontal gyri of both hemispheres, since patients with left
inferior frontal lesions tend to recruit the right inferior frontal
gyrus more reliably than those without such lesions [20]. In
patients with fibromyalgia, the inferior frontal gyrus of the
dominant hemisphere is a key area involved in the lessening
of verbal fluency [95].
Parallel processing of linguistic codes
The parallel distributed processing model for semantic cognition has a feed-forward structure, so that its activation is
hierarchical and unidirectional from units that represent
items and relations, passing through intermediate hubs, to
an output layer that completes the tasks [96]. The knowledge
in such an interactive processing system is stored in the
strength of its connections and gradually acquired through
experience, susceptible to neurodegenerative mechanisms
that may degrade its patterns of neural activity [68].
It appears that parallel processing of linguistic data is what
determines the speed with which information encoding can
take place in the brain. The ability to conjure all the features
of objects, faces and shapes, while simultaneously giving
meaning and being able to express oneself with regard to
such elements, is a unique human characteristic that could
not take place if serial processing were the only way to handle
information.
Conclusions
The opposing views of localization of language functions
versus the flexibility of distributed processing find an outcome
on the fact that several elementary processing units work in an
9
integrated way to generate human language. Even though serial
and parallel processes link these elements toward unified
operations, there is no doubt that little inter-individual variation may be found for the localization of such units, while the
perisylvian networks of the dominant hemisphere tend to be the
most important language systems in human brains.
Understanding the connectivity patterns of language networks
may provide deeper insights into language functions. The data
contained in this study might help substantiate evidence-based
rehabilitation strategies focusing on the enhancement of language organization for patients with aphasic syndromes.
Declaration of interest
The authors acknowledge the financial support by FAPESP – The
State of São Paulo Research Foundation (grant #2015/10109-5).
The authors report no conflicts of interest. The authors alone are
responsible for the content and writing of the paper.
ORCID
Fabricio Oliveira http://orcid.org/0000-0002-8311-0859
Sheilla Marin http://orcid.org/0000-0002-0381-3221
Paulo Bertolucci http://orcid.org/0000-0001-7902-7502
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