Journal of Neurolinguistics 28 (2014) 6380

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Journal of Neurolinguistics
journal homepage: www.elsevier.com/locate/
jneuroling

Review

Bilateral representation of language: A critical

review and analysis of some unusual cases
Byron Bernal a, Alfredo Ardila b, *
a
b

Department of Radiology/Research Institute, Miami Childrens Hospital, Miami, FL, USA

Department of Communication Sciences and Disorders, Florida International University, Miami, FL, USA

a r t i c l e i n f o

a b s t r a c t

Article history:
Received 19 August 2013
Received in revised form 26 September 2013
Accepted 14 October 2013

It is well known that for right-handed individuals, language is

usually and mostly associated with the left hemisphere activity.
The question of the potential bilateral representation of language,
however, has been barely approached. The evidence regarding the
bilateral representation of language taken from Wada test, PET,
fMRI, tractography, and magneto-encephalography is examined.
Departing from the modularity concept and data ow computing
models, two classications topographic and functional of potential language lateralization patterns are proposed; it is pointed
out that language can be bilaterally represented in different patterns, accordingly with the distribution of the main domains
(expressive vs. receptive) and their subfunctions; and with respect
to different modalities of data ow. Five illustrative cases of
bilateral representation of language are presented. It is concluded
that language dominance is mostly a matter of hemispheric
advantage for a specic cognitive function.
2013 Elsevier Ltd. All rights reserved.

Keywords:
Brain asymmetry
Language
Laterality
Brocas area
Wernickes area
fMRI

1. Introduction
Over one century ago, it was well established that for right-handed individuals, language is usually
and mostly associated with the left hemisphere activity (Broca, 1861, 1865; Dejerine, 1914; Wernicke,
1874). These early ndings were based on clinical-pathological observations but have been replicated

* Corresponding author. Department of Communication Sciences and Disorders, Florida International University, 11200 SW
8th Street, AHC3-431B, Miami, FL 33199, USA. Tel.: 1 305 348 2750; fax: 1 305 348 2740.
E-mail address: ardilaa@u.edu (A. Ardila).
0911-6044/$ see front matter 2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.jneuroling.2013.10.002

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B. Bernal, A. Ardila / Journal of Neurolinguistics 28 (2014) 6380

in extensive studies using the intracarotid amytal test (so-called Wada test) (e.g., Kurthen et al., 1994;
Loring et al., 1999; Mddel, Lineweaver, Schuele, Reinholz, & Loddenkemper, 2009; Woermann et al.,
2003). Modern modalities of non-invasive neuroimaging and electro-physiology procedures have
validated those initial ndings as well: fMRI (e.g., Binder, 2011; Holland et al., 2007; Price, 2010), near
infra-red spectroscopy (Bembich, Demarini, Clarici, Massaccesi, & Grasso, 2011; Bisconti, Di Sante,
Ferrari, & Quaresima, 2012; Kennan, Kim, Maki, Koizumi, & Constable, 2002), magnetoencephalography (Kadis et al., 2011), and diffusion tensor imaging/tractography (Matsumoto et al.,
2008; Powell et al., 2006; Rodrigo et al., 2008). However the question of bilateral representation of
language has been barely approached.
The departure question in examining the bilateral representation of language is up to what extent
the right hemisphere can hold language functions. Knecht et al. (2000) measured language lateralization in 326 healthy individuals with functional transcranial Doppler sonography (a non invasive
technique measures the velocity of blood ow through the brains blood vessels using pulsed Doppler
transducer - ultrasonic pulse probe that detects the reected sound from moving blood) utilizing a
word-generation task. The incidence of right hemisphere language dominance was found to increase
linearly with the degree of left-handedness, from 4% in strong right-handers (right handedness
score 100) to 15% in ambidextrous individuals and 27% in strong left-handers (handedness 100).
However, this technique may be inuenced by expertise or research bias because of the potential poor
insonation conditions (Lorenz et al., 2008). Indeed, in a study with 150 healthy subjects (75 lefthanders and 75 right-handers), left-handers exhibited right language dominance in 77.3% of cases
while bilateral representation was observed in 14.7%, and left dominance in 8% of the subjects; 93.3% of
right-handers showed left side dominance, and 6.7% showed bilateral language representation (Basic
et al., 2004).
Khedr, Hamed, Said, and Basahi (2002) assessed language lateralization in normal subjects (25
right-handed and 25 left handed) using transcranial magnetic stimulation. The authors further subdivided the groups into strongly right-handed, moderately right-handed, strongly left-handed,
moderately left-handed and ambidextrous. In the strong right handed subjects, 87% of subjects
showed only language disruption with left hemisphere stimulation, while 8.2% exhibited disruption
with stimulation in either hemisphere. 4.2% of subjects had disruption with stimulus in the right
hemisphere. In strongly left-handed subjects, 73.7% of subjects had left hemisphere dominance, 15.8%
had bilateral representation and 10.5% had right side dominance. In ambidextrous subjects bilateral
representation was observed in 57% of cases. The authors concluded that speech lateralized to the leftside cerebral dominance in strongly right- and left-handed subjects, but bilateral cerebral representation was frequent in mixed handedness and right-sided cerebral dominance rarely occurred.
2. Normal and anomalous right-sided lateralization of language
In 1865, at a meeting of the Socit de Anthropologie de Paris Paul Broca explicitly stated: "Nous
parlons avec lhmisphre gauche"d"We speak with the left hemisphere. (Harris, 1999). Since then, it
has been accepted that the left hemisphere plays a central role in language. Furthermore, Broca (1865)
assumed that left-handers are the mirror-reverse of right-handers for cerebral control of speech, with
the right hemisphere being dominant in left-handers, and the left hemisphere dominant in righthanders. This hypothesis has been referred as conjunction hypothesis (Harris, 1991) and was
considered valid during the late XIX century. Nonetheless, it was later observed that aphasia can also be
associated with right hemisphere damage in dextrals; this type of aphasia is known as crossed
aphasia and was initially described by Bramwell in 1899. Bramwell applied this term to two different
conditions: (a) aphasia in a left-hander with right hemiplegia; and, (b) aphasia in a right-handed individual with left hemiplegia; that is, an aphasia resulting from a cerebral lesion ipsilateral to the
dominant hand. Noteworthy, just a few crossed aphasics were right-handers, but most were lefthanders. He considered that crossed aphasia is relatively frequent as a transient disorder, but it is
extremely unusual as a permanent syndrome; in this latter case, it is only found in left-handers. Hcaen
& Albert (1978) suggested that the term crossed aphasia should be used only to refer to aphasia
following right hemisphere pathology in a right-handed person, and this is the way the term crossed
aphasia is currently used (Ishizaki et al., 2012; Marin, Paghera, De Deyn, & Vignolo, 2004).

B. Bernal, A. Ardila / Journal of Neurolinguistics 28 (2014) 6380

65

The incidence of crossed aphasia is very low (Coppens, Hungerford, Yamaguchi, & Yamadori, 2002).
Hcaen, Mazurs, Ramier, Goldblum, and Merianne (1971) estimated an incidence of 0.38%; while
Benson and Geschwind (1973) proposed a gure of approximately 1%. In large clinical samples, it has
been found to be around 4% in the acute stage and 1% in the chronic stage (Pedersen, Jargensen,
Nakayama, Raaschou, & Olsen, 1995). It is generally accepted that crossed aphasia represents no
more than 3% of all cases of aphasia (Ha, Pyun, Hwang, & Sim, 2012). Some authors, however, have
suggested that the incidence of crossed aphasia could be even lower (Ardila, 2006; Castro-Caldas &
Confraria, 1984).
Right-hemisphere lesions, however, have been found more frequently associated with aphasia in
left-handed individuals (Basso & Rusconi, 1998). Some authors have reported that up to 50% of lefthanders with right hemisphere lesions present aphasia, although currently the accepted percentage
is notoriously lower. Indeed, left hemisphere damage in left-handers may be associated to aphasia in
more than 50% of cases (Benson & Ardila, 1996). The aphasia prole in left-handers in general is similar
between right and left-handers; although it has been suggested that left-handed aphasics are less
impaired in comprehension and writing, but they have reading disorders more frequently than righthanded aphasics (Hcaen & Sauguet, 1971). Comparing the aphasia due to right and left hemisphere
pathology in left-handed individuals, just minor differences are found. By the same token, comparing
aphasia recovery in right- and left-handed individuals, only small and non-signicant differences are
found (Basso & Rusconi, 1998), regardless that in the past it was accepted that aphasia recovery is better
in left-handers.
Left hemisphere structural pre- and peri-natal lesions (Staudt et al., 2002), developmental tumors
(Anderson et al., 2002), vascular malformations (Vikingstad et al., 2000), and focal pre- and post-natal
intractable epilepsy (Hadac, Brozov, Tintera, & Krsek, 2007; Ligeois et al., 2004) are also associated
with right hemisphere activation in language tasks. Transferring of language functions from left to right
hemisphere has been reported in numerous articles after stroke and tumors of the left hemisphere
(e.g., Holodny, Schulder, Ybasco, & Liu, 2002; Kosla et al., 2012; Tyler, Wright, Randall, Marslen-Wilson,
& Stamatakis, 2010; Weiller et al., 1995). All these studies show right hemisphere overtake of homotopic areas after injury of language eloquent areas in the left hemisphere.
Hickok and Poeppel (2004, 2007) have proposed a new framework for understanding aspects of the
functional anatomy of language. This framework assumes that early cortical stages of speech perception involve auditory elds located bilaterally although asymmetrically in the superior temporal
gyrus. Normal language acquisition sets up a degree of bilateral representation in the superior temporal gyrus, contributing to the formation of more widely distributed conceptual representations. This
cortical processing system then diverges into two streams, (1) a ventral stream, which is involved in
mapping sound onto meaning, and (2) a dorsal stream, which is involved in mapping sound onto
articulatory-based representations. The ventral stream projects toward the posterior middle temporal
gyrus; while the dorsal stream projects dorso-posteriorly involving a region in the posterior Sylvian
ssure at the parietal-temporal boundary, and ultimately projecting to the frontal regions.
3. Right hemisphere involvement in language across life span
Neuroimaging studies have supported the assumption that since early in life, language is predominantly processed by the left hemisphere (Dehaene-Lambertz, Dehaene, & Hertz-Pannier, 2002).
However, it has also been found that the degree of lateralization increases in the rst years of life.
Holland et al. (2001) studied a group of healthy children between 7 and 18 years, nding increasing left
lateralization across these ages. In a detailed study, Szaarski, Holland, Schmithorst, and Byars (2006)
found a statistical signicant positive correlation between age in children (range 517 years) and
lateralization indexes for Brocas area. Similar ndings of progressive lateralization of language to the
left hemisphere mostly related to the expressive language system are reported by Lidzba, Schwilling,
Grodd, Krgeloh-Mann, and Wilke (2011). Language progressive lateralization in childhood may be
related to the maturation of the corpus callosum (Allen, Richey, Chai, & Gorski, 1991).
Groen, Whitehouse, Badcock, and Bishop (2012) used functional transcranial Doppler ultrasound for
assessing cerebral lateralization for language production and for visuospatial memory; they selected 60
typically developing children (ages six and 16 years). The expected pattern of left-lateralized activation

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B. Bernal, A. Ardila / Journal of Neurolinguistics 28 (2014) 6380

for language and right-lateralized activation for visuospatial abilities was found in 58% of the children.
No age-related change in direction or strength of lateralization was found for language production. The
authors also tested the hypothesis whether having language and visuospatial functions in the same
hemisphere was associated with poor cognitive performance; no evidence for this functional
crowding hypothesis was found. They, however, observed that children with left-lateralized language
production had higher vocabulary and nonword reading age-adjusted standard scores than other
children, regardless of the laterality of visuospatial memory. They concluded that there is a link between language function and left-hemisphere lateralization that cannot be explained in terms of
maturational changes.
Interestingly, lateralization of language seemingly presents some changes during senescence. More
activation of the right hemisphere during language comprehension and production tasks has been
reported among elderly participants. This observation suggests that the degree of language lateralization decreases with age, and the required cognitive processes become more symmetrical over time
(Wingeld & Grossman, 2006).
Cabeza (2002) proposed the so-called HAROLD model (Hemispheric Asymmetry Reduction in Older
Adults). This model is based on functional neuroimaging and other evidence in the domains of episodic
memory, semantic memory, working memory, perception, and inhibitory control. It was further proposed that age-related hemispheric asymmetry reduction may have a compensatory function or may
reect a dedifferentiation process, having a cognitive or neural origin.
From all the aforementioned studies it seems that the right hemisphere may also hold language
functions either as a functional variant (as in some left handers), as a developmental feature (extremes
of life span) or as an adaptative response to pathology.
4. Bilateral brain representation of language
Different procedures have used to analyze the brain representation of language. These procedures
in general have yielded relatively similar results.
4.1. Wada test
The history of language lateralization has been partially dominated by the Intracarotid Amobarbital
Test described in Japan by J.A. Wada in 1949, but most popular since the 1960s and 1970s. This
technique consists of the injection of an anesthetic (sodium amobarbital) in one of the internal carotids
with the aim to anesthetize a single hemisphere. The subject should experience contralateral hemiplegia, without loss of consciousness. At this point the subject is examined to detect language and
memory decits. After a break, the other carotid artery is also injected and the language and memory
tests are repeated.
Table 1 summarizes a selective review of ve major publications in bilateral Wada tests. It totalizes
1799 bilateral Wada studies in 1446 right-handers and 353 subjects either left-handed or ambidextrus.
Although there is inhomogeneity in the procedures, classication and methods to determine brain
lateralization, the review shows similar distribution of language lateralization categories. In average,
bilateral representation of language is found in 10% of right-handers and in 27% of not right- handers.
From these early studies, there has been attempts to formulate a classication for bilateral language
dominance, that may describe the sometimes perplexing ndings of the Wada test. Kurthen et al.
(1994) described ve categories, based on lateralization indexes: (1) left dominant, (2) right dominant, (3) incomplete left, (4) incomplete right, and (5) strongly bilateral. In this classication, incomplete left, incomplete right and strongly bilateral are subtypes of bilateral representation of language.
Qualitatively, the bilateral representation of language, may be also divided in three subgroups,
accordingly with the patients performance in the Wada test: Positive, negative, and general. Bilateral
positive representation occurred when the subject has incomplete loss of language on one side but lack
of language impairment on the other; Bilateral negative representation occurred when incomplete loss
of language was present on one side and complete loss on the other; General bilateral representation
occurred when partial language loss was present on both sides. In the analysis of the paper, and with
the aim to take into account patterns of language dissociation between the hemsipheres, Kurthens

Table 1
Bilateral language representation by Wada studies (selective review).
No.
Sjcts

Hand (R) : (L)

Left-H
Dom %

Right H
Dom %

Bilat
Dom %

Suggested classication of
bilateral representation

Rasmussen and
Milner (1977)
Kurthen et al. (1994)

262

140 : 122

96
70
77
23

(R)
(L)
(R)
(L)

4 (R)
15 (L)
4 (R)
32 (L)

0
15 (L)
19 (R)
45 (L)

None

173

142 : 31

Risse, Gates, and

Fangman (1997)

368

304 : 64

87 (R)
62 (L)

4 (R)
18 (L)

9 (R)
20 (L)

Loring et al. (1999)

551

469 : 82

86 (R)
48 (L)

5 (R)
29 (L)

9 (R)
23 (L)

Mddel et al. (2009)

445

391 : 54

82 (R)
48 (L)

4 (R)
22 (L)

14 (R)
30 (L)

Total

1799

1446 : 353

86 (R)
50 (L)

4 (R)
23 (L)

10 (R)
27 (L)

Bilateral positive (12 subjects)

Bilateral negative (32 subjects)
General bilateral (19 subjects)
-Subpatterns:
(1)Interhemispheric dissociation
(2)Double representation
(3)Unilateral representation
of subfunctions
(4)Distributed representation
of subfunctions
Duplicated automatic speech
Duplicated auditory
comprehension
Incomplete right dominance
No Wada decit in either
hemisphere
Adopting Benbadis, Dinner,
Chelune, Piedmonte, and
Luders (1995) classication
(based on speech arrest):
Bilateral autonomous
Bilateral dependent
Bilateral independent
Bilateral dependent

Observations

Left dominant (67.6%)

Right dominant (8.7%)
Incomplete left (16.2%)
Incomplete right (0%)
Strongly bilateral (7.5%)

11 cases were not classied. They had modality-specic

limited language decit plus automatic speech. No
subjects found with interhemispheric dissocition
of Broca/Wernicke type.

Bilateral autonomous: little or any decit following

either left or right carotid injection. Bilateral dependent:
language impairment with either carotid injection.
Benbadis et al. acknowledged in an ulterior work that
speech arrest is not a good sign for language
lateralization (1998)
69 patients (16%) with bilateral representation
of language:
Bilateral dependent (6.5%)
Bilateral independent (9%)

B. Bernal, A. Ardila / Journal of Neurolinguistics 28 (2014) 6380

Author

Conventions: Hand, handedness. (L) stands for not right-handed, including ambidextrous. (R), right-handed; Dom, dominant.

67

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group proposes four bilaterality sub-patterns: interhemispheric dissociation, double representation,

unilateral representation of subfunctions, and distributed representation of subfunctions between the
hemispheres; this last one is observed when the patient exhibited incomplete loss of language on both
Wada tests.
The study of Risse, Gates, and Fangman (1997), based on automatic speech and auditory comprehension only, divided the patterns of bilateral language representation in four sub-groups: (1) duplication of automatic speech in the right hemisphere, (2) duplication of auditory comprehension in the
right hemisphere, (3) right dominance for all functions with some impairment with left Wada and (4)
no decit in either hemisphere.
Loring et al. (1999) adopted the classication suggested by Benbadis et al. (1995) consisting of two
types of bilateral language representation: bilateral autonomous language representation, in whose
cases there is little or no language alteration in either side, and bilateral dependent language, characterized by language impairment with both left and right hemisphere injections. Mddel et al.s (2009)
classication is similar although utilizing different terminology: they propose two subgroups: bilateraldependent consisting of those subjects presenting speech arrest after injection of any of the carotids,
and speech-independent consisting of those subjects who did not have speech arrest after either injection. Unfortunately, speech arrest has been proven to be a non-valid method to determine language
lateralization with Wada test (Benbadis et al., 1998).
Noteworthy, all subjects of these reports are epilepsy patients, and the effects of the disease may
play an important role in language reorganization. At least it can be argued that the bilateral language
representation on some of these patients is a brain adaptation to a deviant trajectory of development;
or a result of some mechanism of brain plasticity with re-arrangement of the language circuitry. It
would explain that patients (usually intractable epilepsy patients) with bilateral language representation perform worse on neuropsychological test measures obtained both pre- and postoperatively
(Pataraia et al., 2005). Nevertheless, bilateral language representation in normal subjects has been
found not to be associated to any academic achievement problem or language decit (Knecht et al.,
2001).
4.2. Modern neuroimaging studies
Aside Wada studies, bilateral representation of language has been also found in other different
techniques, including PET, fMRI, tractography and magneto-encephalography. The main advantage of
these studies over Wada tests is that they may be performed on normal volunteers.
PET studies on normal volunteers have found that receptive language tasks elicit more bilateral
activation than expressive language tasks (Mller et al., 1997; Papathanassiou et al., 2000), a nding
conrmed by fMRI studies (e.g., Lidzba et al., 2011). Bilateral activation of expressive areas are much
less frequent but may be found in patients with brain gliomas examined with PET (Thiel et al., 1998).
Tumors and epilepsy are also related to more bilateral or right language representation in fMRI studies
(Adcock, Wise, Oxbury, Oxbury, & Matthews, 2003; Springer et al., 1999) and magnetoencephalography (Tanaka et al., 2013).
An extensive meta-analysis of functional neuroimaging studies including fMRI, PET and SPECT
studies have been published by Vigneau et al. (2011) aimed to describe the involvement of the right
hemisphere in distinct language tasks; the authors found 218 different areas of activation (referred to
as peaks), compared to 728 of the left hemisphere found in 105 experiments. Although the majority of
the peaks during the performance on linguistics tasks were unilateral in the left hemisphere (79%),
more bilateral peaks were observed when the right hemisphere was involved; that means, if the right
hemisphere was activated, usually it was also activated the left hemisphere. The authors conjecture the
right hemisphere works in an inter-hemispheric manner, that is that it somehow requires the left
hemisphere participation. When the peaks were analyzed with respect to each modality of language,
an interesting nding emerged: in phonological tasks, the motor representation for the mouth and
phonological working memory were exclusively found in the left hemisphere. The ndings suggest
that the right hemisphere does not host any phonological representation. In addition, the right frontal
lobe was found to participate in working memory, attentional functions and context processing in
sentence/word processing tasks.

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69

4.3. Insights from tractography

Intraoperative electrical stimulation of the left arcuate fasciculus has demonstrated its involvement in language transferring of phonology traits (Duffau, Gatignol, Mandonnet, Capelle, &
Taillandier, 2008; Mandonnet, Nouet, Gatignol, Capelle, & Duffau, 2007). In addition, the left
arcuate fasciculus has been reported in several articles to be associated to lateralization of language
(Bernal & Ardila, 2009; Nucifora, Verma, Melhem, Gur, & Gur, 2005; Powell et al., 2006; Rodrigo et al.,
2008). However, it has been found that the arcuate fasciculus is also seen left side dominant in
subjects with proven right side language dominance (Vernooij et al., 2007), a puzzling nding suggesting a bilateral representation of language processing not evident or understood by current
technology and state of the art comprehension of language processing. This nding would suggest
that some trans-callosal data-ow may take place assuming that posterior (receptive) to anterior
(expressive) transferring is only suitable through the dominant arcuate fasciculus. There is, however,
at least two alternatives to explain a non-arcuate intrahemispheric transferring: transferring by intermediate relay modules via U bers, and transferring by proxy tracts utilizing other interlobar
associative bundle (e.g., the inferior-occipital-frontal fasciculi). In addition to these signicant ndings related to the left arcuate fasciculus, it has been described that electrical stimulation of the left
ventral pathway, related to the inferior occipitofrontal fascicule, produces semantic paraphasias
(Duffau et al., 2008; Mandonet et al., 2007).

5. Toward a synthesis of bilateral representation of language

From the information collected to date and, in particular, with the insights provided by the modern
neurofunctional studies, a framework emerges of facts that may allow proposing a new explanatory
classication of the bilaterality of language representation.
These are the major facts:
- Expressive language is dissociated from the receptive language areas and is located in frontal areas
(mostly the left inferior frontal gyrus)
- Receptive language is dissociated from the expressive language areas and is mostly located in the
posterior third of the temporal lobe (mostly the left)
- There is a spectrum between left lateralization to right lateralization
- Bilateral representation of language may be found both in a limited number of patients and normal
subjects.
- Some epilepsy and tumor patients show language decit when either hemisphere is temporarily
disrupted.
- Some few epilepsy and tumor patients show no signicant language decit after temporary
disruption of either hemisphere.
- Some epilepsy and tumor patients show just minimal decit in only one hemisphere when
functional disruption is applied to both.
- Some degree of bilateral representation exists for the receptive function.
- Phonology has a segregated pathway (arcuate fasciculus) and it is mostly lateralized to the left
hemisphere
- Semantics is also segregated in the ventral pathway (possibly through the inferior occipital-frontal
fasciculus), and has a weaker lateralization.
In order to integrate these facts within the notion of bilateral representation of language two
conceptual elements can be proposed: (a) Modularity (understood here as a cortical regional specication for a given function), and (b) Data Flow Computing Models (understood for the sake of this
explanation as the transferring of a message, basically as a dichotomy between parallel vs. serial
transferring). Based on modularity, seven different patterns of bilateral language representation could
potentially be distinguished: (1) Bilateral expressive and receptive functions; (2) Bilateral expressive
with left receptive; (3) Bilateral expressive with right side receptive; (4) Bilateral receptive with left

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expressive; (5) Bilateral receptive with right side expressive, (6) Left expressive with right receptive,
and (7) Right expressive with left receptive. This classication will be expanded to more levels after
taking in consideration of the data-ow. These seven patterns could be expressed:

1.
2.
3.
4.
5.
6.
7.

ER: ER
ER: E
E: ER
ER: R
R: RE
E: R
R: E

Where E expressive and R receptive. The left side of the colon is left hemisphere and the right
side refers to the right hemisphere.
The concept of data ow computing stands for two different models of information processing: (a)
serial, and (b) parallel. In serial processing, steps occur one after the other, in such a manner that the
input for a given processor waits for the output of the prior processor in the chain of ow. An example
of this would be that semantic processing cannot occur until the phonological and lexical analysis has
taken place in another module (or processor, to keep the analogy with computers). In parallel processing, the output of any given operation is the input for two or more processing steps in the algorithm. An example of this would be the parallel processing of semantics of a word in conjunction with
the prosody of the intonation.
A number of publications have dealt with this dichotomized model borrowed from computational
sciences (Inui, Okamoto, Miki, Gunji & Kakigi, 2006; Mesulam, 1990; Townsend, 1990). Nonetheless,
some disagreement about which cognitive processes are parallel and which are serial remains;
neurophysiological facts and clinical ndings support the view that auditory processing is an example
of serial processing, and visual processing is a paradigmatic parallel processing, at least in its earliest
stages of processing. The notion of progressive language processing from phonological decoding to
syllables to words to phrases seems to empirically demonstrate the serial component of auditory
language processing. This has support of event-related studies showing that semantics appear in a
window of about 500 ms after word recognition (Hopf, Bader, Meng, & Bayer, 2003). However, parallel
processing has been also shown in language, for example, in reading (words and sentences) utilizing
event-related potentials (Dien, Frishkoff, Cerbone, & Tucker, 2003). In addition, there is parallel processing of prosody and familiar words that can be read as a whole and not in a letter-by-letter decoding
fashion.
Patients with pathology may not only redistribute (reorganize) the modules in a new fashion, but
also introduce changes in the data ow. For example, some modules may become bilateral represented
in a redundant manner while others may be dissociated between the hemispheres. Fig. 1 illustrate the
different potential subtypes: (a) Bilateral receptive language representation with canonical Broca; (b)
The bilateral representation of receptive areas is accompanied by right hemisphere transferring of
Brocas area; (c) Bilateral distributed receptive language; (d) Distributed receptive with non-canonical
Broca; (e) Duplicated expressive-receptive; (f) Bilateral language representation with interhemispheric
dissociation of expressive and receptive sub-functions; (g) True duplication of expressive functions
alone; (h) Same as prior category with receptive transferring to the right hemisphere; (i) Isolated
bilateral expressive representation with interhemispheric dissociation; (j) Similar to prior case but
with Wernickes area transferring; phonological aspects are more probable to remain in the left
hemisphere; (k) Interhemispheric dissociation of language. (l) Subtype of interhemispheric dissociation of language with non-canonical Broca..
5.1. Serial distribution
Serial processing distributed between the hemispheres is probably the most common of all bilateral
representation of language, given the nature of language processing. The patterns of serial distribution

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71

Fig. 1. Possible bilateral language representation based on two by two factors: receptive vs. expressive and phonology vs. semantics.
Drawings have a radiological orientation with left hemisphere represented on the right side. Ovals are divided in two halves
indicating domain dissociation between phonology and semantics (see text for explanation). Left column reects all possibilities for
bilateral representation of Wernickes area, whereas the right column shows bilateral representations of Brocas (otherwise not
included in the rst column) and two cases of expressive-receptive interhemispheric dissociation (k and l). Subtypes: (a) a frequent
normal subtype of bilateral language representation (11 of 39 cases in Risse et al. (1997) series, group II); (b) The bilateral representation of receptive areas is accompanied by right hemisphere transferring of Brocas area. This is an infrequent subtype; the right
lateralized Broca suggests brain reorganization; (c) Bilateral distributed receptive language; this pattern includes some subtypes,
accordingly with the subdomain transferred to the right hemisphere; (d) Distributed receptive with non-canonical Broca; A pattern
highly suggestive of language brain reorganization. Some subtypes may emerge accordingly with the receptive dissociation; (e) This
subtype represents a truly global bilateral representation of language; Wada test should fails to produce decit in either carotid, as it
was found in 2 cases of 39 in Risses et al. series; (f) Bilateral language representation with interhemispheric dissociation of
expressive and receptive sub-functions; four subtypes may be found here: one mirroring the example, and two swapping only one
domain; (g) True duplication of expressive functions alone; it is probably only theoretical as it has not yet been described; (h) Same
as prior category with receptive transferring to the right hemisphere (not described); (i) Isolated bilateral expressive representation
with interhemispheric dissociation; at least 2 subtypes are possible; comprehension is only affected in left Wada, but some aspects
of expression are affected in each side; Wernickes area remain in the left side; (j) Similar to prior case but with Wernickes area
transferring; phonological aspects are more probable to remain in the left hemisphere; (k) Interhemispheric dissociation of language. Rare condition, described in 4 of 490 epilepsy patients (Dongwook et al., 2008); (l) Subtype of interhemispheric dissociation
of language; expressive functions are most likely to transfer away from the seizure focus (Dongwook et al., 2008).

should be interpreted as an interdependence of the modules in which information ow has a recognizable starting point, and from that point on each output proceeds to only one module up-stream in
cognitive complexity or even reaches the nal motor pathway that generates speech. A simple
approach would represent that chain in the following way: phonological discrimination >> word
recognition >> semantic at word level >> syntactic analysis >> working memory >> sentence
processing >> semantic at sentence level >> grammatical analysis >> motor encoding >> motor
response. In such a sequence no matter where the impairment is located, a nal expressive (albeit

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disparate) decit is warranted. Assuming that a distributed inter-hemispheric network may have
modules in both sides of the brain, the ow of information would need to travel between the hemispheres across the corpus callosum or the anterior commissure, back and forth to link all the steps in
the chain of a serial ow. Having this type of distribution, a temporary disruption of either hemisphere
would produce language decits, although they should be different and perhaps partial. Some Wada
tests ndings previously reported by different authors may be explained in this way.
5.2. Parallel distribution
Patterns of parallel processing, on the other hand, should be interpreted in two different ways: (a)
redundancy processing, and (b) distributed processing. Parsing instructions in a redundant manner
have some analogy with algorithms of Resilient Parallel Computing, which is intended to protect
processes form failures by repeating the process just in case one branch of the algorithm fails and
crashes (Liu, Deters, & Zhang, 2010). Parsing instructions in a distributed processing assigns specic
processors to a given function that could be executed while other processor nishes a required process.
In our analogy, the parallel redundancy would trigger two homologous brain modules, in two
different hemispheres to perform the same process; whereas the parallel distributed processing
modules located in different hemispheres will simultaneously process different functions, like in the
example of prosody/semantics. True parallel redundant process is probably inexistent since it would be
a source of conict messing up the cognitive data ow; however, it is possible to imagine a redundancy
between the hemispheres for a given function that theoretically would explain ndings of bilateral
failure on Wada tests.
The combination of the subtypes provided by modularity, and those explained by data- ow may
theoretically explain several types of possible bilateral language representation, as illustrated in Fig. 1.
6. fMRI ndings suggesting distributed bilateral processing
Clinical and fMRI studies have demonstrated the different cortical specication segmenting the
expressive and receptive language functions. Further, fMRI has shown anatomical sub-specication for
isolated expressive and receptive functions. The Brocas area seems to contain two major subcomponents; (a) the pars opercularis, BA 44, and the anterior insula, involved in phonological processing and direct speech production, and (b) the pars triangularis, BA 45, more involved in semantic
and lexical processing (Amunts et al., 2004; Fiebach, Friederici, Mller, & von Cramon, 2002; Heim
et al., 2005; McDermott, Petersen, Watson, & Ojemann, 2003). This functional segregation has validation in the proven distinct structural connectivity that BA 44 and BA 45 exhibit in recent diffusion
tensor imaging studies (Klein et al., 2007; Lemaire et al., 2012). These areas seem to have many other
divergent functions beyond purely language processing (Bornkessel-Schlesewsky, Grewe, &
Schlesewsky, 2012); but of signicant relevance is the dorso-ventral differentiation of the pars opercularis seemingly related with a mirror neuron system (Molnar-Szakacs, Iacoboni, Koski, & Mazziotta,
2005).
Wernickes area sub-specialization has received less attention, in spite of encompassing a large
distribution of Brodmanns areas. Perhaps it is due to the poor anatomical landmarks delimiting the
receptive language cortex. However, it is now accepted that at least transferring of language from
posterior to anterior areas are carried by two different systems, (a) the dorsal system, involved in
phonological processing and (b) the ventral system involved in semantic processing (Duffau et al.,
2002; Glasser & Rilling, 2008; Leclercq et al., 2010; Mandonnet et al., 2007). This subdivision suggests some receptive phonological processing toward BA 40, and a more ventral and posterior semantic
analysis (McDermott et al., 2003).
The subdivision of phonology/semantic domains is only an example, may be the most relevant, but
not the only one. Several other subsystems are intervening in language that may have subspecialization. The dorsal pars opercularis has been found to be involved more specically in
sequencing linguistic and non-linguistic events (Ardila & Bernal, 2007; Makuuchi, Bahlmann,
Anwander & Friederici, 2009; Willems, Ozyrek, & Hagoort, 2009), whereas the ventral part has
been found to be involved in verbal working memory (Koelsch et al, 2009). Synonyms generation vs.

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73

Fig. 2. Axial T1 MRI anatomical images with functional map from an auditory description/comprehension task. Left side of the
image corresponds to the right hemisphere (Radiological orientation). The left image shows activation of the posterior right temporal lobe corresponding to Wernickes area. There are only minute activations in the left hemisphere. The image on the center
shows a large activation in the left inferior frontal gyrus corresponding to Brocas area. The right images show a hypointense image
located in the anterior temporal lobe (within the oval) consistent with a developmental tumor (patient 14 years old, right-handed
girl). (Images courtesy of Miami Childrens Hospital, Department of Radiology).

antonyms generation engages left lateralization regions. However, antonyms activation extends more
anteriorly (Jeon, Lee, Kim, & Cho, 2009); verbal working memory (Chein, Fissell, Jacobs, & Fiez, 2002),
semantic content vs. grammatical structure (Ni et al., 2000), and likely many other functions could be
distinguished.
Departing from the previous information it can be inferred that serial distribution between the
hemispheres can be quite complex, since a sub-specialized module may be located in one hemisphere
while the rest may remain in the other. Wada tests results seem to back up this assertion.
The following images were taken from patients with intractable epilepsy, who underwent fMRI for
language mapping. Some of these patterns are only evident when at least two language paradigms
with different linguistic loads are given. The cases will serve to illustrate key points in bilateral language representation.
Case A (Fig. 2): Bilateral representation of language: Broca/Wernicke dissociation type. It clearly
shows a bilateral representation of language with reorganization occurring only for receptive language
function, most likely in keeping with the malfunction produced by the developmental lesion found in
the left temporal region. A case like this will have a positive bilateral Wada test, but each side producing
a different clinical picture. It would be classied by Kurthen et al. (1994) as a General Bilateral pattern

Fig. 3. Bilateral Brocas and left Wernickes area Orientation and background image as in Fig. 2 fMRI task: auditory description/
comprehension task. Left side of the image corresponds to the right hemisphere (Radiological orientation). Left image shows
complete left lateralization for receptive language. Right image shows bilateral activation of inferior frontal gyrus slightly more
prominent on the right. Patient: 11-year-old right-handed girl. (Images courtesy of Miami Childrens Hospital, Department of
Radiology).

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Fig. 4. Bilateral global representation of language. Redundancy. Orientation and background are the same as aforementioned. fMRI
with auditory description/comprehension task. There is bilateral secondary auditory areas of activation in the posterior temporal
lobes, and bilateral activation of the inferior frontal gyrus. The patient is a 16-year-old right-handed girl with epilepsy. (Images
courtesy of Miami Childrens Hospital, Department of Radiology).

with interhemispheric dissociation. For Loring et al. (1990) and Mddel et al. (2009) this would be
classied as a bilateral dependent representation of language. Of note is the fact that this patient was a
right-hander.
Case B (Fig. 3) shows bilateral representation of expressive language functions, with well-dened
Wernickes left lateralization. The frontal areas are homologous, but only the right insula is involved.
This subject might have a bilateral positive (double representation) of Kurthen et al. (1994), where an
incomplete loss of language may be expected with a left carotid injection and no impairment with a
right carotid injection, provided there is redundancy of the Brocas area. For Loring et al. (1990) and
Mddel et al. (2009) this case will also be a bilateral dependent type. More difcult to classify
accordingly with Risse et al. (1997) subgroups of bilateral language representation, since they based it
too much on impairment of automatic speech. Perhaps the case could be classied as plain duplication
of automatic speech.
Case C (Fig. 4) is an example of global bilateral representation of language. There are some minor
asymmetries, but all canonical language areas are activated in both sides. A pattern like this may
explain all types of Kurthen et al. (1994), either bilateral-positive, bilateral-negative or bilateral global,
or double representation, unilateral representation of subfunctions or distributed representation of
subfunctions, all possible depending upon the distribution of the modules. If the bilateral condition
represents redundancy of both expressive and receptive modules, a bilateral global representation of
Kurthen et al.s is obtained. If, in contrast, a modular distribution (partial or complete) between the
hemispheres has taken place, either a bilateral-positive or bilateral negative is possible. Take for
example, that some phonological functions remain completely lateralized in the left hemisphere while
the rest of sub-modules are bilaterally represented (duplicated). In this case the right Wada will
produce a partial decit (if the reminder modules are distributed) or no decit (if the reminder
modules are duplicated), but the left Wada will produce deep language decit as the language processing has been affected at its root. Likewise, this pattern may explain subtypes 1 (duplication of
automatic speech), 2 (duplication of comprehension) and 4 (no decit in either Wada) of Risse et al.
(1997) but not 3 for only right sided dominant activations. Likewise, the pattern may explain Loring
et al.s types 1 or 2 depending if the organization is just redundancy of processing (as the pattern
suggests) or redistribution of sub-functions.
Case D (Fig. 5) shows a frequent nding in language mapping whenever different paradigms are
applied. In the case shown, the auditory description/comprehension task only yields left hemisphere
activation. In this task, the subject has to respond pressing a button when judging a sentence as true. As
control the subject presses the button when hearing a tone amidst pseudosentences created by playing
the sentences backwards. When the subject performs a task in which it is required to discriminate, if
pairs of words are synonyms or antonyms, contrasted to discrimination of similar or different tones, the
right inferior frontal gyrus is also involved. This bilateral representation is task-related and it is

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75

Fig. 5. Redistribution of sub-functions. Task-specic-dissociated bilateral representation of language. Left side of the image corresponds to the right hemisphere (Radiological orientation). Upper row: fMRI with auditory description/comprehension task. Lower
row: fMRI with a semantic decision task based on antonyms. The rst task only shows left side involvement for expressive and
receptive language. The antonyms task shows bilateral activation of Brocas area with same left sided Wernicke lateralization. Patient: 13-year-old right-handed boy. (Images courtesy of Miami Childrens Hospital, Department of Radiology).

reecting a different strategy of the brain working under specic semantic constrains. It seems that it is
much easier for the brain to judge true that What is on top of the house is the....roof than to decide if
distant far are synonyms, not antonyms. A case like this would be classied as distributed representation of sub-functions in Kurthen et al. (1994), classication; bilateral autonomous by Loring et al.
(1990) and not suitable for classication according to the proposal presented by Risse et al. (1997)

Fig. 6. Bilateral receptive lateralized expressive. Language activation map overlaid on an FLAIR MRI axial series. Left side of the
image corresponds to the right hemisphere (Radiological orientation). The subject was performing a semantic decision task based on
antonyms/synonyms discrimination. Notice the bilateral symmetrical activation of secondary auditory areas in homologous functional areas, and the lateralization of the expressive areas to the left hemisphere. Patient was a 21-year-old man with a developmental tumor in the right frontal lobe. (Images courtesy of Miami Childrens Hospital, Department of Radiology).

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Case E (Fig. 6) Bilateral Wernickes representation has at least two different variants: with left Broca
or with right Broca localization. The rst subtype is the most frequent of all bilateral representations,
and it is probably the only found in normal right- handed patients. Bilateral representation of receptive
functions is well recognized since early clinical studies described less comprehension than expressive
impairment in cases of global aphasia due to hemispheric stroke (Benson & Ardila, 1996; Taylor-Sarno &
Levita, 1981). Likewise, recovery is also faster and better for receptive language than for expressive
functions. In that sense, bilateral representation of expressive functions may be seen always as a
suggesting sign of language network reorganization. Still, the bilateral receptive language representation may have some variants as some sub-receptive functions could be re-distributed or duplicated
between the hemispheres. In fMRI studies, the homologous bilateral activation supposedly would
suggest redundancy of representation, while non-homologous bilateral temporo-parietal activation
would suggest a rather distributed bilateral representation. Notice at this point that Kurthen et al.s
subtypes of double representation, unilateral representation of sub-functions (distributed) and
distributed representation of sub-functions are good for expressive alone, receptive alone or both,
given an ample spectrum of different subtypes of functional bilateral representation for language.
7. Toward an integration
A simple classication, taking into account the different language categorical dissociations that has
been found and demonstrated in Wada and fMRI studies, could be proposed from a topographic
perspective (Table 2).
Any bilateral representation may be subdivided functionally in parallel (this is redundantly processed) or serial. In the rst case, we would see those cases in which the patient does not lose the
redundant function with the Wada test in neither of the carotids, while in the second (serial) he/she
will exhibit partial loss of speech (for example cases mentioned by Kurthen et al. (1994), Loring et al.
(1990) and Risse et al. (1997) cited before). In functional MRI, the serial processing between Brocas
areas may be seen as a task-related dissociation of expressive language (see Fig. 4).
The same rational may apply for cases with bilateral Wernickes representation - a more frequent
situation seen in clinical practice. Parallel processing between Wernickes areas would be seen as
subjects not referring any comprehension impairment after injection of the Amytal in either carotid,
while partial or limited comprehension may appear in both of them. Notice again that parallel processing in these examples is a sort of duplicated data ow, while the serial implies a distributed
modularity.

Table 2
Proposed classication of language lateralization according to a topographic perspective. All main types and subtypes are self
explanatory. The task specic dissociation subtype refers to distribution of data ow in which some language functions reside in
only one hemisphere. Functions dissociated may be explained by transferring of subfunctions (phonology or semantics) to the
right hemisphere. This dissociation is only evident when the patient is presented with two or more paradigms with different
linguistic loads. In this case, brain activations may appear non-congruent between tasks. We have preferred this name, to a more
descriptive but less practical name like "specic-linguistic-sub-domain dissociated language representation."
Isolated Bilateral Expressive Representation
Subtype I: with left Wernickes
Subtype II: with right Wernickes
Isolated Bilateral Receptive Representation
Subtype I: with left Brocas
Subtype II: with right Brocas
Bilateral Global Representation
Bilateral Dissociated Representation
Subtype I: Transhemispheric Broca/Wernicke dissociation
Subtype I.1: Brocas transferred
Subtype I.2: Wernickes transferred
Subtype II: Task-specic dissociation
Subtype I: Brocas dissociation
Subtype II: Wernickes dissociation
Subtype III: Combined dissociation

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77

Table 3
Proposed classication of language lateralization according to a functional perspective. Language modules may be duplicated in
the other hemisphere or distributed between the hemispheres. In the rst option process may occur in parallel assuming
complete capability of each side, or one side should remain quiescent. Notice that, in theroy, serial ow may still happen
assuming unbalanced efciency between the duplicated modules. However, in distributed modularity (types I and II) the serial
processing is obligued as data may ow crossing the hemispheres in the cognitive up-stream trajectory.
I. Duplicated Bilateral Representation of Language (each side sufces to hold the function: parallel processing)
Expressive
Receptive
Both
II. Distributed Bilateral Representation of Language (each hemisphere handles a particular subset of functions: serial
processing)
Expressive (phonology/semantics)
Receptive (Word-level vs. sentence level)
Both
III. Transhemispherical dissociated
Broca/Wernicke

A much more complex scenario is posed by bilaterality of both Brocas and Wernickes areas, since in
this case the serial vs. parallel processing may be distributed in two orthogonal dimensions: anterior to
posterior (receptive to expressive) and side to side between the homologous areas in which dissociations of the sort phonology/semantics may occur, among many others. The multidimensionality of
these intertwined factors may prompt for a quite complex and large classication. A functional classication could consequently also be proposed, as presented in Table 3.
8. Conclusion
Bilateral language representation has been a very complex and intricate aspect of brain organization
of cognition. It is frequent understanding that language lateralization is a matter of all or nothing.
However, language dominance is mostly a matter of hemispheric advantage for a specic multimodular cognitive function: language. As such, language in a strict sense is up to a certain point a
bilateral brain function. Aside expressive/receptive and phonological/semantic dichotomies there are
other many sub-functions for which we are looking for their anatomical and functional correlates with
new neuroimaging techniques such as diffusion tensor imaging tractography and fMRI.
The understanding of the language network in terms of submodules and connectivity will provide
ground to better understanding brain reorganization after structural and functional brain lesions.
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