bilateraliad lenguaje

7212019 BILATERALIAD LENGUAJE

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Review

Bilateral representation of language A criticalreview and analysis of some unusual cases

Byron Bernal a Alfredo Ardila b

a Department of RadiologyResearch Institute Miami Childrenrsquo s Hospital Miami FL USAb Department of Communication Sciences and Disorders Florida International University Miami FL USA

a r t i c l e i n f o

Article history

Received 19 August 2013

Received in revised form 26 September 2013

Accepted 14 October 2013

Keywords

Brain asymmetryLanguage

Laterality

Brocarsquos area

Wernickersquos area

fMRI

a b s t r a c t

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 examinedDeparting from the modularity concept and data 1047298ow computing

models two classi1047297cations ndash topographic and functional ndash of po-

tential language lateralization patterns are proposed it is pointed

out that language can be bilaterally represented in different pat-

terns accordingly with the distribution of the main domains

(expressive vs receptive) and their subfunctions and with respect

to different modalities of data 1047298ow 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 speci1047297c cognitive function

2013 Elsevier Ltd All rights reserved

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 1047297ndings 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 thorn1 305 348 2750 fax thorn1 305 348 2740E-mail address ardilaa1047297uedu (A Ardila)

Contents lists available at ScienceDirect

Journal of Neurolinguistics

j o u r n a l h o m e p a g e w w w e l s e v i e r c o m lo c a t e j n e u r o l i n g

0911-6044$ ndash see front matter 2013 Elsevier Ltd All rights reserved

httpdxdoiorg101016jjneuroling201310002

Journal of Neurolinguistics 28 (2014) 63ndash80



in extensive studies using the intracarotid amytal test (so-called ldquoWada testrdquo) (eg Kurthen et al 1994

Loring et al 1999 Moumlddel Lineweaver Schuele Reinholz amp Loddenkemper 2009 Woermann et al

2003) Modern modalities of non-invasive neuroimaging and electro-physiology procedures have

validated those initial 1047297ndings as well fMRI (eg Binder 2011 Holland et al 2007 Price 2010) near

infra-red spectroscopy (Bembich Demarini Clarici Massaccesi amp Grasso 2011 Bisconti Di Sante

Ferrari amp Quaresima 2012 Kennan Kim Maki Koizumi amp Constable 2002) magneto-encephalography (Kadis et al 2011) and diffusion tensor imagingtractography (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 laterali-

zation in 326 healthy individuals with functional transcranial Doppler sonography (a non invasive

technique measures the velocity of blood 1047298ow through the brainrsquos blood vessels using pulsed Doppler

transducer - ultrasonic pulse probe that detects the re1047298ected 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 frac14 100) to 15 in ambidextrous individuals and 27 in strong left-handers (handedness frac14100)However this technique may be in1047298uenced 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 left-

handers and 75 right-handers) left-handers exhibited right language dominance in 773 of cases

while bilateral representation was observed in 147 and left dominance in 8 of the subjects 933 of

right-handers showed left side dominance and 67 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 sub-

divided 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 82 exhibited disruptionwith stimulation in either hemisphere 42 of subjects had disruption with stimulus in the right

hemisphere In strongly left-handed subjects 737 of subjects had left hemisphere dominance 158

had bilateral representation and 105 had right side dominance In ambidextrous subjects bilateral

representation was observed in 57 of cases The authors concluded that speech lateralized to the left-

side cerebral dominance in strongly right- and left-handed subjects but bilateral cerebral represen-

tation 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 Socieacuteteacute de Anthropologie de Paris Paul Broca explicitly stated Nous

parlons avec lrsquo heacutemisphegravere gauche

dWe speak with the left hemisphere

rdquo (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 right-

handers This hypothesis has been referred as ldquoconjunction hypothesisrdquo (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 ldquocrossed

aphasiardquo 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 in-

dividual with left hemiplegia that is an aphasia resulting from a cerebral lesion lsquoipsilateralrsquo to the

dominant hand Noteworthy just a few crossed aphasics were right-handers but most were left-

handers He considered that crossed aphasia is relatively frequent as a transient disorder but it isextremely unusual as a permanent syndrome in this latter case it is only found in left-handers Heacutecaen

amp Albert (1978) suggested that the term ldquocrossed aphasiardquo should be used only to refer to aphasia

following right hemisphere pathology in a right-handed person and this is the way the term ldquocrossed

aphasiardquo is currently used (Ishizaki et al 2012 Marieumln Paghera De Deyn amp Vignolo 2004)

B Bernal A Ardila Journal of Neurolinguistics 28 (2014) 63ndash8064



The incidence of crossed aphasia is very low (Coppens Hungerford Yamaguchi amp Yamadori 2002)

Heacutecaen Mazurs Ramier Goldblum and Merianne (1971) estimated an incidence of 038 while

Benson and Geschwind (1973) proposed a 1047297gure 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 amp Olsen 1995) It is generally accepted that crossed aphasia represents no

more than 3 of all cases of aphasia (Ha Pyun Hwang amp Sim 2012) Some authors however havesuggested that the incidence of crossed aphasia could be even lower (Ardila 2006 Castro-Caldas amp

Confraria 1984)

Right-hemisphere lesions however have been found more frequently associated with aphasia in

left-handed individuals (Basso amp Rusconi 1998) Some authors have reported that up to 50 of left-

handers 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 amp Ardila1996) The aphasia pro1047297le 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 right-

handed aphasics (Heacutecaen amp 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 comparingaphasia recovery in right- and left-handed individuals only small and non-signi1047297cant differences are

found (Basso amp Rusconi1998) 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 Brozovaacute Tintera amp Krsek 2007 Lieacutegeois 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

(eg Holodny Schulder Ybasco amp Liu 2002 Kosla et al 2012 Tyler Wright Randall Marslen-Wilson

amp Stamatakis 2010 Weiller et al 1995) All these studies show right hemisphere overtake of homo-

topic areas after injury of language eloquent areas in the left hemisphereHickok 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 percep-

tion involve auditory 1047297elds located bilaterally ndash although asymmetrically ndash in the superior temporal

gyrus Normal language acquisition sets up a degree of bilateral representation in the superior tem-

poral 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

1047297ssure 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 pre-

dominantly processed by the left hemisphere (Dehaene-Lambertz Dehaene amp Hertz-Pannier 2002)

However it has also been found that the degree of lateralization increases in the 1047297rst years of life

Holland et al (2001) studied a group of healthy children between 7 and 18 years 1047297nding increasing left

lateralization across these ages In a detailed study Sza1047298arski Holland Schmithorst and Byars (2006)

found a statistical signi1047297cant positive correlation between age in children (range 5ndash17 years) and

lateralization indexes for Brocarsquos area Similar 1047297ndings of progressive lateralization of language to the

left hemisphere mostly related to the expressive language system are reported by Lidzba Schwilling

Grodd Kraumlgeloh-Mann and Wilke (2011) Language progressive lateralization in childhood may berelated to the maturation of the corpus callosum (Allen Richey Chai amp 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

B Bernal A Ardila Journal of Neurolinguistics 28 (2014) 63ndash80 65



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 ldquofunctional

crowdingrdquo hypothesis was found They however observed that children with left-lateralized language

production had higher vocabulary and nonword reading age-adjusted standard scores than otherchildren regardless of the laterality of visuospatial memory They concluded that there is a link be-

tween 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 laterali-

zation decreases with age and the required cognitive processes become more symmetrical over time

(Wing1047297eld amp 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 pro-posed that age-related hemispheric asymmetry reduction may have a compensatory function or may

re1047298ect 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

41 Wada test

The history of language lateralization has been partially dominated by the Intracarotid Amobarbital

Test described in Japan by JA 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 hemi-

plegia without loss of consciousness At this point the subject is examined to detect language and

memory de1047297cits 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 1047297ve major publications in bilateral Wada tests It totalizes

1799 bilateral Wada studies in 1446 right-handers and 353 subjects either left-handed or ambidextrusAlthough there is inhomogeneity in the procedures classi1047297cation 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 classi1047297cation for bilateral language

dominance that may describe the sometimes perplexing 1047297ndings of the Wada test Kurthen et al

(1994) described 1047297ve categories based on lateralization indexes (1) left dominant (2) right domi-

nant (3) incomplete left (4) incomplete right and (5) strongly bilateral In this classi1047297cation incom-

plete 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 patientrsquos 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 lackof 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 Kurthenrsquos




Table 1

Bilateral language representation by Wada studies (selective review)

Author No

Sjcts

Hand (R) (L) Left-H

Dom

Right H

Dom

Bilat

Dom

Suggested classi1047297cation of

bilateral representation

Observati

Rasmussen and

Milner (1977)

262 140 122 96 (R) 4 (R) 0 None

70 (L) 15 (L) 15 (L)

Kurthen et al (1994) 173 142 31 77 (R) 4 (R) 19 (R) 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

Left domi

Right dom

Incomple

Incomple

Strongly b

23 (L) 32 (L) 45 (L)

Risse Gates andFangman (1997) 368 304 64 87 (R) 4 (R) 9 (R) Duplicated automatic speechDuplicated auditory

comprehension

Incomplete right dominance

No Wada de1047297cit in either

hemisphere

11 cases wlimited la

subjects f

of BrocaW

62 (L) 18 (L) 20 (L)

Loring et al (1999) 551 469 82 86 (R) 5 (R) 9 (R) Adopting Benbadis Dinner

Chelune Piedmonte and

Luders (1995) classi1047297cation

(based on speech arrest)

Bilateral autonomous

Bilateral dependent

Bilateral a

either left

language

Benbadis

speech ar

lateralizat

48 (L) 29 (L) 23 (L)

Moumlddel et al (2009) 445 391 54 82 (R) 4 (R) 14 (R) Bilateral independent

Bilateral dependent

69 patien

of languag

Bilateral dBilateral i

48 (L) 22 (L) 30 (L)

Total 1799 1446 353 86 (R) 4 (R) 10 (R)

50 (L) 23 (L) 27 (L)

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



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 compre-

hension only divided the patterns of bilateral language representation in four sub-groups (1) dupli-cation 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 de1047297cit in either hemisphere

Loring et al (1999) adopted the classi1047297cation 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 charac-

terized by language impairment with both left and right hemisphere injections Moumlddel et alrsquos (2009)

classi1047297cation is similar although utilizing different terminology they propose two subgroups bilateral-

dependent 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 in-

jection Unfortunately speech arrest has been proven to be a non-valid method to determine languagelateralization 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 represen-

tation 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 de1047297cit (Knecht et al

2001)

42 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 (Muumlller et al 1997 Papathanassiou et al 2000) a 1047297nding

con1047297rmed by fMRI studies (eg 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 amp Matthews 2003 Springer et al 1999) and magneto-encephalography (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 1047297

nding emerged in phonological tasks the motor representation for the mouth andphonological working memory were exclusively found in the left hemisphere The 1047297ndings 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

sentenceword processing tasks




43 Insights from tractography

Intraoperative electrical stimulation of the left arcuate fasciculus has demonstrated its involve-

ment in language transferring of phonology traits (Duffau Gatignol Mandonnet Capelle amp

Taillandier 2008 Mandonnet Nouet Gatignol Capelle amp Duffau 2007) In addition the left

arcuate fasciculus has been reported in several articles to be associated to lateralization of language(Bernal amp Ardila 2009 Nucifora Verma Melhem Gur amp 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 1047297nding sug-

gesting a bilateral representation of language processing not evident or understood by current

technology and state of the art comprehension of language processing This 1047297nding would suggest

that some trans-callosal data-1047298ow 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 in-

termediate relay modules via U 1047297bers and transferring by proxy tracts utilizing other interlobar

associative bundle (eg the inferior-occipital-frontal fasciculi) In addition to these signi1047297cant 1047297nd-

ings related to the left arcuate fasciculus it has been described that electrical stimulation of the leftventral 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

classi1047297cation 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 de1047297cit when either hemisphere is temporarily

disrupted

- Some few epilepsy and tumor patients show no signi1047297cant language de1047297cit after temporary

disruption of either hemisphere- Some epilepsy and tumor patients show just minimal de1047297cit 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 ldquobilateral representation of languagerdquo two

conceptual elements can be proposed (a) Modularity (understood here as a cortical regional speci1047297-

cation for a given function) and (b) Data Flow Computing Models (understood for the sake of thisexplanation 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




expressive (5) Bilateral receptive with right side expressive (6) Left expressive with right receptive

and (7) Right expressive with left receptive This classi1047297cation will be expanded to more levels after

taking in consideration of the data-1047298ow These seven patterns could be expressed

Where E frac14 expressive and R frac14 receptive The left side of the colon is left hemisphere and the right

side refers to the right hemisphere

The concept of ldquodata 1047298ow computingrdquo 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 theinput for a given processor ldquowaitsrdquo for the output of the prior processor in the chain of 1047298ow 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 pro-

cessing the output of any given operation is the input for two or more processing steps in the algo-

rithm 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 amp Kakigi 2006 Mesulam 1990 Townsend 1990) Nonetheless

some disagreement about which cognitive processes are parallel and which are serial remains

neurophysiological facts and clinical 1047297ndings support the view that auditory processing is an example

of serial processing and visual processing is a paradigmatic parallel processing at least in its earlieststages 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 amp 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 amp Tucker 2003) In addition there is parallel pro-

cessing 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 1047298ow For example some modules may become bilateral represented

in a redundant manner while others may be dissociated between the hemispheres Fig 1 illustrate thedifferent potential subtypes (a) Bilateral receptive language representation with canonical Broca (b)

The bilateral representation of receptive areas is accompanied by right hemisphere transferring of

Brocarsquos 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 Wernickersquos area transferring phonological aspects are more probable to remain in the left

hemisphere (k) Interhemispheric dissociation of language (l) Subtype of interhemispheric dissocia-

tion of language with non-canonical Broca

51 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

1 ER ER

2 ER E

3 E ER

4 ER R

5 R RE

6 E R

7 R E




should be interpreted as an interdependence of the modules in which information 1047298ow has a recog-

nizable starting point and from that point on each output proceeds to only one module up-stream in

cognitive complexity or even reaches the 1047297

nal motor pathway that generates speech A simpleapproach would represent that chain in the following way phonological discrimination gtgt word

recognition gtgt semantic at word level gtgt syntactic analysis gtgt working memory gtgt sentence

processing gtgt semantic at sentence level gtgt grammatical analysis gtgt motor encoding gtgt motor

response In such a sequence no matter where the impairment is located a 1047297nal expressive (albeit

Fig1 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 re 1047298ects all possibilities for

bilateral representation of Wernickersquos area whereas the right column shows bilateral representations of Broca rsquos (otherwise not

included in the 1047297rst 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 repre-

sentation of receptive areas is accompanied by right hemisphere transferring of Broca rsquos 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 de1047297cit in either carotid as it

was found in 2 cases of 39 in Rissersquos 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 Wernickersquos area remain in the left side (j) Similar to prior case but with Wernickersquos area

transferring phonological aspects are more probable to remain in the left hemisphere (k) Interhemispheric dissociation of lan-

guage 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)




disparate) de1047297cit is warranted Assuming that a distributed inter-hemispheric network may have

modules in both sides of the brain the 1047298ow of information would need to travel between the hemi-

spheres across the corpus callosum or the anterior commissure back and forth to link all the steps in

the chain of a serial 1047298ow Having this type of distribution a temporary disruption of either hemisphere

would produce language de1047297cits although they should be different and perhaps partial Some Wada

tests 1047297ndings previously reported by different authors may be explained in this way

52 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 amp Zhang 2010) Parsing instructions in a distributed processing assigns speci1047297c

processors to a given function that could be executed while other processor 1047297nishes 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 processingmodules located in different hemispheres will simultaneously process different functions ndashlike in the

example of prosodysemantics True parallel redundant process is probably inexistent since it would be

a source of con1047298ict messing up the cognitive data1047298ow however it is possible to imagine a redundancy

between the hemispheres for a given function that theoretically would explain 1047297ndings of bilateral

failure on Wada tests

The combination of the subtypes provided by modularity and those explained by data- 1047298ow may

theoretically explain several types of possible bilateral language representation as illustrated in Fig 1

6 fMRI 1047297ndings suggesting distributed bilateral processing

Clinical and fMRI studies have demonstrated the different cortical speci1047297cation segmenting theexpressive and receptive language functions Further fMRI has shown anatomical sub-speci1047297cation for

isolated expressive and receptive functions The Brocarsquos area seems to contain two major sub-

components (a) the pars opercularis BA 44 and the anterior insula involved in phonological pro-

cessing and direct speech production and (b) the pars triangularis BA 45 more involved in semantic

and lexical processing (Amunts et al 2004 Fiebach Friederici Muumlller amp von Cramon 2002 Heim

et al 2005 McDermott Petersen Watson amp Ojemann 2003) This functional segregation has vali-

dation 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 amp

Schlesewsky 2012) but of signi1047297cant relevance is the dorso-ventral differentiation of the pars oper-

cularis seemingly related with a mirror neuron system (Molnar-Szakacs Iacoboni Koski amp Mazziotta2005)

Wernickersquos area sub-specialization has received less attention in spite of encompassing a large

distribution of Brodmannrsquos 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 amp Rilling 2008 Leclercq et al 2010 Mandonnet et al 2007) This subdivision sug-

gests some receptive phonological processing toward BA 40 and a more ventral and posterior semantic

analysis (McDermott et al 2003)

The subdivision of phonologysemantic 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 sub-specialization The dorsal pars opercularis has been found to be involved more speci1047297cally in

sequencing linguistic and non-linguistic events (Ardila amp Bernal 2007 Makuuchi Bahlmann

Anwander amp Friederici 2009 Willems Ozyuumlrek amp Hagoort 2009) whereas the ventral part has

been found to be involved in verbal working memory (Koelsch et al 2009) Synonyms generation vs




antonyms generation engages left lateralization regions However antonyms activation extends more

anteriorly ( Jeon Lee Kim amp Cho 2009) verbal working memory (Chein Fissell Jacobs amp 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 forlanguage 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 lan-

guage representation

Case A (Fig 2) Bilateral representation of language BrocaWernicke 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 classi1047297ed by Kurthen et al (1994) as a General Bilateral pattern

Fig 2 Axial T1 MRI anatomical images with functional map from an auditory descriptioncomprehension task Left side of the

image corresponds to the right hemisphere (Radiological orientation) The left image shows activation of the posterior right tem-

poral lobe corresponding to Wernickersquos 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 Brocarsquos area The right images show a hypointense imagelocated in the anterior temporal lobe (within the oval) consistent with a developmental tumor (patient 14 years old right-handed

girl) (Images courtesy of Miami Childrenrsquos Hospital Department of Radiology)

Fig 3 Bilateral Brocarsquos and left Wernickersquos 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 Childrenrsquos Hospital Department of

Radiology)




with interhemispheric dissociation For Loring et al (1990) and Moumlddel et al (2009) this would be

classi1047297ed 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-de1047297ned

Wernickersquos 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 Broca rsquos area For Loring et al (1990) and

Moumlddel et al (2009) this case will also be a bilateral dependent type More dif 1047297cult to classify

accordingly with Risse et al (1997) subgroups of bilateral language representation since they based ittoo much on impairment of automatic speech Perhaps the case could be classi1047297ed as plain ldquoduplication

of automatic speechrdquo

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 alrsquos 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 whilethe rest of sub-modules are bilaterally represented (duplicated) In this case the right Wada will

produce a partial de1047297cit (if the reminder modules are distributed) or no de1047297cit (if the reminder

modules are duplicated) but the left Wada will produce deep language de1047297cit as the language pro-

cessing has been affected at its root Likewise this pattern may explain subtypes 1 (duplication of

automatic speech) 2 (duplication of comprehension) and 4 (no de1047297cit in either Wada) of Risse et al

(1997) but not 3 for only right sided dominant activations Likewise the pattern may explain Loring

et alrsquos 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 1047297nding in language mapping whenever different paradigms are

applied In the case shown the auditory descriptioncomprehension task only yields left hemisphere

activation In this task the subject has to respond pressing a button when judging a sentence as true Ascontrol 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

Fig 4 Bilateral global representation of language Redundancy Orientation and background are the same as aforementioned fMRI

with auditory descriptioncomprehension 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 Childrenrsquos Hospital Department of Radiology)




re1047298ecting a different strategy of the brain working under speci1047297c semantic constrains It seems that it is

much easier for the brain to judge true that ldquoWhat is on top of the house is theroof rdquo than to decide if

ldquodistant ndash farrdquo are synonyms not antonyms A case like this would be classi1047297ed as ldquodistributed repre-

sentation of sub-functionsrdquo in Kurthen et al (1994) classi 1047297cation bilateral autonomous by Loring et al

(1990) and not suitable for classi 1047297cation according to the proposal presented by Risse et al (1997)

Fig 5 Redistribution of sub-functions Task-speci1047297c-dissociated bilateral representation of language Left side of the image corre-

sponds to the right hemisphere (Radiological orientation) Upper row fMRI with auditory descriptioncomprehension task Lower

row fMRI with a semantic decision task based on antonyms The 1047297rst task only shows left side involvement for expressive andreceptive language The antonyms task shows bilateral activation of Broca rsquos area with same left sided Wernicke lateralization Pa-

tient 13-year-old right-handed boy (Images courtesy of Miami Children rsquos Hospital Department of Radiology)

Fig 6 Bilateral receptive ndash 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

antonymssynonyms discrimination Notice the bilateral symmetrical activation of secondary auditory areas in homologous func-

tional areas and the lateralization of the expressive areas to the left hemisphere Patient was a 21-year-old man with a develop-

mental tumor in the right frontal lobe (Images courtesy of Miami Childrenrsquos Hospital Department of Radiology)




Case E (Fig 6) Bilateral Wernickersquos representation has at least two different variants with left Broca

or with right Broca localization The 1047297rst 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 amp Ardila1996 Taylor-Sarno amp

Levita 1981) Likewise recovery is also faster and better for receptive language than for expressivefunctions 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 represen-

tation 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 rsquos

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 classi1047297cation 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 pro-

cessed) or serial In the 1047297rst 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) heshe

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 Broca rsquos

areas may be seen as a task-related dissociation of expressive language (see Fig 4)

The same rational may apply for cases with bilateral Wernickersquos representation - a more frequentsituation seen in clinical practice Parallel processing between Wernickersquos 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 pro-

cessing in these examples is a sort of duplicated data 1047298ow while the serial implies a distributed

modularity

Table 2

Proposed classi1047297cation of language lateralization according to a topographic perspective All main types and subtypes are self

explanatory The task speci1047297c dissociation subtype refers to distribution of data1047298ow 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 differentlinguistic 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 speci1047297c-linguistic-sub-domain dissociated language representation

Isolated Bilateral Expressive Representation

Subtype I with left Wernickersquos

Subtype II with right Wernickersquos

Isolated Bilateral Receptive Representation

Subtype I with left Brocarsquos

Subtype II with right Brocarsquos

Bilateral Global Representation

Bilateral Dissociated Representation

Subtype I Transhemispheric BrocaWernicke dissociation

Subtype I1 Brocarsquos transferred

Subtype I2 Wernickersquos transferredSubtype II Task-speci1047297c dissociation

Subtype I Brocarsquos dissociation

Subtype II Wernickersquos dissociation

Subtype III Combined dissociation




A much more complex scenario is posed by bilaterality of both Brocarsquos and Wernickersquos 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 dissoci-

ations of the sort phonologysemantics may occur among many others The multidimensionality of

these intertwined factors may prompt for a quite complex and large classi1047297cation A functional clas-

si1047297cation 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 nothingHowever language dominance is mostly a matter of hemispheric advantage for a speci1047297c multi-

modular cognitive function language As such language in a strict sense is up to a certain point a

bilateral brain function Aside expressivereceptive and phonologicalsemantic 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

References

Adcock J E Wise R G Oxbury J M Oxbury S M amp Matthews P M (2003) Quantitative fMRI assessment of the differencesin lateralization of language related brain activation in patients with temporal lobe epilepsy Neuroimage 8(2) 423ndash438

Allen L S Richey M F Chai Y M amp Gorski R A (1991) Sex differences in the corpus callosum of the living human being Journal of Neuroscience 11 933ndash942

Amunts K Weiss P H Mohlberg H Pieperhoff P Eickhoff S Gurd J M et al (2004) Analysis of neural mechanismsunderlying verbal 1047298uency in cytoarchitectonically de1047297ned stereotaxic spacedthe roles of Brodmann areas 44 and 45Neuroimage 22(1) 42ndash56

Anderson D P Harvey A S Saling M M Anderson V Kean M Jacobs R et al (2002) Differential functional magneticresonance imaging language activation in twins discordant for a left frontal tumor Journal of Child Neuralogy 17 (10)766ndash769

Ardila A (2006) Las afasias Accessed March 29 2013 httpneuropsicologblogspotcom200904libros-de-las afasias-alfredo-ardilahtml

Ardila A amp Bernal B (2007) What can be localized in the brain towards a factor theory on brain organization of cognitionInternational Journal of Neuroscience 117 935ndash969

Basic S Hajnsek S Poljakovic Z Basic M Culic V amp Zadro I (2004) Determination of cortical language dominance using

functional transcranial Doppler sonography in left-handers Clinical Neurophysiology 115(1) 154ndash

160Basso A amp Rusconi M L (1998) Aphasia in left-handers In P Coppens Y Lebrun amp A Basso (Eds) Aphasia in atypical

populations (pp 1ndash34) Mahwah NJ Lawrence Erlbaum AssociatesBembich S Demarini S Clarici A Massaccesi S amp Grasso D L (2011) Non invasive assessment of hemispheric language

dominance by optical topography during a brief passive listening test a pilot study Medical Science Monitor 17 (12) CR692ndash

CR697

Table 3

Proposed classi1047297cation of language lateralization according to a functional perspective Language modules may be duplicated in

the other hemisphere or distributed between the hemispheres In the 1047297rst option process may occur in parallel assuming

complete capability of each side or one side should remain quiescent Notice that in theroy serial 1047298ow may still happen

assuming unbalanced ef 1047297ciency between the duplicated modules However in distributed modularity (types I and II) the serial

processing is obligued as data may 1047298ow crossing the hemispheres in the cognitive up-stream trajectory

I Duplicated Bilateral Representation of Language (each side suf 1047297ces 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 (phonologysemantics)

Receptive (Word-level vs sentence level)

Both

III Transhemispherical dissociated

BrocaWernicke




Benbadis S R Binder J R Swanson S J Fischer M Hammeke T A Morris G L et al (1998) Is speech arrest during Wadatesting a valid method for determining hemispheric representation of language Brain and Language 65(3) 441ndash446

Benbadis S R Dinner S D Chelune G J Piedmonte M amp Luders H O (1995) Autonomous versus dependent a classi1047297cationof bilateral language representation by intracarotid amobarbital procedure Journal of Epilepsy 8 255ndash263

Benson D F amp Ardila A (1996) Aphasia A clinical perspective New York Oxford University PressBenson D amp Geschwind N (1973) Aphasia and related disturbances In A Baker (Ed) Clinical Neurology (pp 1ndash26) New York

Harper and RowBernal B amp Ardila A (2009) The role of the arcuate fasciculus in conduction aphasia Brain 132(Pt 9) 2309ndash2316Binder J R (2011) Functional MRI is a valid noninvasive alternative to Wada testing Epilepsy Behavior 20(2) 214ndash222Bisconti S Di Sante G Ferrari M amp Quaresima V (2012) Functional near-infrared spectroscopy reveals heterogeneous

patterns of language lateralization over frontopolar cortex Neuroscience Research 73(4) 328ndash332Bornkessel-Schlesewsky I Grewe T amp Schlesewsky M (2012) Prominence vs aboutness in sequencing a functional

distinction within the left inferior frontal gyrus Brain and Language 120(2) 96ndash107Bramwell B (1899) On ldquocrossedrdquo aphasia Lancet 3 1473ndash1479Broca P (1861) Remarques sur le siegravege de la faculteacute du langage articuleacute suivies d rsquoune observation drsquoapheacutemie Bulletin de la

Socieacuteteacute drsquo Anthropologie 2 330ndash357Broca P (1865) Du siegravege de la faculteacute du langage articuleacute Bulletin de la Socieacuteteacute drsquo Anthropologie 6 337ndash393Cabeza R (2002) Hemispheric asymmetry reduction in older adults the HAROLD model Psychology and Aging 17 (1) 85ndash100Castro-Caldas A amp Confraria A (1984) Age and type of crossed aphasia in dextral due to stroke Brain and Language 23126ndash133Chein J M Fissell K Jacobs S amp Fiez J A (2002) Functional heterogeneity within Broca rsquos area during verbal working

memory Physiology and Behavior 77 (4ndash5) 635ndash639

Coppens P Hungerford S Yamaguchi S amp Yamadori A (2002) Crossed aphasia an analysis of the symptoms their frequencyand a comparison with left hemisphere aphasia symptomatology Brain and Language 83(3) 425ndash463

Dehaene-Lambertz N Dehaene S amp Hertz-Pannier L (2002) Functional neuroimaging of speech perception in infants Sci-ence 298 2013ndash2015

Dejerine J (1914) Semiologie des affections du systeme nerveux Paris MassonDien J Frishkoff G A Cerbone A amp Tucker D M (2003) Parametric analysis of event-related potentials in semantic

comprehension evidence for parallel brain mechanisms Cognitive Brain Research 15(2) 137ndash153Dongwook L Lee S J Swanson D S Sabsevitz T A Hammeke F Winstanley S et al (2008) Fmri and Wada studies in

patients with interhemispheric dissociation of language functions Epilepsy and Behavior 13 350ndash356Duffau H Capelle L Sichez N Denvil D Lopes M Sichez J P et al (2002) Intraoperative mapping of the subcortical

language pathways using direct stimulations An anatomo-functional study Brain 125(Pt 1) 199ndash214Duffau H Gatignol S T Mandonnet E Capelle L amp Taillandier L (2008) Intraoperative subcortical stimulation mapping of

language pathways in a consecutive series of 115 patients with Grade II glioma in the left dominant hemisphere Journal of Neurosurgery 109(3) 461ndash471

Fiebach C J Friederici A D Muumlller K amp von Cramon D Y (2002) fMRI evidence for dual routes to the mental lexicon invisual word recognition Journal of Cognitive Neurosciences 14(1) 11ndash23

Glasser M F amp Rilling J K (2008) DTI tractography of the human brainrsquos language pathways Cerebral Cortex 18(11) 2471ndash

2482Groen M A Whitehouse A J Badcock N A amp Bishop D V (2012) Does cerebral lateralization develop A study using

functional transcranial Doppler ultrasound assessing lateralization for language production and visuospatial memory Brainand Behavior 2(3) 256ndash269

Hadac J Brozovaacute K Tintera J amp Krsek P (2007) Language lateralization in children with pre- and postnatal epileptogeniclesions of the left hemisphere an fMRI study Epileptic Disorders 9(Suppl 1) S19ndashS27

Ha J W Pyun S B Hwang Y M amp Sim H (2012) Lateralization of cognitive functions in aphasia after right brain damageYonsei Medical Journal 53(3) 486ndash494

Harris L J (1991) Cerebral control for speech in right-handers and left-handers an analysis of the views of Paul Broca hiscontemporaries and his successors Brain and Language 40 1ndash50

Harris L J (1999) Early theory and research on hemispheric specialization Schizophrenia Bulletin 25(1) 11ndash39Heacutecaen H amp Albert M L (1978) Human neuropsychology New York Wiley

Heacutecaen H Mazurs G Ramier A Goldblum M amp Merianne L (1971) Aphasie croisee chez un sujet droiter bilingue RevueNeurologique 1 319ndash323Heacutecaen H amp Sauguet J (1971) Cerebral dominance in left-handed subjects Cortex 7 19ndash47Heim S Alter K Ischebeck A K Amunts K Eickhoff S B Mohlberg H et al (2005) The role of the left Brodmann rsquos areas

and 45 in reading words and pseudowords Cognitive Brain Research 25(3) 982ndash993Hickok G amp Poeppel D (2004) Dorsal and ventral streams a framework for understanding aspects of the functional anatomy

of language Cognition 92 67ndash99Hickok G amp Poeppel D (2007) The cortical organization of speech processing Nature Reviews 8 393ndash402Holland S K Plante E Weber Byars A Strawsburg R H Schmithorst V J amp Ball W S Jr (2001) Normal fMRI brain

activation patterns in children performing a verb generation task Neuroimage 14 837ndash843Holland S K Vannest J Mecoli M Jacola L M Tillema J M Karunanayaka P R et al (2007) Functional MRI of language

lateralization during development in children International Journal of Audiology 46 (9) 533ndash551Holodny A I Schulder M Ybasco A amp Liu W C (2002) Translocation of Brocarsquos area to the contralateral hemisphere as the

result of the growth of a left inferior frontal glioma Journal of Computer Assisted Tomography 26 (6) 941ndash943Hopf J M Bader M Meng M amp Bayer J (2003) Is human sentence parsing serial or parallel Evidence from event-related

brain potentials Cognitive Brain Research 15(2) 165ndash177Inui K Okamoto H Miki K Gunji A amp Kakigi R (2006) Serial and parallel processing in the human auditory cortex a

magnetoencephalographic study Cerebral Cortex 16 (1) 18ndash30Ishizaki M Ueyama H Nishida Y Imamura S Hirano T amp Uchino M (2012) Crossed aphasia following an infarction in the

right corpus callosum Clinical Neurology and Neurosurgery 114(2) 161ndash165




Jeon H A Lee K M Kim Y B amp Cho Z H (2009) Neural substrates of semantic relationships common and distinct left-frontal activities for generation of synonyms vs antonyms Neuroimage 48(2) 449ndash457

Kadis D S Pang E W Mills T Taylor M J McAndrews M P amp Smith M L (2011) Characterizing the normal developmentaltrajectory of expressive language lateralization using magnetoencephalography Journal of the International Neuropsycho-logical Society 17 (5) 896ndash904

Kennan R P Kim D Maki A Koizumi H amp Constable R T (2002) Non-invasive assessment of language lateralization by

transcranial near infrared optical topography and functional MRI Human Brain Mapping 16 (3) 183ndash

189Khedr E M Hamed E Said A amp Basahi J (2002) Handedness and language cerebral lateralization European Journal of Applied Physiology 87 (4ndash5) 469ndash473

Klein J C Behrens T E Robson M D Mackay C E Higham D J amp Johansen-Berg H (2007) Connectivity-based parcellationof human cortex using diffusion MRI establishing reproducibility validity and observer independence in BA 4445 andSMApre-SMA Neuroimage 34(1) 204ndash211

Knecht S Draumlger B Deppe M Bobe L Lohmann H Floumlel A et al (2000) Handedness and hemispheric language domi-nance in healthy humans Brain 123(12) 2512ndash2518

Knecht S Draumlger B Floumlel A Lohmann H Breitenstein C Deppe M et al (2001) Behavioural relevance of atypical languagelateralization in healthy subjects Brain 124(Pt 8) 1657ndash1665

Koelsch S Schulze K Sammler D Fritz T Muumlller K amp Gruber O (2009) Functional architecture of verbal and tonal workingmemory an FMRI study Human Brain Mapping 30(3) 859ndash873

Kosla K Pfajfer L Bryszewski B Jaskoacutelski D Stefanczyk L amp Majos A (2012) Functional rearrangement of language areas inpatients with tumors of the central nervous system using functional magnetic resonance imaging Polish Journal of Radi-ology 77 (3) 39ndash45

Kurthen M Helmstaedter C Linke D B Hufnagel A Elger C E amp Schramm J (1994) Quantitative and qualitative evaluationof patterns of cerebral language dominance An amobarbital study Brain and Language 46 (4) 536ndash564

Leclercq D Duffau H Delmaire C Capelle L Gatignol P Ducros M et al (2010) Comparison of diffusion tensor imagingtractography of language tracts and intraoperative subcortical stimulations Journal of Neurosurgery 112(3) 503ndash511

Lemaire J J Golby A Wells W M Pujol S Tie Y amp Rigolo L (2012) Extended Brocarsquos area in the functional connectome of language in adults combined cortical and subcortical single-subject analysis using fMRI and DTI tractography BrainTopography 26 (3) 428ndash441

Lidzba K Schwilling E Grodd W Kraumlgeloh-Mann I amp Wilke M (2011) Language comprehension vs language productionage effects on fMRI activation Brain and Language 119(1) 6ndash15

Lieacutegeois F Connelly A Cross J H Boyd S G Gadian D G Vargha-Khadem F et al (2004) Language reorganization inchildren with early-onset lesions of the left hemisphere an fMRI study Brain 127 (Pt 6) 1229ndash1236

Liu D Deters R amp Zhang W J (2010) Architectural design for resilience Enterprise Information Systems 4 137ndash152Lorenz M W Thoelen N Loesel N Lienerth C Gonzalez M Humpich M et al (2008) Assessment of cerebral autor-

egulation withrsquo transcranial Doppler sonography in poor bone windows using constant infusion of an ultrasound contrastagent Ultrasound Medical Biology 34(3) 345ndash353

Loring D W Meador K J Lee G P Murro A M Smith J R Flanigin H F et al (1990) Cerebral language lateralizationevidence from intracarotid amobarbital testing Neuropsychologia 28(8) 831ndash838

Loring D W Strauss E Hermann B P Perrine K Trenerry M R Barr W B et al (1999) Effects of anomalous languagerepresentation on neuropsychological performance in temporal lobe epilepsy Neurology 53(2) 260ndash264

Makuuchi M Bahlmann J Anwander A amp Friederici A D (2009) Segregating the core computational faculty of humanlanguage from working memory Proceedingof the National Academy of Sciences of U S A 106 (20) 8362ndash8367

Mandonnet E Nouet A Gatignol P Capelle L amp Duffau H (2007) Does the left inferior longitudinal fasciculus play a role inlanguage A brain stimulation study Brain 130(Pt 3) 623ndash629

Marieumln P Paghera B De Deyn P P amp Vignolo L A (2004) Adult crossed aphasia in dextrals revisited Cortex 40 41ndash74Matsumoto R Okada T Mikuni N Mitsueda-Ono T Taki J Sawamoto N et al (2008) Hemispheric asymmetry of the

arcuate fasciculus a preliminary diffusion tensor tractography study in patients with unilateral language dominancede1047297ned by Wada test Journal of Neurology 255(11) 1703ndash1711

McDermott K B Petersen S E Watson J M amp Ojemann J G (2003) A procedure for identifying regions preferentiallyactivated by attention to semantic and phonological relations using functional magnetic resonance imaging Neuro-

psychologia 41(3) 293ndash

303Mesulam M M (1990) Large-scale neurocognitive networks and distributed processing for attention language and memory Annals of Neurology 28(5) 597ndash613

Moumlddel G Lineweaver T Schuele S U Reinholz J amp Loddenkemper T (2009) Atypical language lateralization in epilepsypatients Epilepsia 50(6) 1505ndash1516

Molnar-Szakacs I Iacoboni M Koski L amp Mazziotta J C (2005) Functional segregation within pars opercularis of the inferiorfrontal gyrus evidence from fMRI studies of imitation and action observation Cerebral Cortex 15(7) 986ndash994

Muumlller R A Rothermel R D Behen M E Muzik O Mangner T J amp Chugani H T (1997) Receptive and expressive languageactivations for sentences a PET study Neuroreport 8(17) 3767ndash3770

Ni W Constable R T Mencl W E Pugh K R Fulbright R K Shaywitz S E et al (2000) An event-related neuroimagingstudy distinguishing form and content in sentence processing Journal of Cognitive Neurosciences 12(1) 120ndash133

Nucifora P G Verma R Melhem E R Gur R E amp Gur R C (2005) Leftward asymmetry in relative 1047297ber density of the arcuatefasciculus Neuroreport 16 (8) 791ndash794

Papathanassiou D Etard O Mellet E Zago L Mazoyer B amp Tzourio-Mazoyer N A (2000) Common language networkfor comprehension and production a contribution to the de1047297nition of language epicenters with PET Neuroimage 11(4)

347ndash357Pataraia E Billingsley-Marshall R L Castillo E M Breier J I Simos P G Sarkari S et al (2005) Organization of receptive

language-speci1047297c cortex before and after left temporal lobectomy Neurology 64(3) 481ndash487Pedersen P M Jargensen H S Nakayama H Raaschou H O amp Olsen T S (1995) Aphasia in acute stroke incidence de-

terminants and recovery Annals of Neurology 38 659ndash666




Powell H W Parker G J Alexander D C Symms M R Boulby P A Wheeler Kingshott C A et al (2006) Hemisphericasymmetries in language related pathways a combined functional MRI and tractography study Neuroimage 32(1)388ndash399

Price C J (2010) The anatomy of language a review of 100 fMRI studies published in 2009 Annals of the New York Academy of Sciences 1191 62ndash88

Rasmussen T amp Milner B (1977) The role of early brain injury in the lateralization of cerebral speech functions Annals of the

New York Academy of Sciences 299 35ndash

69Risse G L Gates J R amp Fangman M C (1997) A reconsideration of bilateral language representation based on the intracarotidamobarbital procedure Brain and Cognition 33(1) 118ndash132

Rodrigo S Oppenheim C Chassoux F Hodel J de Vanssay A Baudoin-Chial S et al (2008a) Language lateralization intemporal lobe epilepsy using functional MRI and probabilistic tractography Epilepsia 49(8) 1367ndash1376

Springer J A Binder J R Hammeke T A Swanson S J Frost J A Bellgowan P S et al (1999) Language dominance inneurologically normal and epilepsy subjects a functional MRI study Brain 122(Pt 11) 2033ndash2046

Staudt M Lidzba K Grodd W Wildgruber D Erb M amp Kraumlgeloh M (2002) Right hemispheric organization of languagefollowing early left-sided brain lesions functional MRI topography Neuroimage 16 (4) 954ndash967

Sza1047298arski J P Holland S K Schmithorst V J amp Byars A W (2006) fMRI study of language lateralization in children andadults Human Brain Mapping 27 202ndash212

Tanaka N Liu H Reinsberger C Madsen J R Bourgeois B F Dworetzky B A et al (2013) Language lateralization rep-resented by spatiotemporal mapping of magnetoencephalography American Journal of Neuroradiology 34(3) 558ndash563

Taylor-Sarno M amp Levita E (1981) Some observations on the nature of recovery in global aphasia after stroke Brain andLanguage 13(1) 1ndash12

Thiel A Herholz K von Stockhausen H M van Leyen-Pilgram K Pietrzyk U Kessler J et al (1998) Localization of language-related cortex with 15O-labeled water PET in patients with gliomas Neuroimage 7 (4 Pt 1) 284ndash295

Townsend J (1990) Serial vs Parallel processing sometimes they Look like Tweedledum and Tweedledee but they can (andshould) Be distinguished Psychology Science 1 36ndash53

Tyler L K Wright P Randall B Marslen-Wilson W D amp Stamatakis E A (2010) Reorganization of syntactic processingfollowing left-hemisphere brain damage does right-hemisphere activity preserve function Brain 133(11) 3396ndash3408

Vernooij M W Smits M Wielopolski P A Houston G C Krestin G P amp van der Lugt A (2007) Fiber density asymmetry of the arcuate fasciculus in relation to functional hemispheric language lateralization in both right- and left-handed healthysubjects a combined fMRI and DTI study Neuroimage 35(3) 1064ndash1076

Vigneau M Beaucousin V Herveacute P Y Jobard G Petit L Crivello F et al (2011) What is right-hemisphere contribution tophonological lexico-semantic and sentence processing Insights from a meta-analysis Neuroimage 54(1) 577ndash593

Vikingstad E M Cao Y Thomas A J Johnson A F Malik G M amp Welch K M (2000) Language hemispheric dominance inpatients with congenital lesions of eloquent brain Neurosurgery 47 (3) 562ndash570

Weiller C Isensee C Rijntjes M Huber W Muumlller S Bier D et al (1995) Recovery from Wernicke rsquos aphasia a positronemission tomographic study Annals of Neurology 37 (6) 723ndash732

Wernicke C (1874) Der Aphasiche Symptomencomplex Breslau Cohn amp WeigertWillems R M Ozyuumlrek A amp Hagoort P (2009) Differential roles for left inferior frontal and superior temporal cortex in

multimodal integration of action and language Neuroimage 47 (4) 1992ndash2004Wing1047297eld A amp Grossman M (2006) Language and the aging brain patterns of neural compensation revealed by functional

brain imaging Journal of Neurophysiology 96 2830ndash2839Woermann F G Jokeit H Luerding R Freitag H Schulz R Guertler S et al (2003) Language lateralization by Wada test

and fMRI in 100 patients with epilepsy Neurology 61(5) 699ndash701




in extensive studies using the intracarotid amytal test (so-called ldquoWada testrdquo) (eg Kurthen et al 1994

Loring et al 1999 Moumlddel Lineweaver Schuele Reinholz amp Loddenkemper 2009 Woermann et al

2003) Modern modalities of non-invasive neuroimaging and electro-physiology procedures have

validated those initial 1047297ndings as well fMRI (eg Binder 2011 Holland et al 2007 Price 2010) near

infra-red spectroscopy (Bembich Demarini Clarici Massaccesi amp Grasso 2011 Bisconti Di Sante

Ferrari amp Quaresima 2012 Kennan Kim Maki Koizumi amp Constable 2002) magneto-encephalography (Kadis et al 2011) and diffusion tensor imagingtractography (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 laterali-

zation in 326 healthy individuals with functional transcranial Doppler sonography (a non invasive

technique measures the velocity of blood 1047298ow through the brainrsquos blood vessels using pulsed Doppler

transducer - ultrasonic pulse probe that detects the re1047298ected 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 frac14 100) to 15 in ambidextrous individuals and 27 in strong left-handers (handedness frac14100)However this technique may be in1047298uenced 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 left-

handers and 75 right-handers) left-handers exhibited right language dominance in 773 of cases

while bilateral representation was observed in 147 and left dominance in 8 of the subjects 933 of

right-handers showed left side dominance and 67 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 sub-

divided 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 82 exhibited disruptionwith stimulation in either hemisphere 42 of subjects had disruption with stimulus in the right

hemisphere In strongly left-handed subjects 737 of subjects had left hemisphere dominance 158

had bilateral representation and 105 had right side dominance In ambidextrous subjects bilateral

representation was observed in 57 of cases The authors concluded that speech lateralized to the left-

side cerebral dominance in strongly right- and left-handed subjects but bilateral cerebral represen-

tation 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 Socieacuteteacute de Anthropologie de Paris Paul Broca explicitly stated Nous

parlons avec lrsquo heacutemisphegravere gauche

dWe speak with the left hemisphere

rdquo (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 right-

handers This hypothesis has been referred as ldquoconjunction hypothesisrdquo (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 ldquocrossed

aphasiardquo 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 in-

dividual with left hemiplegia that is an aphasia resulting from a cerebral lesion lsquoipsilateralrsquo to the

dominant hand Noteworthy just a few crossed aphasics were right-handers but most were left-

handers He considered that crossed aphasia is relatively frequent as a transient disorder but it isextremely unusual as a permanent syndrome in this latter case it is only found in left-handers Heacutecaen

amp Albert (1978) suggested that the term ldquocrossed aphasiardquo should be used only to refer to aphasia

following right hemisphere pathology in a right-handed person and this is the way the term ldquocrossed

aphasiardquo is currently used (Ishizaki et al 2012 Marieumln Paghera De Deyn amp Vignolo 2004)










Confraria 1984)











in left-handers

























































41 Wada test







tests are repeated



















Table 1


Author No

Sjcts

Hand (R) (L) Left-H

Dom

Right H

Dom

Bilat

Dom



Observati

Rasmussen and

Milner (1977)

262 140 122 96 (R) 4 (R) 0 None

70 (L) 15 (L) 15 (L)




-Subpatterns




of subfunctions


of subfunctions

Left domi

Right dom

Incomple

Incomple

Strongly b

23 (L) 32 (L) 45 (L)


comprehension



hemisphere


subjects f

of BrocaW

62 (L) 18 (L) 20 (L)






Bilateral dependent

Bilateral a

either left

language

Benbadis

speech ar

lateralizat

48 (L) 29 (L) 23 (L)


Bilateral dependent

69 patien

of languag


48 (L) 22 (L) 30 (L)

Total 1799 1446 353 86 (R) 4 (R) 10 (R)

50 (L) 23 (L) 27 (L)







Wada tests





















2001)























































subjects


disrupted






hemisphere



































fashion
















1 ER ER

2 ER E

3 E ER

4 ER R

5 R RE

6 E R

7 R E






















































































distinguished





















Radiology)






right-hander



















































































modularity

Table 2





























8 Conclusion









References












CR697

Table 3







Expressive

Receptive

Both


processing)



Both


BrocaWernicke












































































































Confraria 1984)











in left-handers

























































41 Wada test







tests are repeated



















Table 1


Author No

Sjcts

Hand (R) (L) Left-H

Dom

Right H

Dom

Bilat

Dom



Observati

Rasmussen and

Milner (1977)

262 140 122 96 (R) 4 (R) 0 None

70 (L) 15 (L) 15 (L)




-Subpatterns




of subfunctions


of subfunctions

Left domi

Right dom

Incomple

Incomple

Strongly b

23 (L) 32 (L) 45 (L)


comprehension



hemisphere


subjects f

of BrocaW

62 (L) 18 (L) 20 (L)






Bilateral dependent

Bilateral a

either left

language

Benbadis

speech ar

lateralizat

48 (L) 29 (L) 23 (L)


Bilateral dependent

69 patien

of languag


48 (L) 22 (L) 30 (L)

Total 1799 1446 353 86 (R) 4 (R) 10 (R)

50 (L) 23 (L) 27 (L)







Wada tests





















2001)























































subjects


disrupted






hemisphere



































fashion
















1 ER ER

2 ER E

3 E ER

4 ER R

5 R RE

6 E R

7 R E






















































































distinguished





















Radiology)






right-hander



















































































modularity

Table 2





























8 Conclusion









References












CR697

Table 3







Expressive

Receptive

Both


processing)



Both


BrocaWernicke





























































































































41 Wada test







tests are repeated



















Table 1


Author No

Sjcts

Hand (R) (L) Left-H

Dom

Right H

Dom

Bilat

Dom



Observati

Rasmussen and

Milner (1977)

262 140 122 96 (R) 4 (R) 0 None

70 (L) 15 (L) 15 (L)




-Subpatterns




of subfunctions


of subfunctions

Left domi

Right dom

Incomple

Incomple

Strongly b

23 (L) 32 (L) 45 (L)


comprehension



hemisphere


subjects f

of BrocaW

62 (L) 18 (L) 20 (L)






Bilateral dependent

Bilateral a

either left

language

Benbadis

speech ar

lateralizat

48 (L) 29 (L) 23 (L)


Bilateral dependent

69 patien

of languag


48 (L) 22 (L) 30 (L)

Total 1799 1446 353 86 (R) 4 (R) 10 (R)

50 (L) 23 (L) 27 (L)







Wada tests





















2001)























































subjects


disrupted






hemisphere



































fashion
















1 ER ER

2 ER E

3 E ER

4 ER R

5 R RE

6 E R

7 R E






















































































distinguished





















Radiology)






right-hander



















































































modularity

Table 2





























8 Conclusion









References












CR697

Table 3







Expressive

Receptive

Both


processing)



Both


BrocaWernicke






































































































Table 1


Author No

Sjcts

Hand (R) (L) Left-H

Dom

Right H

Dom

Bilat

Dom



Observati

Rasmussen and

Milner (1977)

262 140 122 96 (R) 4 (R) 0 None

70 (L) 15 (L) 15 (L)




-Subpatterns




of subfunctions


of subfunctions

Left domi

Right dom

Incomple

Incomple

Strongly b

23 (L) 32 (L) 45 (L)


comprehension



hemisphere


subjects f

of BrocaW

62 (L) 18 (L) 20 (L)






Bilateral dependent

Bilateral a

either left

language

Benbadis

speech ar

lateralizat

48 (L) 29 (L) 23 (L)


Bilateral dependent

69 patien

of languag


48 (L) 22 (L) 30 (L)

Total 1799 1446 353 86 (R) 4 (R) 10 (R)

50 (L) 23 (L) 27 (L)







Wada tests





















2001)























































subjects


disrupted






hemisphere



































fashion
















1 ER ER

2 ER E

3 E ER

4 ER R

5 R RE

6 E R

7 R E






















































































distinguished





















Radiology)






right-hander



















































































modularity

Table 2





























8 Conclusion









References












CR697

Table 3







Expressive

Receptive

Both


processing)



Both


BrocaWernicke









































































































Wada tests





















2001)























































subjects


disrupted






hemisphere



































fashion
















1 ER ER

2 ER E

3 E ER

4 ER R

5 R RE

6 E R

7 R E






















































































distinguished





















Radiology)






right-hander



















































































modularity

Table 2





























8 Conclusion









References












CR697

Table 3







Expressive

Receptive

Both


processing)



Both


BrocaWernicke

































































































































subjects


disrupted






hemisphere



































fashion
















1 ER ER

2 ER E

3 E ER

4 ER R

5 R RE

6 E R

7 R E






















































































distinguished





















Radiology)






right-hander



















































































modularity

Table 2





























8 Conclusion









References












CR697

Table 3







Expressive

Receptive

Both


processing)



Both


BrocaWernicke





























































































































fashion
















1 ER ER

2 ER E

3 E ER

4 ER R

5 R RE

6 E R

7 R E






















































































distinguished





















Radiology)






right-hander



















































































modularity

Table 2





























8 Conclusion









References












CR697

Table 3







Expressive

Receptive

Both


processing)



Both


BrocaWernicke
























































































































































































distinguished





















Radiology)






right-hander



















































































modularity

Table 2





























8 Conclusion









References












CR697

Table 3







Expressive

Receptive

Both


processing)



Both


BrocaWernicke








































































































right-hander



















































































modularity

Table 2





























8 Conclusion









References












CR697

Table 3







Expressive

Receptive

Both


processing)



Both


BrocaWernicke



















































































































































modularity

Table 2





























8 Conclusion









References












CR697

Table 3







Expressive

Receptive

Both


processing)



Both


BrocaWernicke












































































































8 Conclusion









References












CR697

Table 3







Expressive

Receptive

Both


processing)



Both


BrocaWernicke




































































































bilateraliad lenguaje

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