University of Groningen

Cerebellar induced differential polyglot aphasia
Marien, Peter; van Dun, Kim; Van Dormael, Johanna; Vandenborre, Dorien; Keulen, Stefanie;
Manto, Mario; Verhoeven, Jo; Abutalebi, Jubin
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Brain and Language
DOI:
10.1016/j.bandl.2017.09.001
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Marien, P., van Dun, K., Van Dormael, J., Vandenborre, D., Keulen, S., Manto, M., Verhoeven, J., &
Abutalebi, J. (2017). Cerebellar induced differential polyglot aphasia: A neurolinguistic and fMRI study.
Brain and Language, 175, 18-28. https://doi.org/10.1016/j.bandl.2017.09.001

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Brain and Language 175 (2017) 18–28

Contents lists available at ScienceDirect

Brain and Language
journal homepage: www.elsevier.com/locate/b&l

Cerebellar induced differential polyglot aphasia: A neurolinguistic and fMRI
study

MARK

⁎

Peter Mariëna,b,1, , Kim van Duna,1, Johanna Van Dormaelc, Dorien Vandenborrea,d,
Stefanie Keulena,e, Mario Mantof, Jo Verhoeveng, Jubin Abutalebih
a

Clinical and Experimental Neurolinguistics, CLIN, Vrije Universiteit Brussel, Brussels, Belgium
Department of Neurology and Memory Clinic, ZNA Middelheim Hospital, Antwerp, Belgium
c
Department of Neurological Rehabilitation, University Hospital Brussels, Brussels, Belgium
d
Speech therapy and audiology, Thomas More, Antwerp, Belgium
e
Center for Language and Cognition, Rijksuniversiteit Groningen, Groningen, The Netherlands
f
Unité d’Étude du Mouvement, FNRS Neurologie, ULB Erasme, Brussels, Belgium
g
Department of Language and Communication Science, City University, London, UK
h
Centre for Neurolinguistics and Psycholinguistics, University Vita-Salute San Raffaele, Milan, Italy
b

A R T I C L E I N F O

A B S T R A C T

Keywords:
Cerebellum
Polyglot aphasia
Bilingualism
fMRI
Differential recovery

Research has shown that linguistic functions in the bilingual brain are subserved by similar neural circuits as in
monolinguals, but with extra-activity associated with cognitive and attentional control. Although a role for the
right cerebellum in multilingual language processing has recently been acknowledged, a potential role of the left
cerebellum remains largely unexplored.
This paper reports the clinical and fMRI findings in a strongly right-handed (late) multilingual patient who
developed differential polyglot aphasia, ataxic dysarthria and a selective decrease in executive function due to
an ischemic stroke in the left cerebellum. fMRI revealed that lexical-semantic retrieval in the unaffected L1 was
predominantly associated with activations in the left cortical areas (left prefrontal area and left postcentral
gyrus), while naming in two affected non-native languages recruited a significantly larger bilateral functional
network, including the cerebellum. It is hypothesized that the left cerebellar insult resulted in decreased right
prefrontal hemisphere functioning due to a loss of cerebellar impulses through the cerebello-cerebral pathways.

1. Introduction

and level of exposure (Abutalebi, 2008; Perani & Abutalebi, 2005). A
more divergent network is associated with late acquisition of the L2
language (Liu & Cao, 2016) and less proficiency (Kotz, 2009). As outlined by Abutalebi and Green (2007), a non-native language which is
not processed with the same ease as L1 is less automatized in neurocognitive terms and as such in need of increased cognitive control (i.e.,
language control). These language control mechanisms allow multilinguals to adequately suppress one language while communicating in
another and to flawlessly switch between several target languages.
Converging evidence from clinical and experimental neuroimaging
studies shows that the neural system subserving language control and
selection processes consists of a widely distributed general cognitive
control system mainly involving the bilateral dorsolateral prefrontal
areas (specifically the middle and inferior frontal gyri), the anterior
cingulate cortex, the bilateral inferior parietal lobules, and subcortical
structures such as the basal ganglia, the thalamus, and the cerebellum

During the past decades a substantial amount of clinical and experimental research has been dedicated to the functional organization
of the bilingual brain and the neural networks subserving language
processing in bi- or multilinguals in comparison to monolinguals.
Findings from these studies have reported that essentially monolinguals
and bilinguals process languages in the same neural fashion with the
exception that bilingual language processing is often paralleled by
extra-activity in areas related to cognitive and attentional control
(Abutalebi & Green, 2007, 2016). This extra-activity is usually associated with some specific factors related to second language (L2) processing. Indeed, much of the available literature on the neurobiology of
multilingualism indicates that the neural representation and organization of language is the product of a complex process depending on
various factors such as age of language acquisition, level of proficiency

⁎

1

Corresponding author at: Department of Neurology, ZNA Middelheim, Lindendreef 1, B-2020 Antwerp, Belgium.
E-mail address: peter.marien5@telenet.be (P. Mariën).
The first two authors (PM and KvD) contributed equally to the manuscript.

http://dx.doi.org/10.1016/j.bandl.2017.09.001
Received 22 March 2017; Received in revised form 27 June 2017; Accepted 3 September 2017
Available online 14 September 2017
0093-934X/ © 2017 Elsevier Inc. All rights reserved.

Brain and Language 175 (2017) 18–28

P. Mariën et al.

ganglia, a 68-year-old right-handed woman developed bilingual
aphasia affecting expression in her mother tongue (Venetian) more than
in her second language (Italian) while comprehension was preserved in
both languages (Aglioti & Fabbro, 1993; Aglioti et al., 1996). Left
temporal lobe damage, on the other hand, resulted in a loss of all expressive and receptive second language skills, leaving his mother
tongue fully intact (Ku et al., 1996). In our case, the pathological
fixation on his mother tongue was linked to damage to the left cerebellum. A hypothesis is put forward to explain the selective disruption
of the non-native languages due to left cerebellar stroke.

(Abutalebi & Green, 2016; Green & Abutalebi, 2013). Although crucial
involvement of the basal ganglia (e.g. thalamus, left caudate, left putamen) in bilingual language processing has been convincingly demonstrated (Abutalebi, Della Rosa, Castro Gonzaga, et al., 2013;
Abutalebi, Della Rosa, Ding, et al., 2013; Crinion et al., 2006; Zou,
Ding, Abutalebi, Shu, & Peng, 2012), a possible role of the recently
acknowledged linguistic and cognitive posterior cerebellum, specifically including lobule VII and Crus I, and part of the prefronto-cerebellar loop involved in language and executive control
(Stoodley & Schmahmann, 2009) in bilingual language processing has
been much less explored.
The cerebellum is linked to all the key regions of the language
control network and in their adaptive control model
(Green & Abutalebi, 2013), Green and Abutalebi (2013) attribute a role
in “opportunistic planning” to the cerebellum during multilingual language processing. This model attributes a prominent role to the cerebellar - left prefrontal connection in using more readily available L1
words/structures to convey meaning in a less proficient language
(Green & Abutalebi, 2013). Functional imaging studies using sentence
production and comprehension tasks have to elucidate this view but, as
hypothesized (Abutalebi & Green, 2016), it is plausible that cerebellar
activation mediates the prediction of future input (L2 processing) based
on past knowledge (L1 structures/vocabulary) (Ito, 2008). The ability
to make predictions entails maintaining an ongoing representation,
which ensures resistance to interference (Abutalebi & Green, 2016).
Several studies have reported changes in cerebellar grey matter density
in bilingual speakers correlated to proficient performance (bilateral
VIIa Crus I/II and right lobule V (Pliatsikas, Johnstone, & Marinis,
2014))2; and the density in the right posterior vermis might predict the
ease with which they resist interference from their first language
(Filippi et al., 2011). These studies imply a cerebellar role in the multilingual control network, although the role of the cerebellum in prediction has been challenged (Argyropoulos, 2016).
Clinical findings might contribute to our knowledge about the cerebellar role in multilingualism, but bilingual or polyglot aphasia is a
diverse and complex phenomenon that is still poorly understood
(Paradis & Libben, 2014). A variety of aphasia symptoms and recovery
patterns have been observed in bilinguals/multilinguals after stroke in
language-critical regions (Lorenzen & Murray, 2008). Although parallel
recovery typically occurs in most of the multilingual cases, a number of
non-parallel recovery patterns have been documented in the literature
(Fabbro, 2001). Green and Abutalebi (2008) argued that non-parallel
recovery in multilingual aphasia is due to disruption of the language
control network. One such pattern of non-parallel recovery is involuntary and uncontrolled ‘pathological language mixing and
switching’ (Mariën, Abutalebi, Engelborghs, & De Deyn, 2005; Kong,
Abutalebi, Lam, & Weekes, 2014). Damage to the fronto(-parieto)-subcortical circuit can lead to pathological language switching and mixing,
and even to fixation on one single language (Green & Abutalebi, 2008).
Kong et al. (2014) related pathological language mixing and switching
to an impairment of executive functions, suggesting a shared frontobasal ganglia network between the domain-general executive system
and language control.
We report the clinical and functional neuroimaging findings in a
strongly right-handed multilingual patient who following a left cerebellar stroke developed aphasia in each of the six languages he acquired
as a late polyglot, while his mother tongue (L1) remained largely unaffected (differential polyglot aphasia). Pathological fixation on one
language has been previously reported after subcortical damage
(Aglioti, Beltramello, Girardi, & Fabbro, 1996; Aglioti & Fabbro, 1993),
and after damage to the language-dominant temporal lobe (Ku,
Lachmann, & Nagler, 1996). After a stroke affecting the left basal

2. Case report
2.1. History
A 72-year-old right-handed man was admitted to hospital after
acute onset of language disturbances, balance problems, vertigo, and
vomiting. On admission, the clinical neurological examination revealed
left-sided ataxia with a strong tendency to fall over to the right side. He
could stand up straddled. He was not able to understand or express
himself in any other but his maternal language (English (L1)) that was
unaffected, apart from mild word-finding difficulties for low-frequency
words and mild ataxic dysarthria (slurred speech):
“I was watching television at my apartment in Antwerp when suddenly the room seemed to spin around violently. I tried to stand but
was unable to do so. I felt a need to vomit and managed to crawl to
the bathroom to take a plastic bowl. My next instinct was to call the
emergency services, but the leaflet I have outlining the services was
in Dutch and for some reason, I was unable to think (or speak) in any
other language than my native English. I have lived in Antwerp for
many years and use Dutch (Flemish) on a day-to-day basis. I called
my son-in-law, who speaks fluent English and he drove me to
Middelheim Hospital. We normally speak English when together. I
understood none of the questions asked of me in Dutch by hospital
staff and they had to be translated back to me in English. My speech
was slurred. I had lost some words, I was aware of that, but I cannot
recall which words. I made no attempt to speak any of the other
languages I know, and in the first hours of my mishap happening, I
do not think I realized that I had other languages.”
Medical history consisted of arterial hypertension, type 2 diabetes
mellitus and a right occipital infarction 10 years before the current
stroke. He had an educational level of 12 years (grammar school) and
had worked as a war and political correspondent for British, US and
Australian newspapers in several countries for more than 40 years. He
mastered seven languages: English (maternal language; L1), French
(learned at school from age 11 onwards, L2), German (learned at school
from age 13 onwards, L3), Slovene (L4) and Serbo-Croat (L5) (learned
by means of a crash course at age 24), Hebrew (Ivrit, learned during an
intensive course at age 28, L6), and Dutch (moved to live in Belgium
from age 35 onwards, L7). He used English (L1), Dutch (L7) and French
(L2) on a nearly daily basis. He was in regular contact with friends in
Belgrade and Berlin with whom he communicated in Serbo-Croat (L5)
and German (L3). He read the Serbian and German press online and
followed several forums that talk of the old Yugoslavia, its politics and
economics.
T2-weighted axial FLAIR MRI of the brain showed an inhomogeneous hyperintense lesion in the territory of the medial branch
of the left PICA slightly encroaching upon the posterior portion of the
lower medulla at the left (gracile and cuneate nuclei) consistent with a
recent infarction in the vascular territory of the left PICA (Fig. 1A–C).
An old vascular lesion in the left occipital lobe (Fig. 1D and E) and some
periventricular white matter lesions were found as well (Fig. 1F). Diffusion-weighted MRI (axial images) confirmed a hyperintense signal in
the territory of the medial branch of left PICA (Fig. 2A–C) with involvement of the medial portion of left dentate nucleus. Based on the

2
All cerebellar anatomy terminology is in accordance with Schmahmann, Doyon,
Petrides, Evans, and Toga (2000).

19

Brain and Language 175 (2017) 18–28

P. Mariën et al.

Fig. 1. Structural MRI of the brain. Axial MR images showing a hyperintense signal in the territory of the medial branch of left posterior inferior cerebellar artery (PICA; white arrows in
A, B, C), with a small extension to the posterior portion of the lower medulla on the left (gracile and cuneate nuclei; arrowhead in A). The inferior cerebellar peduncles (dotted arrows in
B) and the middle cerebellar peduncles (dotted arrows in C) are spared, as well as the mesencephalon (dotted arrows in D). Hypersignals in left occipital lobe (D, E) and periventricular
white matter (F) are detected. Legend: R = right.

fluency. I carry out a simple test: counting to 20 in each language,
and trying to form easy sentences. I felt inwardly pleased with my
progress.”

type of the stroke and the MRI, part of lobules VIIIa/VIIIb and IX were
likely affected, together with VIIa Crus I/II. MR angiography (axial
image) showed a hyperintense area in the lumen of left vertebral artery
instead of a flow void (Fig. 2D). The angiogram revealed an absence of
opacification of left vertebral artery (Fig. 2E). Anticoagulant therapy
was started.
By the end of the first day remission of ataxic dysarthria was noted.
The patient indicated that Dutch gradually began to return from the
second day poststroke onwards and that a reversion to a previously
learnt accent (Antwerp dialect and Estuary English) had taken place in
both his mother tongue and in Dutch:

In-depth neuropsychological and neurolinguistic investigations
were performed one week after stroke (see Section 2.2) and language
therapy as well as an intensive locomotor rehabilitation programme
were started which substantially improved gait and balance. During the
next four weeks language skills gradually improved but apart from his
mother tongue, all non-native languages remained affected at the lexical and syntactic level. In addition, non-native speech was characterized by the phenomenon of language mixing and switching:

“My Dutch began to return in the mid-day, by no means perfect, but
enough to converse with the nursing staff. When speaking Dutch,
there is a “voice in my head” telling me that I am not speaking with
good grammar, but I am pleased I can converse and be understood. I
was still struggling for some everyday words and grammar. There
appears to be more Antwerp accent (local) when speaking, though
not at all times. (…) My English is no longer impaired in any way,
though I still have trouble in finding certain words, words that I
know, but do not use every day. I then find the word I was looking
for in the morning popping into my mind for no apparent reason in
the middle of the afternoon. In several years of commuting between
Europe and Australia (five or six times a year for more than
12 years) as editor of a magazine, I had adopted a bit of an
Australian accent, and the tendency to put the stress on certain
words, sometimes making a sentence sound more like a question.
That has gone. I am speaking in a more Estuary English, the English
of my younger days (southern England).”

“Words in all my languages are coming back to me. Many are words
that I have learned over the years, but rarely have use for – words
that do not fit into my everyday life. My Dutch is often ‘local’ – but
when reading Gazet van Antwerpen [Flemish newspaper] and De
Telegraaf [Hollandic newspaper], I recognize instantly the different
styles of language. (…) I have tried to recall my Slovene, but it gets
mingled badly with Serbo-Croat. The same goes for German, which
reverts to Dutch (mixed up). Dutch and German have considerable
similarity (my opinion) and Serbo-Croat and Slovene both are Slavic
languages with many similarities.”

2.2. Neuropsychological and neurolinguistic investigations
In-depth neurocognitive assessments were performed in the patient's maternal language one week poststroke on the basis of standardized clinical test batteries. Neuropsychological assessments consisted
of the Mini Mental State Examination (MMSE; Folstein,
Folstein, & McHugh, 1987), the revised version of the Repeatable Battery for the Assessment of Neuropsychological Status (RBANS;
Randolph, 1998), Raven’s Colored Progressive Matrices (Raven, 1965),

On the third day poststroke the patient noted that the other languages also started to return:
“I find my other languages starting to return, in varying degrees of

20

Brain and Language 175 (2017) 18–28

P. Mariën et al.

Fig. 2. Magnetic Resonance Angiography. Diffusion-weighted MRI (axial images) confirming a hyperintense signal in the territory of the medial branch of left posterior inferior cerebellar
artery (PICA; white arrows in A, B, C). Note the involvement of the medial portion of left dentate nucleus. MR angiography (axial image) shows an area of hypersignal in the lumen of left
vertebral artery instead of a flow void (white arrow in D). The angiogram reveals an absence of opacification of left vertebral artery (E). Legend: R = right.

depressed, low average ability to inhibit a competing and more automatic response set.
Assessment of native language functions by means of the CAT revealed maximum scores for all subtests. By contrast, the CAT-NL disclosed a profile (Table 2) in which reading at both the comprehension
and production (reading aloud) level was better preserved than oral and
written language production. Oral language comprehension was severely affected at the word (24/30; z: −2.6), sentence (24/32; z: −4.0)
and paragraph level (2/4; z: −2.1) while written language comprehension only scored in the defective range at the word level (24/30; z:
−5.5). Repetition was only preserved for complex words. By contrast,
pathological scores were obtained for word (16/32; z: −11.0), nonword (2/10; z: −3.8) and sentence repetition (4/6; z: −4.5). Digit
string repetition was depressed and scored in the clinical defective
range (4/7; z: −1.6). As reflected by a total score of 24/58 naming was
severely disrupted. Object (18/48; z: −5.7) and action naming (6/10; z:
−4.4) scored in the severely pathological range. Examination of
reading skills only disclosed a pathological result for word reading (44/
48; z: −2.2). The reading of complex words, function words and nonwords was normal. Writing skills were severely disrupted. The patient
scored within the severely pathological range for written picture
naming (10/23; z: −5.8) and writing to dictation (22/28; z: −4.5).
Agrammatism was found in oral as well as written language production.
Paraphasias (phonematic and semantic) only exceptionally occurred
but speech and written language output was characterized by the intrusion of foreign words (English).
Visual confrontation naming was normal for English (BNT: 57/60, z:
+0.3) but scored in the severely defective range for Dutch (BNT: 25/

the Stroop Color Word Test (Golden, 1978), and the Wisconsin Card
Sorting Test (WCST; Heaton, Chelune, Talley, Kay, & Curtis, 1993).
Formal investigation of language was performed in both English and
Dutch by means of the English and Dutch version of the Comprehensive
Aphasia Test (CAT; Howard, Swinburn, & Porter, 2004; CAT-NL; VischBrink, De Smet, & Mariën, 2014), the Boston Naming Test (BNT)
(English: Kaplan, Goodglass, & Weintraub, 1983; Dutch: Mariën,
Mampaey, Vervaet, Saerens, & De Deyn, 1998), and semantic verbal
fluency tasks consisting of the production of as many names as possible
of animals, means of transport, vegetables and clothes during one
minute (unpublished norms). Neuropsychological and neurolinguistic
test results are shown in Tables 1 and 2. A z-score of −1.5 was considered clinically abnormal. A z-score of more than −2 was considered
pathological.
A strong and consistent right hand preference was objectified by
means of the Edinburgh Handedness Inventory (Oldfield, 1971) demonstrating a laterality quotient of +100. General cognitive screening
was normal (MMSE: 27/30, z: −0,6). The RBANS showed a superior
visuospatial/constructive skill index (= 121, z: +1,40) and a very
superior immediate recall index (= 136, z: +2,40). Language (= 96, z:
−0,27), attention (= 94, z: −0,4), and delayed recall (= 101, z:
+0,07) were within the normal range, although a clinically abnormal
score was found for figure recall. Raven’s Colored Progressive Matrices
revealed a high average spatial intelligence level (pct. 90). The ability
to form abstract concepts, to shift and maintain goal-oriented cognitive
strategies in response to changing environmental contingencies as
measured by means of the WCST was normal as well (4 categories
within 64 trials). The Stroop Color Word test (pct. 15) showed a
21

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P. Mariën et al.

60, z: −10,6) (Table 1). The majority of errors consisted of ‘don't know
responses’ (n = 18/35 errors) and intrusions of foreign (English) words
(n = 11/35 errors). Controlled oral word association (semantic word
fluency) scored within the low average range (38 items, z: −1.2).

Table 1
Neurocognitive test results 2 weeks poststroke.
Neurocognitive tests

Global cognitive screening
Mini Mental State Examination
RBANS
Learning
- List Learning
- Story Memory
Visuo-spatial
- Figure Copy
- Line Orientation
Language
- Picture Naming
- Semantic Fluency
Attention
- Digit Span
- Coding
Recent Memory
- List Recall
- List Recognition
- Story Recall
- Figure Recall
Language
Boston Naming Test (English)
Boston Naming Test (Dutch)
Executive Functions
Wisconsin Card Sorting Test
Controlled Oral Word Association
- Semantic Fluency
Stroop Color-Word Test
- Card I
- Card II
- Card III
Frontal Assessment Battery
Raven’s Colored Progressive
Matrices

(Raw Score or SS) z-score
or Pc

Mean

SD

(27/30) −0,6

28

1,6

2.3. Functional Magnetic Resonance imaging (fMRI)

(1 3 6) +2,4
(34) +1,5
(24) +1,8
(1 2 1) +1,4
(19) +0,6
(20) +1,3
(96) −0,2
(10) +0,5
(17) −0,5
(94) −0,4
(10) −0,1
(35) −0,7
(1 0 1) +0,07
(8) +1,2
(20) +1,7
(11) −8,2
(6) −1,3

100
26,5
17,4
100
17,8
16,4
100
9,6
19,8
100
10,4
41,3
100
4,9
12,5
19,2
41,3

15,0
5,0
3,6
15,0
1,8
2,8
15,0
0,7
5,2
15,0
2,5
9,0
15,0
2,5
11,2
1,0
9,0

(57/60) +0,3
(25/60) −10,6

53,0
54,9

7,3
2,8

(4/64) −0,3

5,58

1,10

(38) −1,2

56,1

15,13

(46″) Pc 45
(44″) Pc 90
(129″) Pc 15
18/18
Pc 90

48
63
99

2.3.1. Stimuli and tasks
To build a set of items for fMRI purposes, an experimental visual
confrontation naming task was constructed that consisted of a selection
of 50 black and white drawings (Snodgrass & Vanderwart, 1980), of
high-frequency words in English (L1) (Snodgrass & Vanderwart, 1980),
French (L2) (Alario & Ferrand, 1999), German (L3) (Bates et al., 2003),
Serbo-Croat (L4) (Kostíc, 1999), Slovenian (L5) (Erjavec & Dzeroski,
2004), Hebrew (L6) (Frost & Plaut, 2001), and Dutch (L7) (Keuleers,
Brysbaert, & New, 2010).
Administration of the naming tests one month poststroke showed
that the patient named less than 20 percent of the high-frequency items
correctly in German, Hebrew, Serbo-Croat and Slovenian and more
than 80 percent in English (L1), French (L2) and Dutch (L7). Only the
sets in which he scored above 80 percent correct were retained for fMRI
purposes. Three sets consisting of 40 high-frequency items that were all
named correctly in English (L1), French (L2) and Dutch (L7) were included in the fMRI paradigm.
Four blocks of ten images were generated for each language, and
four blocks of control line drawings without meaning (scribbles) for a
total of 16 blocks. Each of the 40 black and white drawings were presented to the patient just before the actual scanning to make sure he
could still name the object or animal in the requested language. The
blocks were presented randomly during the scan with nine seconds rest
between the blocks to avoid switching effects. Each image was shown
for three seconds, resulting in blocks of 30 s. To indicate in which
language the patient had to name the depicted item, the flag of the
country (United Kingdom (L1), Belgium (L7), France (L2)) was added in
the upper left corner of the images. The patient named the pictures
covertly to avoid movement artefacts. Therefore the entire block of 30 s
was used in the analysis to identify naming activations.

Legend: SS = standard score; SD = Standard Deviation; Pc = percentile; RBANS =
Repeatable Battery for the Assessment of Neuropsychological Status Cut-off score for the
Frontal Assessment Battery is 14/18.

Table 2
Test results comprehensive aphasia Test-NL.
Subtests

(Raw Score) z-score

Cut-off

Mean

SD

Language comprehension

Oral
Words
Sentences
Paragraphs
Written
Words
Sentences

(50/66) −4.1
(24/30) −2.6
(24/32) −4.0
(2/4) −2,1
(56/62) −1.4
(24/30) −5.5
(32/32)

62
24
26
1
59
29
30

62.8
28.5
30.8
3.5
59.8
29.5
30.4

3.1
1.7
1.7
0.7
2.7
1.0
2.2

Language production

Repetition
Words
Complex words
Nonwords
Digit strings
Sentences
Naming
Objects
Actions
Word fluency
Reading
Words
Complex words
Function words
Nonwords
Writing
Copying
Picture naming
to Dictation

(32/61) −7.2
(16/32) −11.0
(6/6)
(2/10) −3.8
(4/7) −1.6
(4/6) −4.5
(24/58)
(18/48) −5.7
(6/10) −4.4
(22) −0.8
(66/70) −1.2
(44/48) −2.2
(6/6)
(6/6)
(10/10)
(60/82) −4.5
(28/31) −0.7
(10/23) −5.8
(22/28) −4.5

57
31
6
9
6
6

57.8
31.4
5.9
9.0
5.6
5.8
83.3
43.5
9.5
30.3
68.8
47.3
5.9
6.0
9.6
79.2
30.1
21.6
27.4

3.6
1.4
0.5
1.8
1.0
0.4
12.9
4.5
0.8
10.3
2.4
1.5
0.4
0.2
1.2
4.3
3.1
2.0
1.2

22

43
9
29
68
47
6
6
9
74
30
21
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2.3.2. Acquisition
Functional MRI was conducted five months poststroke on a 3T
Siemens scanner (TrioTim) equipped with a standard 32-channel head
coil. A BOLD sensitive T2∗-weighted single shot gradient recalled (GR)
echo planar imaging (EPI) sequence (TE/TR: 50/3000 ms; FA: 90°) was
used resulting in voxel dimensions of 3 × 3 × 3 mm3 (interleaved),
FOV = 1344 × 1344, matrix = 64 × 64. Functional images were acquired in the axial orientation.

Table 3
FWE-corrected p-values of the clusters and peaks, number of activated voxels, and MNI
coordinates of the activated clusters in the different comparisons.
Cluster
p(FWEcorr)

Peak
#voxels

EN > CTRL
0.005
84

2.3.3. Analysis
fMRI data were analyzed using SPM12 software (www.fil.ion.ucl.ac.
uk/spm). After motion and slice timing correction, the unwarped
functional images were registered to the T1 weighted anatomical data
set. The anatomical image was then segmented and the forward deformation field was used to normalize the functional images to MNI
(Montreal Neurological Institute) space. The registered functional data
were smoothed spatially with a Gaussian kernel with a full width at half
maximum (FWHM) of 6 × 6 × 6 mm3. Activations during the control
condition were subtracted from the activations during naming in the
three languages to assess language-specific activations (EN > CTRL;
FR > CTRL; DU > CTRL). A conjunction analysis of these three contrasts was performed to identify the common regions. In addition, differences between the languages were investigated by contrasting
French and Dutch with English (FR > EN; DU > EN). A conjunction
analysis of these two contrasts revealed the activations specific for L2
languages. The clusters specific for Dutch naming were identified by
masking the contrast DU > EN with the contrast FR > EN. Clusters with
a peak with an uncorrected p-value smaller than 0.001 and a minimal
cluster size of 20 voxels were detected. Only clusters with a family-wise
error (FWE)-corrected p-value ≤ 0.05 or with a cluster peak with an
FWE-corrected p-value ≤ 0.01 are reported. All clusters are listed in
Table 3.

0.399
0.052

22
49

FR > CTRL
0.000
2830

2.3.4. Results
2.3.4.1. English (L1) compared to control task. Silent naming of pictures
in the patient’s mother tongue (English, L1) activated three brain
regions. The strongest activation was found in the right frontal lobe,
including the middle and superior frontal gyrus. A smaller cluster was
detected in the contralateral left frontal homologue region. A third
cluster was marginally activated in the left postcentral gyrus, near
Wernicke’s area. These clusters are visualized in Fig. 3.

0.052

49

0.000

433

0.000

365

0.000

128

DU > CTRL
0.000
2488

2.3.4.2. French (L2) compared to control task. During French picture
naming (Fig. 4), a large bilateral frontal network was recruited
including the bilateral anterior insular regions, the middle and
superior frontal gyri, the left cingulate gyrus, and a small part of the
right superior temporal gyrus. Besides a large activation in the left
superior temporal gyrus, a smaller (and less activated) contralateral
right cluster was found in the homologue region. A right fronto-parietal
cluster was also observed including the cingulate gyrus. In addition, the
left posterior cerebellum (primarily lobule VI/VIIb) was activated.
2.3.4.3. Dutch (L7) compared to control task. Dutch picture naming
resulted in largely the same clusters of activation as in French picture
naming (Fig. 5). At the supratentorial level, a large bilateral frontal
network including the middle and superior frontal gyri was found as
well as activation of the insular regions and the left and right temporal
regions. No activation was found in the cingulate gyri. At the
infratentorial level bilateral activation of the right (primarily VIIa
Crus I-II) and left posterior cerebellum (primarily lobule VI/VIIb)
were found.
2.3.4.4. Regions common to all languages. The three regions activated
during English picture naming (the right and left middle and superior
frontal gyrus and the left postcentral gyrus) were common to naming in
all languages, but only the shared right frontal cluster reached

0.000

206

0.001

109

0.000

238

MNI coordinates {mm}

p(FWEcorr)

x

y

z

0.001
0.589
0.007
0.233
0.654

21
36
−60
−24
−33

51
51
−12
48
57

−9
−6
18
−3
3

R dorsolateral
prefrontal area
L postcentral gyrus
L dorsolateral
prefrontal area

0.000

18

51

−9

R dorsolateral
prefrontal area

0.000
0.000

24
−18

45
57

−6
3

0.001
0.000
0.001

−24
−30
−42

51
48
24

−6
−3
18

0.002

−24

12

45

0.000
0.000
0.000
0.001
0.000
0.001
0.003
0.000

33
21
30
−30
−36
−45
−42
60

0
6
15
0
3
0
6
−12

12
21
6
15
27
18
15
9

0.002
0.000
0.311
0.000
0.000
0.000
0.000
0.001
0.023
0.007
0.138
0.868

−15
60
66
−57
−57
−51
18
21
24
−18
−21
−12

−15
−30
−24
−15
−3
−27
−18
−30
−18
−78
−60
−69

39
3
12
3
0
12
39
36
21
−21
−12
−3

0.000

18

51

−9

0.000
0.000
0.028
0.000

12
−6
48
−21

63
63
−15
51

−6
0
27
−3

0.000
0.007
0.001
0.035
0.052
0.024

−30
−12
−18
−42
−36
−45

48
54
57
24
27
3

−3
−6
3
18
15
15

0.000

−54

−24

15

0.017
0.002
0.003
0.016
0.000
0.000
0.474
0.000
0.007
0.030
0.000
0.001
0.006

−57
21
−30
−21
−18
−36
−48
63
57
66
36
21
33

−3
3
0
−18
−78
−72
−63
−33
0
−24
−48
−42
−57

0
21
12
18
−21
−24
−21
3
0
12
−42
−39
−36

L dorsolateral
prefrontal area

L inferior frontal
gyrus
L middle frontal
gyrus
R insula
R insular region
L insula
L insular region

R superior
temporal gyrus
L cingulate gyrus
R superior
temporal gyrus
L superior
temporal gyrus
R cingulate gyrus

L posterior
cerebellum

R dorsolateral
prefrontal area

R precentral gyrus
L dorsolateral
prefrontal area

L inferior frontal
gyrus
L superior
temporal gyrus
R insular region
L insular region
L posterior
cerebellum
R superior
temporal gyrus
R posterior
cerebellum
(continued on next page)

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P. Mariën et al.

and a more anterior cluster involving primarily the right cerebellar
hemisphere), the left fusiform gyrus, the cingulate gyrus, and the
bilateral dorsolateral prefrontal regions were significantly stronger
activated compared to English (Fig. 7).

Table 3 (continued)
Cluster

Peak

MNI coordinates {mm}

p(FWEcorr)

#voxels

p(FWEcorr)

x

y

z

0.000

180

0.012
0.020
0.139

−45
−45
−33

−57
−66
−75

30
39
45

L angular gyrus

0.001
0.589
0.233
0.972
0.401

21
36
−24
−33
−60

51
51
48
57
−6

−9
−6
−3
6
−3

R dorsolateral
prefrontal area
L dorsolateral
prefrontal area
L superior
temporal gyrus

FR > EN AND DU > EN
0.000
413
0.012
0.082
0.029
0.002
104
0.017
0.144
0.993
0.007
79
0.028
0.991
0.002
104
0.048
0.048
0.393

−57
−45
−27
57
60
48
−42
−30
30
27
36

3
−9
−15
6
−12
−3
30
30
21
39
15

33
48
48
0
9
12
21
24
0
0
6

L precentral gyrus

DU > EN excluding FR > EN
0.000
348
0.000
0.001
0.002
0.000
1858
0.000

−18
−36
−48
−57

−78
−66
−54
−27

−21
−30
−24
15

L posterior
cerebellum

−63
−45
12
21
24
24
27
24
60
57
63
−3
6
−15
18
30
33
0
0
3

−33
−48
63
57
42
−45
−72
−57
−39
−24
−30
3
9
3
−21
−9
−21
0
12
24

24
51
−6
−6
−9
−39
−27
−33
15
12
9
66
66
66
15
12
12
30
27
21

COMMON
0.007
80
0.186

32

0.912

8

0.000

478

0.000

234

0.000

199

0.004

89

0.002

100

0.001

107

0.001
0.001
0.001
0.046
0.076
0.004
0.018
0.020
0.007
0.012
0.036
0.017
0.018
0.293
0.021
0.195
0.577
0.042
0.136
0.729

3. Discussion
Following a left cerebellar ischemic stroke this strongly righthanded multilingual patient acutely developed a transient mild ataxic
dysarthria and differential polyglot aphasia initially characterized by a
complete loss of all six non-native languages while his maternal language was only very mildly affected by word-finding diffifculties for
low-frequency words. Within the course of a few days, remission of
polyglot aphasia started to take place but apart from full recovery of the
mother tongue, all non-native languages remained affected to a different degree at the lexical and syntactic level. In addition, non-native
speech was characterized by the phenomenon of pathological language
mixing and switching and reversion to a previously learned accent
occurred as well (see Keulen et al., 2017).
To assess cerebral language lateralization, an fMRI visual confrontation naming study consisting of 40 high-frequency objects and
animals versus 40 simple meaningless line drawings was performed in
English (L1), French (L2) and Dutch (L7). Since aphasia still substantially affected lexical-semantic retrieval in German, Hebrew,
Serbian and Slovenian one month after stroke these languages could not
be reliably tested in the scanner. As evidenced by fMRI results, naming
in the maternal language (L1) was predominantly associated with left
hemisphere activations (left postcentral gyrus) and a bilaterally distributed dorsolateral prefrontal activation pattern (right more than
left). Naming in the non-native languages French (L2) and Dutch (L7)
recruited a significantly larger neuronal network consisting of extensive
bilateral frontal activations, left parieto-temporal activations extending
towards the temporal lobe and activation of the right temporal homologue. In addition, an activated cluster was found in the left posterior
cerebellum (lobule VI/VIIb) for L2 naming, and in the right cerebellum
(more anteriorly in the VIIa Crus I-II) for Dutch naming.
Current knowledge about the neural organization of the bilingual
brain seems to indicate that irrespectively of considerable diversity due
to age of L2 acquisition and level of L2 proficiency, native as well as
non-native languages are computed by a highly similar neural circuitry
located in the perisylvian cortical and subcortical regions of the language dominant hemisphere. Abutalebi and Green (2016) defined the
bilingual language network on the basis of a close functional interplay
between the dorsal anterior cingulate cortex/pre-SMA, the left prefrontal cortex, the left caudate nucleus, and the bilateral inferior parietal lobules, controlled by the right prefrontal cortex, the thalamus and
putamen, and the cerebellum. Within this neural network a possible
crucial role of the cerebellum seems to be gradually emerging (Filippi
et al., 2011; Pillai et al., 2004). Damage to the left posterior cerebellum
(involving VIIb Crus I/II, anatomically and functionally linked to the
right dorsolateral prefrontal area) resulting in the loss of all L2 languages might indicate an important role for the functional language
network subserved by crossed cerebellocerebral pathways between the
left cerebellum and the cortical association areas of the right dorsolateral prefrontal cortex (which was strongly implicated in picture
naming in all languages).
The constellation of anatomoclinical findings in this strongly righthanded multilingual patient deserves some further attention. Green and
Abutalebi (2008) have argued that non-parallel recovery, such as pathological mixing and switching, is usually the result of an impairment
of the language control network (Green & Abutalebi, 2008), supported
by domain-general executive mechanisms (Kong et al., 2014). As a result, it might be hypothesized that due to the damage in the left cerebellar hemisphere, the dorsolateral prefrontal areas, responsible for
inhibiting and selecting the correct responses, were functionally disrupted through cerebellocerebral diaschisis. The ability to inhibit the

R superior
temporal gyrus
L middle frontal
gyrus
R insular region

L superior
temporal gyrus
L inferior parietal
lobe
R dorsolateral
prefrontal area
R posterior
cerebellum
R superior
temporal gyrus
L (pre-)SMA
R (pre-)SMA
R thalamus
R putamen
R insula
Cingulate gyrus

Legend: R = Right; L = Left; EN = naming in English; FR = naming in French;
DU = naming in Dutch; CTRL = Visual control task; mm = millimeters; FWEcorr = Family-Wise Error corrected; MNI = Montreal Neurological Institute;
SMA = Supplementary Motor Area.

significance.
2.3.4.5. Dutch (L7) and French (L2) compared to English (L1). Regions
that were more activated in the languages learned at a later age (Dutch
and French) than the native language (English) were primarily situated
in the left and right fronto-temporal areas (Fig. 6). In the left
hemisphere, a large cluster in the precentral gyrus in the vicinity of
the insular region and a more anterior region in the middle frontal
gyrus were actively recruited, while in the right hemisphere a frontotemporal region in the rolandic operculum was activated together with
the insula. During Dutch naming, however, the areas that were stronger
activated than during English naming were more diffuse and
widespread. In addition to larger activation of left and right frontotemporal areas, both cerebellar hemispheres (left posterior cerebellum,
24

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Fig. 3. fMRI visual confrontation naming (p = 0.0001).
fMRI of visual confrontation naming in English (L1) versus a
visual control task shows strongest activation in the right
frontal lobe (A), including the middle and superior frontal
gyrus. In addition to a region of activation in the left postcentral gyrus (C) a much smaller cluster is found in the
contralateral left frontal homologue region (not visualized).
Legend: R = right; L = left; A = anterior; P = posterior.

Fig. 4. fMRI of visual confrontation naming (p = 0.0001) in French (L2) versus a visual control task recruited the bilateral dorsolateral prefrontal areas (right: A, left: B), and the
cingulate gyri (right: E, left: F). Besides a large activation in the left superior temporal gyrus including the insular regions (C), a smaller contralateral right cluster was found in the
homologue region (K). In addition, the left posterior cerebellum (D) was activated, and the left (I) and right (J) basal ganglia. Legend: R = right; L = left; A = anterior; P = posterior.

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Brain and Language 175 (2017) 18–28

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Fig. 5. fMRI of visual confrontation naming (p = 0.0001) in Dutch (L7) versus a visual control task disclosed activation of the bilateral dorsolateral prefrontal areas (right: A, left: B), and
the left and right temporal regions including the anterior insula (right: K, left: C). Activations in the right (H) and left posterior cerebellum (D), and in the basal ganglia (right: J, left: I)
were found as well. Legend: R = right; L = left; A = anterior; P = posterior.

test).
Functional MRI revealed that naming in French and Dutch, languages learned at a later age, relied heavily on an extensive control
network primarily involving the bilateral dorsolateral prefrontal areas,
and the insular regions/basal ganglia. A number of studies has shown
that left dorsolateral prefrontal/inferior frontal gyrus activity may be
related to response selection and right dorsolateral prefrontal/inferior
frontal gyrus activity to response inhibition (Abutalebi & Green, 2016;

stronger L1 was impaired, causing a temporary loss of all non-native
languages. This might explain why the two most used non-native languages (French and Dutch) recovered faster, and why pathological
language mixing and switching persisted when using the other nonnative languages. Selective disruption of the executive mechanisms was
also apparent at the non-linguistic level. Neurocognitive investigations
revealed no abnormalities except for a severely impaired ability to inhibit competing and more automatic responses (Stroop color-word

Fig. 6. Conjunction analysis of visual confrontation naming in Dutch (L7) and French (L2) versus visual confrontation naming in English (L1). Regions more activated in L7 and L2 than in
L1 included the left and right fronto-temporal areas. In the left hemisphere, a large cluster in the precentral gyrus in the vicinity of the insular region (B) and a more anterior region in the
middle frontal gyrus (A) were actively recruited, while in the right hemisphere a fronto-temporal region in the rolandic operculum (C) was activated together with the anterior insula (D).
Legend: R = right; L = left; A = anterior; P = posterior.

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Fig. 7. fMRI of visual confrontation naming in Dutch (L7) versus visual confrontation naming in English (L1) after subtracting the activated areas in French (L2) (see Fig. 6). The areas
that were stronger activated in L7 than in L1 (and L2) were more diffusely distributed and widespread. In addition to larger activation of left and right fronto-temporal areas including the
insula (right: K, left: C) and a cluster in the left inferior parietal lobule (M), both cerebellar hemispheres (left posterior cerebellum extending into the fusiform gyrus (D), right posterior
and anterior cerebellum (H)), and the bilateral dorsolateral prefrontal regions (AB) were significantly stronger activated in L7 compared to L1/L2. Legend: R = right; L = left;
A = anterior; P = posterior.

Acknowledgments

Aron, Behrens, Smith, Frank, & Poldrack, 2007). Of note, we report
activity of the cingular cortex only during naming of the second languages (as observed in the contrast second languages > L1) and we
suggest that this may be due to increased monitoring demands for those
languages in which the patient struggles. Conflict monitoring and error
detection are two well known cognitive processes ascribed to the cingular cortex and these processes are key for correct language output in
multilinguals. On the other hand, and interestingly, only one area
seemed to “work more efficiently” (in terms of functional brain activity
for L1), i.e., the right prefrontal cortex. This area is linked to response
inhibition (Abutalebi & Green, 2016; Aron et al., 2007) and, indeed,
during L1 production, the patient never had intrusions from the other
languages. Pathological switching was more common when speaking
the second languages but not when speaking in L1 underlining that
response inhibition was impaired specifically for the second languages.
In other words, the left cerebellar lesion led to a functional deactivation
of the right prefrontal cortex only for the later acquired languages,
which may be less resistant to brain damage. The observed activation
during Dutch picture naming of the right cerebellar Crus I and II, known
to be functionally and anatomically connected to the prefrontal areas
involved in executive control and language (Stoodley & Schmahmann,
2009), might reflect in our patient a compensatory mechanism for the
damaged left cerebellar hemisphere to regain the proficiency of a language learned as a late bilingual through response selection by the left
prefrontal area. These results indicate that not only the right cerebellum
is involved in the language control system, but that the left cerebellum
might also be implicated.

We are grateful to Johanna Van Dormael for setting up the fMRI
naming tasks in the different languages, to Wim Van Hecke for performing the fMRI experiment, and to Jubin Abutalebi for lending his
expertise in this case study.Statement of significance
This case study of a right-handed patient with differential polyglot
aphasia for the first time demonstrates a crucial role of the left cerebellum in multilingual language processing. Cerebellar induced disruption of the control network subserving multilingual language processing may induce devastating linguistic distortions.
Conflict of interest
The authors declare that they have no conflict of interest to declare.
Funding
This study was supported by a research grant of the Fund for
Scientific Research-Flanders (G035714N) and by a Strategic Research
Program (SPR15) awarded by the Vrije Universiteit Brussel, Belgium.
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