Journal of Neurology

https://doi.org/10.1007/s00415-019-09616-2

ORIGINAL COMMUNICATION

Striking loss of second language in bilingual patients with semantic

dementia
Ratnavalli Ellajosyula1,2 · Jwala Narayanan1,3 · Karalyn Patterson4

Received: 30 July 2019 / Revised: 1 November 2019 / Accepted: 2 November 2019

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Abstract
Background Studies of bilingual or multilingual patients with neurodegenerative diseases that disrupt language like the
primary progressive aphasias (PPA) may contribute valuable information on language organization in the bilingual brain and
on the factors affecting language decline. There is limited literature on bilingual PPA and in particular on semantic dementia,
a type of PPA with selective loss of semantic memory. We studied the nature and severity of naming and comprehension
deficits across languages in bilingual patients with semantic dementia (SD).
Methods Sixteen bilingual patients with SD and 34 bilingual age-matched controls were administered the modified Boston
Naming Test and components of Cambridge Semantic Battery. The patients’ performance on picture naming and word
comprehension was compared across languages and with controls. The most proficient language on self-rating was labelled
as L1 and less proficient as L2.
Results We observed striking loss of second language (L2) in SD for both receptive and expressive language, even in patients
who were premorbidly fluent in their L2. Naming and comprehension in every patient’s L2 were impaired relative to both
their own first-language (L1) scores and controls’ L2 scores. Furthermore, item-specific correct responses in each patient’s
L2 were a subset of their successes in L1.
Discussion A striking contrast in performance between two languages in bilingual patients with SD indicates that a bilin-
gual’s L2 or less proficient language is more vulnerable to neurodegeneration. Our findings also support a common semantic
network in the brain for the different languages of bilinguals.

Keywords Primary progressive aphasia · Semantic dementia · Bilingualism · Naming · Word comprehension

Background

More than half the world’s population is bilingual, and the

proportion of bilingual aphasic patients evaluated in clini-
Electronic supplementary material The online version of this cal practice is rapidly increasing [1, 2]. There are two main
article (https​://doi.org/10.1007/s0041​5-019-09616​-2) contains issues central to bilingual aphasia of interest to researchers
supplementary material, which is available to authorized users. across diverse disciplines: (1) the patterns of impairment,
and factors influencing recovery or decline, in the two lan-
* Ratnavalli Ellajosyula
ratnavallie@gmail.com guages; and (2) the nature of the representations and pro-
cessing of language in bilinguals. Study of primary progres-
1
Department of Neurology, Manipal Hospital, sive aphasias (PPAs) with slow decline in language due to
Bangalore 560017, India focal neurodegeneration may be especially revealing about
2
Department of Neurology, Annasawmy Mudaliar Hospital, these issues [3, 4]. PPAs have been classified into three vari-
Bangalore, India ants, semantic, nonfluent/agrammatic, and logopenic, each
3
Department of Neuropsychology, Annasawmy Mudaliar associated with a distinct pattern of brain atrophy [5, 6].
Hospital, Bangalore, India Semantic variant PPA, more commonly called semantic
4
Department of Clinical Neurosciences and MRC Cognition dementia (SD), which is probably the best-understood vari-
and Brain Sciences Unit, University of Cambridge, ant, is characterized by profound deterioration of semantic
Cambridge, UK

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knowledge [7–10]. The three PPA variants appear to be
important lesion models for understanding semantic mem-
ory, speech fluency and syntax and phonological working
memory. An important question to be answered is how neu-
rodegeneration affects these different linguistic capacities in
each language spoken by a bi- or multilingual patient. Con-
trasting performance in two languages might be informative
in the evaluation of PPA, as well as of theoretical interest for
cognitive neuroscience and linguistics.
In spite of increasingly common presentations of bilin-
gual aphasia in the clinic, there are a limited number of
research studies on PPA in bilinguals [11–21]. One describes
two multilingual patients with SD, with relative preservation
of first language and substantial loss of the later-learned lan-
guages [11]. In both patients, words comprehended in one
language were not consistently named or comprehended in
the other languages they knew, leading the authors to pro-
pose separate lexical-semantic systems for the different
languages. Another brief report mentions loss of both first
and second languages in a multilingual Taiwanese woman
with SD [12]. In the largest study on clinical features, soci-
odemographics and biomarkers of bilingual PPA published
to date, Costa et al. [21] combined 13 cases culled from a
literature search with 20 new cases. Formal language assess-
ment was done in only 45% of patients. In addition to the
above-mentioned papers, they added two more SD patients.
Despite the expected heterogeneity both between and within
subtypes, the authors reported largely parallel patterns of
impairment in the patients’ two languages across all sam-
ples. The study had several limitations as pointed out by the
authors, including its retrospective nature, limited sample
size, heterogeneity of assessment tools and incomplete lin-
guistic data. A recent review chapter attempted to analyse
the published cases of bilingual PPA and concluded that
the language decline was either (a) parallel in L1 and L2 or
(b) differential with L2 more impaired [22]. There was no
patient where L1 was more affected. The authors concluded
that the order of acquisition of languages was a much more
important factor than either proficiency in or age of acquisi-
tion of a patient’s two languages.
India is an ideal setting to study bilingual aphasia as it
is home to 234 dialects and 122 languages, of which 22 are
officially recognized [23]. Around 25% of the population
is bilingual, which amounts to roughly 250 million people.
Currently, we are investigating language profiles of bilin-
gual patients with mild cognitive impairment, Alzheimer’s
disease, PPA and frontotemporal dementia in our memory
clinic [24]. Here, we report our first set of findings in bilin-
gual patients with SD. The aim of the study was to examine
the nature and severity of impairment across different lan-
guages in bilingual (multilingual) SD patients. The other
objective was to compare performance across each patient’s
languages at the item-specific level on the same tests. Such
13
Journal of Neurology
results may inform one of the central questions in this
research topic: to what extent are the processes underlying
a language skill such as object naming or word comprehen-
sion shared or independent across the different languages of
a bilingual individual?
Methods
Patients
Patients presenting with PPA attending the Cognitive Neu-
rology Clinic, Manipal Hospital, Bangalore, India over a
5-year period were identified. Of the 20 patients diagnosed
with SD, 4 were excluded because 2 were monolinguals and
2 were too impaired to complete the tests. A total of 16
patients, 6 women and 10 men, formed the sample of the
study (Table 1). The mean age at diagnosis was 65.5 (8.2)
years and at reported onset was 62.9 (8.8) years. All patients
or their caregivers gave informed consent to participate in
the study, according to the Declaration of Helsinki, which
was approved by the hospital ethics committee.
The diagnosis of SD was based on criteria for semantic
variant PPA [6]. All the patients were living at home with
family, and detailed history was taken from two reliable
caregivers (spouse and a son or daughter) as well as the
patient. A comprehensive neurological examination, neu-
ropsychological testing and neuroimaging were performed.
Magnetic resonance imaging (MRI) scans at presentation
showed moderate atrophy of bilateral temporal lobes, espe-
cially anterior and medial, more prominent on the left side
in 13 and on the right in 3 patients.
Language details
A questionnaire was used to collect information from the
patient and the caregivers regarding languages spoken, read
and written, age of acquisition, proficiency and medium of
education. Premorbid proficiency for speaking was assessed
on a scale of 0–7 (7 being most proficient) using self-ratings.
Seven patients could do a self-rating but nine patients had
poor comprehension, so the caregivers’ ratings were used in
these cases. The most proficient language for speaking was
referred to as L1, which was the same as the mother tongue
in 14/16 patients. If two languages were rated equal, the
preferred language was considered as L1. Six patients were
bilinguals and 10 multilinguals, three of whom spoke four
languages premorbidly (Table 2). Thirteen patients could
read and write in L2 as well. Seven patients received their
bilingual exposure before 5 years (early bilinguals). Most
frequent languages were Kannada as L1 in seven and Eng-
lish as L2 in eight patients. Two patients spoke dialects (L1)
Bhojpuri and Tulu, which have no written form. English was
Journal of Neurology

Table 1  Patient characteristics and performance on the Addenbrooke’s Cognitive Examination-Revised (ACE-R) and the language subcompo-
nent of the ACE-R, with patients ordered from least to most impaired on total ACE-R
Patient Gender Education Occupation Age at diag- Reported age at Estimated dura- ACE-R (100) ACE-R-
(years) nosis (years) onset (years) tion (months) language
(26)

Patient 1 Male 15 Head clerk 60 58 24 78* 24

Patient 2 Male 12 Business 59 56 36 65 17
Patient 3 Male 16 Business 61 60 8 65 8
Patient 4 Male 12 Government employee 64 63 12 61 14
Patient 5 Male 17 Real estate business 73 68 60 52 20
Patient 6 Male 17 Advocate 58 55 36 50 9
Patient 7 Female 13 Teacher 69 67 24 40 12
Patient 8 Female 15 Housewife 76 74 24 36 8
Patient 9 Male 20 Professor of Engineering 61 58 36 33* 11
Patient 10 Male 14 Business (Civil Engineer) 70 68 24 32 17
Patient 11 Female 17 Civil servant 66 65 8 30 5
Patient 12 Male 17 Director in Government 88 87 12 27 13
Patient 13 Female 12 Housewife 57 53 48 16 0
Patient 14 Male 13 Ayurvedic physician 66 63 36 16 0
Patient 15 Female 0 Housewife 62 57 60 NP –
Patient 16 Female 3 Housewife 58 54 48 NP –

*ACE scores in L2 NP—not possible

learnt formally in school in all the patients who could speak
English (L2 or L3); it is also the language of instruction in
college and university. Six patients had equal proficiency rat-
ings of 7 in both L1 and L2. Before the onset of symptoms,
all the patients were using L2 every day, either socially (9)
or at work (6) or both (1) and eight patients were still work-
ing. For instance, patient 9 was teaching in English at an
Engineering college at the onset of symptoms.
Assessment
Cognitive assessment
The Addenbrooke’s Cognitive Examination-Revised (ACE-
R) [25] which has been adapted and widely used in an Indian
population [26] was used as a global screen of cognitive
function.
Language assessment
Modified Boston Naming Test (mBNT) A 30-item nam-
ing test similar to the Boston Naming Test (BNT) was
developed from an Indian version of the Snodgrass and
Vanderwart pictures [27] and their names, with high- and
low- frequency object names across three Indian languages
(Kannada, Hindi and Tamil) and English. The pictures con-
sisted of colour photographs of objects. The modified test
was administered in a healthy elderly population.
Cambridge Semantic Battery (CSB) Picture naming and
word-to-picture matching subcomponents of the Cam-
bridge Semantic Battery (CSB) [28] were administered
to evaluate semantic memory across different languages.
Each test used the same 64 items, with 8 stimuli in each
of 8 categories: 4 groups of living things or natural kinds
(domestic animals, wild animals, birds, and fruits) and 4
of manmade objects or artefacts (large household items,
small household items, tools and vehicles).
Naming test The patient is asked to name a line drawing
of each of the 64 items. The stimuli were presented in a
random order. Maximum score is 64.
Word-to-picture matching Patients are presented with
64 picture arrays, one for each item, with each array con-
sisting of a target picture and 9 other pictures from the
same category. They are asked to point to the target picture
named by the examiner. Maximum score is 64.
The language assessment was done over two different
sessions. The tests were first administered in the patient’s
L1, followed by neuropsychological tests to reduce con-
founding factors including test repetition. Then, the lan-
guage tests in L2 and L3 were administered. The interval
between the assessments was usually 3–7 days. Language
subcomponents and abilities were also assessed informally
as part of the cognitive examination by the neurologist.

13
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Table 2  Language details of patients
Patient Number of Mother tongue L1—self-rating L2—self-rating L3 and L4—self- Read and write Reads newspapers Type of Proficiency-bal- Method of
languages for proficiency for proficiency rating for profi- bilingual anced or dominant acquisition
spoken (estimated AOA) (estimated AOA) ciency (estimated (AOA) (comments) of L2
AOA)

Patient 1 2 Bhojpuri Bhojpuri—7 Hindi—7 (4) – L2 L2 Early Balanced Informal

Patient 2 2 Tulu Tulu—7 Kannada—7 (3) – L2 L2 Early Balanced Informal
Patient 3 3 Telugu Telugu—7 English—6 (16) Hindi—4 (30) L1, L2, L3 L1, L2 Late Dominant L1 College
Patient 4 2 Kannada Kannada—7 English—4 (12) – L1, L2 L1 Late Dominant L1 School
Patient 5 3 Kannada Kannada—7 English—5 (15) Hindi—5 (20) L1, L2, L3 L2 Late Dominant L1 College
Patient 6 3 Kannada Kannada—7 English—5 (10) Hindi—4 (12) L1, L2 L2 Late Dominant L1 School
Patient 7 2 Bengali Bengali—7 Hindi—2 (15) – Reads—L1, L2 L1 Late Dominant L1 College
Writes—L1 (but teaches Hindi
in school)
Patient 8 3 Tamil Kannada—7 (4) Tamil—7 (0) English—5 (7) L1, L2, L3 L3 Early Balanced Informal
Patient 9 3 Oriya Oriya—7 English—6 (6) Hindi—6 (4) L1, L2, L3 L2 Late Dominant L1 School
(teaching in
English at an
Engineering
college)
Patient 10 3 Kannada Kannada—7 English—6 (7) Tulu—6 (25) L1, L2 L2 Late Balanced School
Patient 11 4 Marathi Marathi—7 Kannada—7 (4) English—6 (7) L1, L2, L3, L4 L3 Early Balanced Informal
Hindi—5 (10)
Patient 12 4 Tamil Hindi—7 (9) English—6 (4) Tamil—5 (0) L1, L2, L3, L4 L1, L2 Early Balanced School
Kannada—5(4)
Patient 13 3 Kannada Kannada—7 English—4 (6) Hindi—4 (8) L1, L2 L2 Late Dominant L1 School
Patient 14 4 Kannada Kannada—7 Marathi—7 (4) English—7 (6) L1, L2, L3, L4 L2, L3 Early Balanced Informal
Hindi—7 (8)
Patient 15 2 Telugu Telugu—7 Kannada—7 (4) – No – Early Balanced Informal
Patient 16 2 Telugu Telugu—7 Kannada—6 (7) – No – Late Dominant L1 Informal

L1 most proficient language, L2 second most proficient language, L3 third most proficient language, L4 fourth most proficient language, AOA age of acquisition
Journal of Neurology
Journal of Neurology
Controls
34 bilingual healthy controls with a mean age of 65.5 (6.4)
years underwent a clinical interview, the ACE-R, mBNT
naming and the CSB naming and word comprehension tests.
The CSB and mBNT were administered in L1 and L2. Of
the 34 controls, it was possible to match 10 to an individual
patient for age, sex, same L1 and L2 and even similar profi-
ciency ratings in L1 and L2. Details of language background
and performance on tests are provided in Supplementary
Table 1.
Independent T tests were carried out comparing patients
and the whole control group across age, education and lan-
guage proficiency ratings in L1 and L2. No significant dif-
ferences were found between the groups on age (48, t = 0.46,
p = 0.79, Hedges’ g = 0.02), education (48, t = 0.28, p = 0.78,
Hedges’ g = 0.09), or language proficiency rating in L2 (48,
t = 1.2, p = 0.22, Hedges’ g = 0.38). Language proficiency
ratings in L1 were identical.
The Wilcoxon Signed Rank Test comparing patients and
matched controls indicated no significant difference across
age (Z = 1.83, p = 0.07), education (Z = 0.71, p = 0.48) or lan-
guage proficiency ratings in L2 (Z = 0.45, p = 0.66).
Results
Qualitative observations
Relatives commonly reported the patients’ impoverished
ability to converse in L2 or L3, in which they were previ-
ously fluent. All patients except two had reverted to use of
L1 both at home and in social situations. Patients with Eng-
lish as L2 could no longer read the English newspaper. Eight
patients could speak a few words or phrases in L2 but speech
was quite impoverished and they were unable to name most
objects in L2 on bedside testing. Eight patients could not
understand even simple instructions in L2 and were unable
to speak a single sentence in the L2 in which they were pre-
viously fluent. In the examiner’s assessment, of the patients
who had spoken three or more languages premorbidly, five
demonstrated a similar extent of impaired ability to under-
stand spoken L2 and L3, while in five patients, L2 was better
than L3 (patients 3, 5, 8, 9 and 12).
When spoken to in Kannada (L2), patient 16 responded,
“I don’t understand English”. She was unable to differentiate
between the languages when asked to say which language
she herself was using; in fact, failure to differentiate between
the languages was striking in five patients (patients 8, 11,
12, 14 and 16). Patient 12 frequently mixed Hindi and Eng-
lish while speaking. Patient 8 tended to use both Kannada
(preferred language) and Tamil (mother tongue) but mixed
the two languages while speaking, both at home and during
testing.
Performance on tests
Controls
As demonstrated in Supplementary Table 1 and Fig. 1a,
b, the performance of the control participants on the two
naming tests revealed a very small and not entirely consist-
ent advantage for L1. In 80% of the control comparisons
between L1 and L2 naming (the two naming tests com-
bined), naming scores for L1 vs. L2 were either equal or
differed by only 1 or 2 points, with some actually a point
or two higher in L2. This is a crucial finding: if language
performance was found to be significantly better in L1 than
L2 in healthy participants, such a finding in the SD patients
could not be unambiguously interpreted as an effect of the
brain disease.
Patients
Most patients performed poorly on the ACE-R, only four
scoring above 60/100 (Table 1), establishing that the group
has more advanced disease than the reported duration of
illness would suggest.
Table 3 and Fig. 1a, b present the number and percent
correct for the patients who managed to complete either
the mBNT or the CSB naming tests, or both of these. With
the sole exception of patient 1 for CSB naming in his L1,
the naming scores were low, even in the patients’ L1s. Four
patients who were able to attempt these tests in their L3
had scores at floor, and these results will not be considered
further. Some of the patients would often respond in their L1
even when the test was being administered in L2.
In cases where naming performance was severely
degraded in L1, it is obviously not meaningful to assess the
L1–L2 discrepancy. Consider, therefore, the 12 instances
where a patient’s naming score in L1 was ≥ 20% correct on
either the BNT or the CSB (Table 3). The average naming
score for L1 in these 12 instances was 41%. The correspond-
ing average for the same patients on the same tests in L2 was
13%. This is a striking result, because all these patients were
proficient bilinguals premorbidly (7/9 had 6 or 7 proficiency
ratings for L2). Furthermore, eight of them could previously
read and write L2 and one could read and write only in L2.
The same striking L1 > L2 percent correct contrast was
observed in the test of single-word comprehension (forced-
choice word-to-picture matching): for the seven patients with
performance ≥ 20% in their L1, the average percentage cor-
rect in L1 = 60% and in L2 = 17%. This is a very important
result to highlight, because it establishes that the L1 > L2
discrepancy is not confined to expressive language but also
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 Journal of Neurology

Fig. 1  a Naming (percent cor- A 100

rect) performance in individual L1 L2
90
patients, semantic dementia
(SD) patient group, whole 80
group controls (WGC) and 70

Percent Correct
matched controls (MC) across 60
most proficient language (L1)
and second most proficient 50
language (L2) on the modified 40
Boston Naming Test (mBNT). 30
b Naming (percent correct) per-
formance in individual patients, 20
semantic dementia (SD) patient 10
group, whole group controls 0
(WGC) and matched controls Pt 8 Pt 11 Pt 12
SD MC WGC
Pt 2 Pt 3 Pt 5 Pt 9 Pt 15
(MC) across most proficient Mean
language (L1) and second most
proficient language (L2) on the L1 L2
Cambridge Semantic Battery B 100
(CSB). Pt patient 90
80
70
Percent Correct

60
50
40
30
20
10
0
Pt 1 Pt 3 Pt 4 Pt 5 Pt 6 Pt 8 Pt 9 Pt 10 Pt 12 SD MC WGC
Mean

applies to receptive language/comprehension. Patients like
these who are towards the more impaired end of SD progres-
sion are, predictably, profoundly anomic even in their L1.
In some sense, therefore, the large L1 > L2 discrepancy on
word-picture matching, which is a less challenging receptive
test of language, is even more informative and striking than
the difference in naming.
On the comparison of item-specific naming performance
across languages, there was only one instance of a correct
response in L2 when that patient did not correctly name
the corresponding item in L1. Patient 9 named crocodile
correctly in English but not in Oriya (L1). That is, with the
exception of one item for one patient, L2 correct naming
responses were a proper subset of L1 correct responses.
At the level of item-specific responses in word-to-picture
matching, when patients’ levels of success in L1 were above
chance (the only situation in which it makes sense to do this
comparison), no patient ever chose the correct picture for the
spoken name in L2 without a corresponding correct response
to the same item in L1; in other words, L2 correct choices
were a fully proper subset of L1 correct choices.
Patients were tested informally on reading and writing.
Eight of the sixteen patients still retained some ability to
read and write in L2, but reading errors were prominent
(including surface dyslexia in English). Although sponta-
neous writing was not possible in all the patients, they did
write words and sentences to dictation but with errors (mis-
spellings, missing words).
Whole‑group statistical analyses
Independent T tests compared performance of patients and
controls across L1 and L2 on mBNT, CSB naming and CSB
word-to-picture matching (Table 4). The patients’ perfor-
mance was significantly lower than controls across L1 (with
medium effect sizes) and L2 on mBNT, CSB naming and
CSB word-picture matching (with medium to large effect
sizes).
Matched control statistical analyses
Wilcoxon Signed Rank Tests indicated that the median test
ranks across BNT naming, CSB naming and CSB word-
to-picture matching were significantly different between
patients and their matched controls for L1 and L2 (Table 4).
Each participant’s performance across L1 and L2 was also
analysed separately for SD patients and the control group.
Wilcoxon Signed Rank Tests indicated that the median test

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Journal of Neurology

Table 3  Performance of patients in most proficient language (L1) versus second most proficient language (L2) on naming (both modified Boston
Naming Test—mBNT and Cambridge Semantic battery—CSB) and word-to-picture matching—CSB: number (and percent) correct
Patient Naming (mBNT)—N = 30 Naming (CSB)—N = 64 Word-to-picture matching (CSB)—
Correct responses (percentage) Correct responses (percentage) N = 64
Correct responses (percentage)
L1 L2 L1 L2 L1 L2

Patient 1 NA NA 53 (83) 30 (47) NA 41 (64)

Patient 2 5 (17) 2 (7) NA NA NA NA
Patient 3 9 (30) 0 (0) 31 (48) 2 (3) 46 (72) 19 (30)
Patient 4 NA NA 21 (33) 0 (0) 41 (64) 19 (30)
Patient 5 15(50) 6 (20) 31(48) 13 (20) 49 (77) 20 (31)
Patient 6 NA NA 6 (9) 0 (0) 22 (34) 0 (0)
Patient 7 0 (0) 0 (0) 0 (0) 0 (0) 29 (45) 0 (0)
Patient 8 2 (7) 0 (0) 5 (8) 1 (2) 10 (16) 9 (14)
Patient 9 18 (60) 10 (33) 25 (39) 14 (22) NA NA
Patient 10 NA NA 15 (23) 0 (0) 36 (56) 0 (0)
Patient 11 7 (23) 1 (3) NA NA NA NA
Patient 12 3 (10) 1 (3) 13 (20) 5 (8) 45 (70) 20 (31)
Patient 13 0 (0) 0 (0) 0 (0) 0 (0) NA NA
Patient 14 0 (0) 0 (0) 0 (0) 0 (0) NA NA
Patient 15 13 (43) 0 (0) NA NA NA NA
Patient 16 1 (3) 0 (0) NA NA NA NA
Mean [SD] (%) for 6.08 [6.35] (20%) 1.67 [3.14] (6%) 16.67 [16.29] (26%) 5.41 [9.3] (9%) 34.75 [13.5] (54%) 10.88 [9.69] (17%)
all patients, even
when score is 0
Mean [SD] (%) 12.4 [4.4] (41%) 3.4 [4.4] (11%) 27 [13.5] (42%) 9.1 [10.9] (14%) 38.3 [9.9] (60%) 11.1 [10.4] (17%)
for patients
whose scores in
L1 ≥ 20%

NA not administered

Table 4  Comparison of performance of semantic dementia (SD) matching—CSB in most proficient language (L1) and second most
patients and controls on naming (both modified Boston naming test— proficient language (L2)
mBNT and Cambridge semantic battery-CSB) and word-picture
Matched controls Whole group controls
Mean (s.d.) Median WSRT p value Mean (s.d.) t p value ES
Z

mBNT L1 SD 7 (5.68) 7 2.37 0.02 8 (6.22) 15.48 0.00 5.81

mBNT L1 controls 25.3 (4.27) 25.5 27.68 (2.21)
CSB Naming L1 SD 15.25 (11.69) 14 2.52 0.01 20.5 (15.36) 12.16 0.00 4.38
CSB Naming L1 controls 52.4 (5.74) 53 59.24 (5.82)
CSB word-to-picture matching L1 SD 34.75 (13.54) 38.5 2.52 0.01 34.13 (14.89) 12.19 0.00 4.79
CSB word-to-picture matching L1 controls 62.5 (2.46) 64 63.21 (1.96)
mBNT L2 SD 1.14 (2.19) 0 2.38 0.02 2.22 (3.49) 21.2 0.00 7.96
mBNT L2 controls 24.1 (4.79) 24.5 26.65 (2.96)
CSB Naming L2 SD 2.62 (4.53) 0.5 2.52 0.01 7.3 (9.67) 19.41 0.00 6.98
CSB Naming L2 controls 48.4 (5.3) 46.5 57.15 (6.37)
CSB word-to-picture matching L2 SD 10.88 (9.69) 14 2.53 0.01 9.88 (10.3) 28.96 0.00 11.39
CSB word-to-picture matching L2 controls 61.1 (2.47) 61 62.44 (2.23)

WSRT Wilcoxon signed rank test, ES effect size (Hedges’ g)

13

ranks across mBNT naming (Z = 2.53, p = 0.01), CSB match-
ing (Z = 2.53, p = 0.01), CSB naming (Z = 2.67, p = 0.01)
were significantly lower in L2 as compared to L1 in the SD
patient group. In contrast, the median test ranks between L1
and L2 on mBNT naming (Z = 1.45, p = 0.15), CSB match-
ing (Z = 1.71, p = 0.09), CSB naming (Z = 1.59, p = 0.11)
showed no significant differences in the control group.
Discussion
This study of word production and comprehension across
different languages in a fairly large case series of bilingual
patients with SD yielded results that address two major
issues. First, despite a large literature on the cognitive and
clinical features of SD, very little has previously been docu-
mented on the fate of language abilities in the different lan-
guages of bilingual individuals with SD. Second is a more
general question about the neural networks for word compre-
hension and production in bilingual individuals.
Although all patients were impaired in both production
(picture naming) and comprehension (spoken word-to-
picture matching) in their L1, their corresponding levels of
success in L2 (and L3 where available) were dramatically
worse. The performance was significantly different from
controls especially for L2. Even at presentation, many of
the patients had essentially lost the ability to converse in L2
or L3. Strikingly, some even failed to identify the language
in which the examiner or they themselves were speaking.
Severely deteriorated performance in L2 and L3 was seen
in early and late bilinguals, in the two illiterate and all the
remaining literate patients, and in the equally proficient as
well as the less proficient bilinguals. In addition, the phe-
nomenon was seen whether L2 was similar to L1 (e.g.,
Bhojpuri and Hindi are both Indo-Aryan languages; Telugu
and Kannada are both Dravidian languages) or distinctively
different (Kannada and English). When it is remembered
that, premorbidly, all of these individuals spoke their L2
daily, could read and write in L2 (13/16) and read newspa-
pers only in L2 or L3 (10/16), these results are very notable
indeed. Two patients who spoke dialect at home but were
using L2 for speaking socially and for reading and writing
also showed the striking loss. A point worth emphasizing is
the ubiquitous loss or impairment of L2 in spite of the het-
erogeneity of the patient sample in terms of disease severity,
years of education, variety of languages spoken (8 as L1 and
5 as L2) and premorbid proficiency in L1/L2.
These prominent findings were easily demonstrable in
the clinic while eliciting history or on naming of common
objects in L2. Of course, our findings need to be replicated
across other bilingual populations from other countries
but, in our experience, this phenomenon does not occur
in patients with other PPAs, Alzheimer’s disease or the
13
Journal of Neurology
behavioural variant of frontotemporal dementia, all of which
we are currently investigating.
Evidence from a number of recent studies suggests that
semantic knowledge/processing for the different languages
of multilingual individuals is subserved by a common net-
work in the brain [29, 30]. In healthy bilingual participants,
the results of several functional imaging studies strongly
support the view (a) that semantic representations are shared
between an individual’s L1 and L2, and (b) that the most
significant shared neural activation is observed in the left
anterior temporal lobe which is, notably, the most consistent
area of atrophy in SD [31, 32]. This same region was also the
source of differential functional MRI activation for semantic
versus phonemic fluency in both languages of a large set of
healthy bilinguals [33].
The item-wise correspondence of results between L1 and
L2 in both naming and comprehension in our study seems
fully compatible with the proposal that, when a bilingual
person sees an object or picture of it, there is only one con-
ceptual representation for that object which sends activation
to the name in either L1 or L2 (or both). Our interpretation is
that, as the semantic system deteriorates in SD, the stronger
premorbid connections between L1 language representa-
tions (for both input and output) and language-independent
semantic representations will be more resistant than L2 to
this deterioration [34]. Of course our data only support this
claim for the concrete concepts studied here (objects and
animals). Abstract words—even within one language—tend
to have meanings that are more context-specific and may
have slightly different neural representations in L1 vs. L2.
It is likely that the advantage for L1 over L2 has funda-
mentally the same basis as the dramatic impact of stimu-
lus frequency, familiarity and/or age of acquisition that is
already well documented in all aspects of performance in
SD, with a massively significant advantage for the higher
frequency, more familiar and earlier learned aspects of expe-
rience [35]. Many studies have demonstrated significant age
of acquisition effects for naming in monolingual speakers
after brain damage [36–38], in healthy participants [39] and
in computational models [40, 41]. Other factors may also
contribute, however, such as degree of proficiency in, usage
of and exposure to [30, 42, 43], or even actual AOA of L2.
In this regard, it is worth noting that the relatively spared
language or L1 in our study was usually but not quite always
the mother tongue or primary language, with two patients
(patients 8 and 12) being exceptions. For the remaining 14
patients, L1 was also their mother tongue or primary lan-
guage. Thus, what our results demonstrate is that the most
used or most proficient and usually first-acquired language
was relatively spared and the other languages were largely
lost.
Limitations of our study include relatively low scores and
the inability of some patients to complete the tests in spite
Journal of Neurology
of the rather short duration of symptoms reported by their
families. This may be in part due to cultural effects, where
even well-educated healthy people seem to do poorly on
tests as compared to western populations [24]. A lack of
awareness of dementia in general, failure to recognize early
symptoms by the family and misdiagnosis by the primary
physician may also have contributed to the apparent discrep-
ancy between duration and performance on tests. We made
every effort to match controls to patients and succeeded
in matching 10 with similar language characteristics. An
exactly matched control sample, though of course ideal,
would be extremely difficult to identify. Furthermore, as in
many clinical studies, it was not feasible to achieve an ideal
combination of extensive cognitive testing and sophisticated
brain imaging in a large patient cohort.
Future directions include a study of the interaction of fac-
tors such as age of acquisition, degree of proficiency and
usage of/exposure to L2 on language decline in SD as com-
pared to the other varieties of PPA.
In conclusion, we found a dramatic loss of less proficient
and usually later-acquired languages (L2/L3) in our bilingual
(and multilingual) patients with SD. Furthermore, any cor-
rect responses for both naming and word comprehension in
L2 were virtually always matched by success on the same
items in L1. These results suggest (a) that less proficient
and usually later-learned languages are more vulnerable to
neurodegeneration, and (b) that different languages connect
to a common semantic network in the brain.
Acknowledgements The authors thank all the patients and their fami-
lies for participating in the study and colleagues for referrals. Some of
the findings from this study have been presented at the International
Neuropsychological Society (INS) meeting in London, 6–8 July 2016,
at the British Neuropsychological Society (BNS) meeting in London,
1 November 2018 and the International conference on Frontotemporal
dementias in Sydney, 11–14 November 2018.
Funding This research did not receive any specific grant from funding
agencies in the public, commercial or not-for-profit sectors.
Compliance with ethical standards
Conflicts of interest On behalf of all the authors, the corresponding
author states that there is no conflict of interest.
Ethical standard The study has been approved by the hospital ethics
committee.
Informed consent All patients or their caregivers and controls gave
informed consent according to the Declaration of Helsinki.
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