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Published

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Jan

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Bilingualism

and

Cognitive

Reserve

A

Critical

Overview

and

a

Plea

for

Methodological

Innovations

Noelia

Calvo

Adolfo

M

García

Laura

Manoiloff

and

Agustín

Ibáñez

Author

information

Article

notes

Copyright

and

License

information

This

article

has

been

cited

by

other

articles

in

PMC

Go

to

Abstract

Keywords

bilingualism

Alzheimers

disease

cognitive

reserve

retrospective

studies

experimental

research

Go

to

Introduction

Our

daily

activities

have

profound

cognitive

consequences

In

particular

they

may

influence

our

chances

to

develop

Alzheimers

disease

ADthe

most

prevalent

form

of

dementia

Ferri

et

al

Hebert

et

al

characterized

by

progressive

episodic

memory

loss

and

other

executive

linguistic

and

behavioral

symptoms

McKhann

et

al

For

example

AD

is

more

likely

to

occur

if

one

leads

a

lonely

life

Wilson

et

al

Cacioppo

et

al

or

suffers

from

a

vascular

disease

Dickstein

et

al

Conversely

AD

may

be

delayed

or

even

prevented

through

sustained

stimulating

activities

For

instance

the

onset

of

dementia

is

considerably

delayed

in

individuals

who

have

higher

educational

and

occupational

achievements

Stern

or

who

develop

musical

expertise

HannaPladdy

and

MacKay

The

latter

findings

have

been

taken

as

evidence

for

the

phenomenon

of

cognitive

reserve

CR

the

brains

capacity

for

functional

compensation

or

resilience

following

damage

or

throughout

healthy

aging

Stern

Cabeza

and

Dennis

In

the

former

sense

CR

refers

to

the

relationship

between

the

degree

of

pathology

or

brain

damage

and

the

intensity

or

earliness

of

its

clinical

manifestations

Stern

In

particular

the

deleterious

effects

of

brain

damage

would

be

delayed

or

reduced

by

experienceinduced

changes

in

specific

neurocognitive

networks

Stern

This

would

be

favored

by

activities

which

engage

circuits

sensitive

to

agerelated

attrition

and

agerelated

functional

activation

increases

Cabeza

and

Dennis

The

view

has

recently

emerged

that

CR

may

be

enhanced

by

a

specific

type

of

linguistic

experience

lifelong

bilingualism

Kavé

et

al

Bak

et

al

In

line

with

evidence

for

a

bilingual

advantage

in

executive

functioning

see

Section

Bilingualism

Key

Notions

and

Findings

some

studies

found

that

symptoms

of

dementia

Bialystok

et

al

Chertkow

et

al

Craik

et

al

Alladi

et

al

Woumans

et

al

and

mild

cognitive

impairment

MCI

Ossher

et

al

Bialystok

et

al

have

a

later

onset

in

bilingualplurilingual

than

in

monolingual

patients

Moreover

Schweizer

et

al

reported

comparable

cognitive

performance

between

bilingual

and

monolingual

AD

patients

despite

greater

brain

atrophy

in

the

former

Bilingualism

has

also

been

claimed

to

favor

CR

throughout

healthy

aging

Bak

et

al

especially

if

high

proficiency

levels

are

attained

Gollan

et

al

Additional

studies

found

that

lifelong

bilingualism

is

positively

associated

with

white

matter

integrity

Gold

et

al

Olsen

et

al

and

gray

matter

density

Abutalebi

et

al

in

several

brain

areas

crucially

including

the

frontal

lobes

However

the

claim

that

bilingualism

fosters

CR

is

not

uncontroversial

First

several

studies

have

failed

to

replicate

the

above

findings

Crane

et

al

Sanders

et

al

Clare

et

al

Zahodne

et

al

Kowoll

et

al

Lawton

et

al

Second

nontrivial

methodological

caveats

can

be

identified

in

the

seemingly

confirmatory

reports

Finally

the

evidence

for

volumetric

brain

differences

between

bilinguals

and

monolinguals

does

not

directly

imply

increased

CR

Moreover

it

remains

unclear

which

cognitive

functions

would

be

preserved

by

bilingualism

and

when

such

protective

effects

would

become

manifest

Consequently

at

present

it

is

not

clear

whether

bilingualism

delays

the

onset

of

dementia

The

main

results

vary

from

study

to

study

with

some

of

them

agreeing

on

at

least

years

of

delay

in

AD

and

MCI

symptoms

and

others

yielding

no

difference

between

monolinguals

and

bilinguals

It

may

well

be

the

case

that

bilingualism

contributes

to

CR

in

laterlife

Yet

for

this

view

to

be

fully

embraced

we

must

explicitly

address

contradictory

findings

identify

possible

lurking

variables

and

outline

methodological

alternatives

thereof

The

present

paper

pursues

those

three

goals

First

we

review

the

available

evidence

highlighting

its

inconsistencies

Go

to

Bilingualism

Key

notions

and

findings

The

term

bilingualism

has

received

various

definitions

in

the

specialized

literature

Whereas

some

authors

have

used

it

restrictively

to

mean

nativelike

mastery

of

two

languages

eg

Bloomfield

others

employ

it

more

broadly

as

the

alternate

use

of

two

languages

irrespective

of

proficiency

eg

Weinreich

Mackey

In

line

with

the

latter

view

here

we

will

subscribe

to

Grosjeans

definition

of

a

bilingual

as

any

person

who

uses

two

languages

or

dialects

in

daily

life

Within

this

broad

population

bilinguals

can

be

classified

in

terms

of

age

of

second

language

acquisition

early

vs

late

bilinguals

simultaneity

of

acquisition

simultaneous

vs

sequential

bilinguals

proficiency

from

incipient

to

low

mid

and

highproficiency

bilinguals

and

frequency

of

use

active

vs

latent

bilinguals

among

other

variables

Note

that

the

notion

of

bilingualism

is

sometimes

taken

as

synonymous

with

plurilingualism

ie

sustained

use

of

more

than

two

languages

However

both

need

to

be

differentiated

Indeed

cognitive

performance

in

several

domains

including

inhibitory

control

Marian

et

al

is

modulated

by

the

acquisition

of

languages

beyond

the

Thus

the

term

bilingual

should

be

reserved

to

individuals

who

possess

daily

functional

skills

in

only

two

languages

Neuroanatomically

a

native

language

and

an

are

subserved

by

independent

neural

networks

although

these

may

be

located

in

shared

gross

regions

as

indicated

by

aphasiological

Paradis

electrostimulation

Ojemann

and

Whitaker

Rapport

et

al

and

neuroimaging

Chee

et

al

Klein

et

al

studies

During

verbal

production

language

selection

and

inhibition

of

lexical

competitors

implicate

both

cortical

left

prefrontal

cortex

and

subcortical

anterior

cingulate

cortex

left

caudate

nucleus

bilateral

supramarginal

gyri

structures

Abutalebi

and

Green

Switching

between

both

languages

depends

on

a

broad

bilateral

frontotemporal

network

as

shown

by

a

recent

metaanalysis

Luk

et

al

However

a

bilinguals

neurocognitive

profile

is

sensitive

to

variables

such

as

age

of

acquisition

exposure

and

proficiency

For

example

the

functional

and

anatomical

correlates

of

the

and

the

tend

to

be

more

similar

in

early

than

in

late

bilinguals

especially

if

exposure

is

constant

Ardal

et

al

Neville

et

al

Perani

et

al

Kim

et

al

WeberFox

and

Neville

Ullman

Paradis

Similarly

the

neurofunctional

mechanisms

engaged

by

each

language

are

typically

more

convergent

in

highthan

in

lowproficiency

bilinguals

eg

Perani

et

al

Videsott

et

al

as

confirmed

by

a

metaanalysis

of

neuroimaging

studies

Sebastian

et

al

Another

line

of

research

has

assessed

how

bilingualism

impacts

cognitive

functions

across

multiple

domains

Bilinguals

have

been

observed

to

present

advantages

in

certain

aspects

of

executive

functioning

such

as

inhibitory

control

and

working

memory

for

a

review

see

Bialystok

et

al

Such

effects

have

been

reported

in

children

Carlson

and

Meltzoff

AdiJapha

et

al

Bialystok

young

adults

RodriguezFornells

et

al

Costa

et

al

Prior

and

MacWhinney

and

older

adults

Bialystok

et

al

Salvatierra

and

Rosselli

In

this

vein

a

metaanalysis

of

studies

reported

that

bilingualism

was

associated

with

increased

attentional

control

and

working

memory

skills

among

other

domains

Adesope

et

al

By

way

of

explanation

it

has

been

proposed

that

the

more

stringent

language

control

demands

faced

by

bilinguals

during

everyday

communication

enhance

domaingeneral

executive

functioning

This

view

is

further

supported

by

evidence

that

professional

simultaneous

interpreters

outperform

noninterpreter

bilinguals

certain

executive

measures

such

as

working

memory

tasks

Bajo

et

al

Christoffels

et

al

Yudes

et

al

However

claims

for

a

bilingual

advantage

have

recently

come

under

fire

First

some

nonexecutive

domains

such

as

singlelanguage

receptive

vocabulary

and

fluency

consistently

reveal

bilingual

disadvantages

Bialystok

et

al

Moreover

several

recent

comparisons

of

executive

performance

between

bilinguals

and

monolinguals

have

mostly

yielded

results

for

a

review

see

Duñabeitia

and

Carreiras

It

has

even

been

shown

that

cognitive

advantages

of

bilinguals

relative

to

monolinguals

may

be

eliminated

depending

on

the

data

trimming

procedure

Zhou

and

Krott

In

addition

the

evidence

of

enhancements

induced

by

interpreting

expertise

is

not

entirely

robust

for

a

review

see

García

Finally

studies

on

possible

neuroanatomical

changes

associated

with

the

bilingual

experience

have

yielded

ambiguous

results

GarcíaPentón

et

al

Thus

although

claims

for

distinctive

neurocognitive

effects

of

bilingualism

have

attracted

great

scholarly

and

media

attention

in

recent

years

accumulating

data

reveals

a

hazy

and

inconsistent

picture

As

we

argue

below

the

same

seems

to

be

true

of

studies

on

bilingualism

and

CR

Go

to

Cognitive

reserve

in

bilinguals

with

dementia

An

inconsistent

body

of

data

The

main

claims

for

a

protective

effect

of

bilingualism

stem

from

retrospective

analyses

of

clinical

records

Although

recent

studies

have

explored

the

issue

by

considering

motor

diseaseseg

Parkinsons

disease

Hindle

et

al

the

bulk

of

the

evidence

comes

from

comparisons

between

monolingual

and

bilingual

AD

patients

Bialystok

et

al

first

observed

that

dementia

appeared

roughly

years

later

in

bilingual

immigrants

who

spoke

English

and

any

other

language

A

similar

finding

was

reported

by

Craik

et

al

in

a

sample

including

immigrants

and

nonimmigrants

A

delay

of

approximately

years

was

also

observed

in

elderly

AD

patients

including

nonimmigrant

bilinguals

Woumans

et

al

This

pattern

was

replicated

in

subjects

with

mixed

types

of

dementia

Alladi

et

al

and

patients

with

both

MCI

and

AD

Bialystok

et

al

Also

a

study

controlling

for

childhood

intelligence

in

healthy

individuals

found

that

elderly

bilinguals

had

better

cognitive

performance

than

predicted

from

their

baseline

abilities

Bak

et

al

However

other

studies

have

only

partially

supported

the

hypothesis

as

they

found

confirmatory

evidence

only

for

specific

bilingual

subgroups

Chertkow

et

al

compared

the

age

of

symptom

onset

and

diagnosis

in

subjects

who

were

monolingual

bilingual

and

plurilingual

AD

patients

They

reported

a

delay

of

years

for

immigrant

bilinguals

and

plurilinguals

but

no

significant

benefit

in

nonimmigrant

bilinguals

Moreover

a

protective

effect

was

observed

for

nonimmigrants

whose

was

French

but

not

for

those

whose

was

English

Ossher

et

al

examined

patients

with

MCI

and

observed

a

symptomonset

delay

only

for

amnestic

bilinguals

Also

a

study

on

executive

functions

inhibition

attention

and

working

memory

with

healthy

elderly

participants

found

that

bilingual

advantages

were

restricted

to

highly

proficient

individuals

Gollan

et

al

In

addition

Kousaie

and

Phillips

used

a

Stroop

task

in

a

nonimmigrant

sample

of

young

and

older

monolinguals

and

bilinguals

and

showed

that

only

bilingual

young

adults

had

a

general

speed

advantage

relative

to

their

monolingual

counterparts

but

this

was

not

associated

with

smaller

Stroop

interference

Crucially

several

longitudinal

studies

on

AD

found

no

evidence

for

increased

CR

in

bilinguals

In

the

report

by

Crane

et

al

secondgeneration

JapaneseAmericans

nondemented

at

baseline

were

assessed

for

dementia

on

three

occasions

over

years

Midlife

use

of

spoken

and

written

Japanese

was

not

related

to

lower

cognitive

decline

rates

in

later

life

Another

study

Sanders

et

al

compared

the

incidence

of

dementia

in

elderly

native

and

nonnative

English

users

The

latter

group

gave

no

evidence

of

increased

CR

and

actually

exhibited

a

small

yet

not

significant

increase

in

risk

for

dementia

Notably

nonnative

speakers

with

at

least

years

of

education

had

a

fourfold

increased

risk

for

dementia

compared

to

less

educated

participants

Similarly

Zahodne

et

al

tested

AD

participants

at

month

intervals

for

up

to

years

Almost

subjects

developed

dementia

in

the

course

of

the

study

Bilingualism

was

associated

with

better

memory

and

executive

function

at

baseline

However

it

was

not

related

to

rates

of

cognitive

decline

or

dementia

conversion

Finally

Kowoll

et

al

did

not

observe

significant

neuropsychological

differences

between

monolingual

and

bilingual

MCIAD

patients

in

a

sample

of

participants

However

the

authors

concluded

that

the

dominant

language

may

be

compromised

first

in

bilingual

MCI

patients

while

severe

deficits

of

the

nondominant

language

would

appear

later

when

AD

becomes

manifest

results

have

also

been

reported

in

cohort

studies

Clare

et

al

conducted

a

crosssectional

investigation

with

early

AD

patients

At

the

time

of

diagnosis

bilinguals

were

on

average

years

older

than

monolinguals

but

they

also

exhibited

significantly

greater

cognitive

deficits

Moreover

despite

relatively

better

performance

on

inhibition

and

response

conflict

tasks

bilinguals

possessed

no

significant

advantages

on

executive

function

Additional

evidence

comes

from

the

cohort

study

by

Lawton

et

al

They

assessed

Hispanic

Americans

above

age

half

of

whom

were

immigrants

every

months

for

years

Fiftyfive

participants

were

diagnosed

with

AD

and

with

vascular

dementia

Crucially

mean

age

of

diagnosis

was

not

significantly

different

among

bilingual

and

monolingual

USborn

or

immigrant

patients

For

further

details

on

these

studies

see

Table

Table

Summary

of

retrospective

studies

on

the

relationship

between

bilingualism

and

cognitive

reserve

in

demented

populations

In

sum

positive

and

results

have

been

evenly

documented

in

the

literature

This

suggests

that

bilingualism

may

contribute

to

CR

but

only

under

certain

unknown

conditions

To

a

large

extent

such

discrepancies

may

reflect

methodological

differences

between

and

shortcomings

within

the

available

studies

Such

factors

are

discussed

below

in

an

attempt

to

foster

more

robust

approaches

to

the

issue

Go

to

Methodological

caveats

within

and

across

studies

Nonexperimental

research

faces

important

caveats

when

it

targets

a

population

as

diverse

as

bilinguals

especially

those

affected

with

heterogeneous

conditions

such

as

AD

The

impossibility

to

control

critical

factors

and

collect

relevant

subject

data

leads

to

widespread

intra

and

intergroup

variability

In

this

sense

the

above

studies

are

characterized

by

major

differences

andor

limitations

concerning

four

factors

i

the

conception

of

bilingualism

and

the

assessment

of

language

proficiency

ii

sample

design

iii

the

instruments

used

to

assess

cognitive

skills

and

diagnose

the

underlying

clinical

entity

and

iv

the

examination

of

other

variables

known

to

affect

CR

Shortcomings

in

the

conception

and

assessment

of

bilingualism

The

literature

presents

several

caveats

regarding

the

conception

of

bilingualism

and

the

assessment

of

language

proficiency

Most

of

the

retrospective

studies

in

Section

Cognitive

reserve

in

Bilinguals

with

Dementia

An

Inconsistent

Body

of

Data

established

bilingualism

and

proficiency

via

subjective

interviews

with

the

patients

Bialystok

et

al

Chertkow

et

al

Craik

et

al

Crane

et

al

Sanders

et

al

Woumans

et

al

or

their

caregivers

Chertkow

et

al

Craik

et

al

Schweizer

et

al

Alladi

et

al

Woumans

et

al

However

subjective

estimations

of

proficiency

can

be

unreliable

and

biased

by

selfperception

Hulstijn

In

some

studies

eg

Chertkow

et

al

data

concerning

acquisition

and

immigration

status

were

unavailable

and

thus

impressionistically

estimated

Likewise

age

of

acquisition

varied

greatly

among

and

even

within

studies

In

the

case

of

Woumans

et

al

for

instance

some

participants

had

acquired

their

since

birth

others

around

puberty

and

still

others

during

adulthood

This

constitutes

another

potential

confound

given

that

bilinguals

rely

on

different

cognitive

mechanisms

depending

on

the

manner

and

age

of

appropriationviz

incidental

acquisition

vs

metalinguistic

learning

Paradis

as

well

as

the

sociocultural

circumstances

framing

bilingual

developmenteg

circumstantial

vs

elective

bilingualism

in

immigrants

and

learners

respectively

Valdés

and

Figueroa

Moreover

most

reports

confounded

bilingualism

with

plurilingualism

For

instance

in

the

study

by

Alladi

et

al

of

the

participants

spoke

two

languages

whereas

more

than

spoke

three

or

more

languages

This

is

a

nontrivial

consideration

since

the

neurocognitive

resources

taxed

during

bilingual

processing

are

sensitive

to

the

presence

of

additional

languages

Marian

et

al

Indeed

a

study

comparing

bilinguals

trilinguals

and

plurilinguals

Kavé

et

al

showed

that

the

number

of

nonnative

languages

spoken

influenced

cognitive

performance

beyond

the

effect

of

demographic

variables

Also

most

of

the

studies

included

bilinguals

possessing

varied

language

pairs

only

some

of

which

were

typologically

similar

eg

Kowoll

et

al

Woumans

et

al

However

access

and

control

mechanisms

in

bilingual

processing

differ

depending

on

the

typological

distance

between

languages

Tao

et

al

García

Moreover

assessments

of

monolingualism

are

absent

in

most

studies

This

is

a

critical

aspect

for

the

literature

on

bilingualism

and

CR

as

there

may

not

be

such

a

thing

as

a

pure

monolingual

De

Bot

and

Jaensch

All

in

all

the

literature

on

bilingualism

and

CR

proves

inconsistent

and

sometimes

flawed

in

its

characterization

of

the

former

variable

To

a

large

extent

this

is

due

to

the

reliance

on

retrospective

nonexperimental

approaches

which

precludes

the

construction

of

carefully

controlled

samples

It

is

crucial

to

for

the

field

to

develop

more

robust

sampling

procedures

especially

in

the

exploration

of

possible

neurological

correlations

Indeed

proficiency

positively

correlates

with

gray

matter

volume

in

controlrelevant

areas

Stein

et

al

and

with

the

age

of

AD

diagnosis

and

symptom

onset

Gollan

et

al

Variability

in

sample

design

Proper

randomization

is

not

easily

achieved

in

retrospective

designs

and

sample

sizes

vary

greatly

across

studies

In

the

present

review

three

studies

included

less

than

participants

Gollan

et

al

Schweizer

et

al

Kowoll

et

al

two

less

than

Clare

et

al

Lawton

et

al

six

less

than

Bialystok

et

al

Craik

et

al

Kousaie

and

Phillips

Ossher

et

al

Woumans

et

al

three

between

and

Chertkow

et

al

Alladi

et

al

Bak

et

al

and

another

three

between

and

Crane

et

al

Sanders

et

al

Zahodne

et

al

Since

effect

sizes

are

partially

linked

to

sample

sizes

especially

when

effects

are

robust

Little

these

differences

across

studies

may

partly

account

for

their

discrepant

findings

In

retrospective

studies

as

in

experimental

designs

demographic

eg

age

sex

education

and

clinical

eg

other

pathologies

variables

must

be

matched

between

compared

groups

to

adjust

for

potential

confounds

and

increase

precision

in

the

analysis

In

this

sense

a

further

caveat

of

the

studies

is

that

they

compare

samples

of

different

sizes

In

some

cases

there

were

more

monolinguals

than

bilinguals

eg

Chertkow

et

al

Zahodne

et

al

Lawton

et

al

and

in

the

study

by

Sanders

et

al

one

of

the

groups

tripled

the

other

in

size

Samples

with

such

different

sizes

may

lead

to

biased

results

as

the

larger

one

is

likely

to

feature

greater

variance

and

thus

be

more

representative

of

its

respective

population

This

is

especially

true

when

the

smaller

group

is

the

one

composed

by

bilinguals

as

random

selections

of

such

individuals

may

not

realistically

represent

the

wide

spectrum

of

ages

of

acquisition

levels

of

competence

and

degrees

of

exposure

This

scenario

is

further

complicated

by

sample

heterogeneity

Some

studies

compared

monolinguals

and

bilinguals

others

examined

different

types

of

bilinguals

and

still

others

considered

different

types

of

dementia

sometimes

without

control

group

see

Table

for

details

In

particular

dementias

are

not

homogeneous

conditions

and

they

may

differ

in

their

susceptibility

of

early

diagnosis

progression

speed

degree

of

genetic

compromisevulnerability

and

the

local

or

global

nature

of

affected

cognitive

domains

In

addition

inclusion

and

exclusion

criteria

in

most

studies

are

either

absent

or

poorly

specified

Finally

these

studies

fail

to

complement

measures

of

statistical

significance

p

value

with

calculations

of

effect

size

This

would

be

useful

to

ascertain

the

minimum

number

of

participants

needed

to

avoid

a

Type

II

or

β

error

Sullivan

and

Feinn

Importantly

sample

size

should

be

established

before

initiating

any

study

and

as

far

as

possible

it

should

not

be

changed

during

the

course

of

the

study

Kadam

and

Bhalerao

In

this

respect

only

few

studies

have

contemplated

these

measures

Bak

et

al

Bialystok

et

al

Clare

et

al

Woumans

et

al

and

some

have

excluded

participants

who

were

not

relevant

for

the

analysis

changing

the

size

of

the

initial

sample

Chertkow

et

al

Crane

et

al

Gollan

et

al

Sanders

et

al

Zahodne

et

al

Lawton

et

al

All

in

all

there

is

major

variability

in

sample

size

calculation

and

stability

Also

some

crucial

statistical

aspects

have

not

been

made

explicit

enough

in

the

literature

Retrospective

studies

may

lack

power

to

achieve

significance

but

these

measures

should

at

least

be

mentioned

Sullivan

and

Feinn

Reservations

on

the

instruments

used

to

assess

cognitive

deficits

and

diagnose

the

underlying

clinical

entity

Importantly

there

is

variability

in

the

criteria

for

the

diagnosis

of

MCI

and

AD

All

but

one

of

the

studies

targeting

pathological

groups

established

diagnosis

through

the

consensus

of

medically

qualified

clinical

staff

In

seven

of

them

Bialystok

et

al

Chertkow

et

al

Craik

et

al

Sanders

et

al

Kowoll

et

al

Lawton

et

al

AD

was

diagnosed

following

NINCDSADRDA

criteria

McKhann

et

al

two

followed

the

DSM

IIIIV

criteria

Crane

et

al

Sanders

et

al

respectively

one

relied

on

Clare

et

al

and

three

followed

other

criteria

Schweizer

et

al

Alladi

et

al

Clare

et

al

in

the

absence

of

clinical

staff

consensus

In

addition

to

these

diagnostic

discrepancies

the

underlying

pathology

was

not

consistent

among

or

even

within

some

studies

Ossher

et

al

focused

on

patients

with

MCI

as

established

via

the

criteria

in

Petersen

This

condition

was

considered

in

tandem

with

AD

by

Bialystok

et

al

who

followed

the

diagnostic

criteria

proposed

by

Albert

et

al

Also

for

patients

in

the

study

by

Chertkow

et

al

dementia

onset

was

defined

as

the

clinic

visit

at

which

a

preceding

MCI

diagnosis

changed

to

AD

Moreover

the

study

by

Bialystok

et

al

included

patients

diagnosed

with

other

dementias

including

possible

AD

These

differences

also

cast

further

doubt

on

the

consistency

of

the

results

given

that

diagnosis

can

vary

greatly

depending

on

the

type

of

impairment

exhibited

by

patients

and

on

the

criteria

used

to

establish

the

underlying

clinical

entity

Burvill

Further

reservations

concern

the

instruments

used

to

assess

dementia

Virtually

all

studies

have

done

so

via

the

MMSE

Folstein

et

al

Whereas

some

have

incorporated

additional

measureseg

the

Behavioral

Neurology

Assessment

Schweizer

et

al

Bialystok

et

al

the

Clinical

Dementia

Rating

Schweizer

et

al

Alladi

et

al

the

Addenbrookes

Cognitive

ExaminationRevised

Alladi

et

al

in

most

cases

this

was

the

only

neuropsychological

measure

employed

eg

Bialystok

et

al

Chertkow

et

al

Craik

et

al

Kowoll

et

al

Woumans

et

al

However

abundant

research

shows

that

the

MMSE

is

of

limited

value

to

diagnose

onset

dementia

Wind

et

al

Kim

and

Caine

measure

its

progression

within

periods

of

less

than

years

Clark

et

al

detect

MCI

TangWai

et

al

and

even

assess

general

cognitive

profile

Feher

et

al

Actually

it

is

possible

to

have

AD

and

still

score

on

this

test

Shiroky

et

al

In

addition

initial

symptoms

of

AD

could

be

even

more

difficult

to

detect

in

individuals

with

higher

CR

Furthermore

neither

the

MMSE

nor

the

other

instruments

used

are

specifically

aimed

at

assessing

executive

domains

whose

evaluation

may

be

critical

to

ascertain

the

specific

impact

of

bilingualism

on

CR

Bialystok

et

al

Note

also

that

executive

dysfunction

may

represent

one

of

the

early

manifestations

of

AD

Thus

the

inclusion

of

additional

sensitive

measures

especially

those

targeting

executive

performance

could

prove

crucial

for

the

field

to

progress

Is

it

really

bilingualism

Lurking

variables

known

to

affect

CR

Claims

for

a

specific

relationship

between

bilingualism

and

CR

must

rule

out

the

influence

of

confounding

factors

Available

studies

have

only

partially

succeeded

in

this

regard

While

most

of

them

offer

data

on

the

patients

age

education

level

and

socioeconomic

status

SES

they

rarely

contemplate

other

relevant

factors

CR

may

be

enhanced

by

varied

habits

and

personality

traits

For

instance

it

may

be

promoted

through

social

networking

Bennett

et

al

or

sustained

intellectual

stimulation

across

the

lifespan

rather

than

education

Scarmeas

and

Stern

Other

contributing

factors

are

overall

fitness

amount

of

exercise

and

type

of

sustained

physical

activity

eg

Davenport

et

al

In

particular

healthy

aerobic

exercise

reduces

hippocampal

volume

loss

and

improves

memory

in

adulthood

Erickson

et

al

CR

may

also

be

enhanced

by

the

development

of

emotional

skills

favoring

adaptive

behaviors

and

resilience

in

the

face

of

stress

Staudinger

et

al

Such

skills

may

figure

more

prominently

in

immigrant

than

in

nonimmigrant

individuals

thus

the

conclusions

advanced

in

some

studies

eg

Bialystok

et

al

Chertkow

et

al

Craik

et

al

Kowoll

et

al

may

have

been

misattributed

or

overgeneralizedie

they

may

not

be

applicable

for

any

type

of

bilingual

On

the

other

hand

some

poorly

controlled

factors

can

be

detrimental

to

CR

In

particular

some

of

them

may

play

a

distinctive

role

in

bilingual

populations

especially

in

immigrant

groups

Importantly

one

of

the

most

studied

factors

known

to

enhance

CR

is

SES

which

has

been

analyzed

in

most

studies

with

bilingual

immigrant

groups

In

this

regard

high

SES

has

been

associated

with

reduced

risk

of

MCIAD

Sattler

et

al

however

migration

often

involves

a

loss

of

SES

and

increased

rates

of

mental

illness

Bhugra

and

Becker

Moreover

immigrant

populations

are

at

increased

risk

for

congenital

and

acquired

neurological

disorders

White

et

al

Zahuranec

et

al

alcohol

abuse

due

to

the

stress

of

acculturation

Caetano

et

al

Szaflarski

et

al

eating

disorders

Geller

and

Thomas

Bulik

et

al

poor

sleep

quality

Voss

and

Tuin

and

the

acquisition

of

bad

health

habits

like

smoking

Bethel

and

Schenker

At

the

same

time

sustained

use

of

more

than

one

language

has

been

linked

to

greater

chances

of

alcohol

use

in

adolescence

Epstein

et

al

and

to

fewer

acknowledgments

of

the

dangers

associated

with

smoking

Unger

et

al

Differences

between

bilinguals

and

monolinguals

in

these

variables

may

further

underlie

discrepancies

in

the

literature

Hippocampal

neurogenesis

decreases

in

excessive

drinkers

Stevenson

et

al

and

possibly

in

teetotalers

den

Heijer

et

al

Instead

moderate

consumption

may

favor

acetylcholine

release

in

the

hippocampus

Henn

et

al

and

thus

reduce

risk

of

AD

Also

cigarette

smoking

accelerates

cortical

thinning

a

robust

biomarker

of

cognitive

decline

Karama

et

al

Memory

impairments

are

also

associated

to

other

bad

health

habits

like

poor

sleep

or

eating

disorders

Green

and

Rogers

Walker

and

Stickgold

among

several

others

However

these

factors

have

been

barely

controlled

in

the

reviewed

literature

Some

of

them

have

been

considered

with

varying

degrees

of

robustness

The

most

objective

data

have

been

offered

by

Schweizer

et

al

who

applied

the

Katz

Activities

of

Daily

Living

index

Bialystok

et

al

used

a

selfassessment

questionnaire

to

glean

data

on

the

patients

diet

alcohol

use

smoking

habits

and

physical

and

social

activity

this

approach

is

less

reliable

due

to

the

biases

inherent

in

selfreports

of

socially

sanctioned

practices

For

their

part

Alladi

et

al

interviewed

patients

relatives

to

gather

information

on

vascular

risk

factors

diabetes

smoking

and

alcoholism

although

no

further

methodological

specifications

are

offered

on

how

data

were

collected

Results

in

this

study

may

have

also

been

biased

by

the

use

of

a

heterogeneous

sample

of

highly

educated

older

bilinguals

Indeed

disease

development

may

be

slower

and

more

sensitive

to

factors

other

than

bilingualism

in

older

than

in

younger

participants

More

critically

of

the

studies

seems

to

have

employed

instruments

specifically

designed

to

assess

such

variables

see

Section

Improving

the

Toolkit

for

Subject

Sampling

and

Assessment

In

sum

the

paucity

of

information

regarding

these

factors

undermines

claims

for

and

against

a

positive

relationship

between

bilingualism

and

CR

As

we

propose

below

future

studies

should

more

carefully

consider

other

variables

which

may

promote

positive

eg

synaptic

strengthening

or

negative

eg

atrophy

synaptic

weakening

plastic

changes

that

may

be

related

to

MCI

and

AD

and

which

may

have

critical

effects

in

the

bilingual

population

Go

to

A

plea

for

methodological

improvements

and

experimental

approaches

The

evidence

on

the

relationship

between

bilingualism

and

CR

is

inconsistent

and

characterized

by

methodological

limitations

These

shortcomings

however

do

not

necessarily

imply

that

CR

is

unaffected

by

the

bilingual

experience

We

propose

that

the

issue

may

be

more

properly

addressed

by

refining

the

control

of

relevant

subject

variables

and

by

incorporating

experimental

tasks

Improving

the

toolkit

for

subject

sampling

and

assessment

Many

of

the

limitations

can

be

circumvented

by

adopting

better

instruments

to

assess

and

classify

participants

with

a

view

to

maximizing

homogeneity

within

and

comparability

between

samples

First

the

assessment

of

bilingualism

and

bilingual

proficiency

should

be

carefully

considered

Questionnaires

should

be

comprehensive

enough

to

assess

critical

information

such

as

biographical

information

from

participants

and

relatives

use

of

proficiency

language

dominance

acquisition

attitude

and

language

preference

and

social

status

Codó

Moreover

to

maximize

comparability

across

studies

the

use

of

standardized

questionnaires

is

highly

advisable

A

good

candidate

in

this

sense

is

the

Language

History

Questionnaire

Li

et

al

Also

to

better

control

for

proficiency

it

would

be

useful

to

include

objective

measures

such

as

standardized

language

tests

or

examinations

in

specific

languages

eg

DIALANG

Diplômes

dÉtudes

en

Langue

Française

Zertifikar

Deutsch

Certificado

de

Español

Lengua

y

Uso

vocabulary

tests

like

LLEX

Meara

Cloze

tests

Hulstijn

or

even

the

Bilingual

Aphasia

Test

Paradis

and

Lecours

Paradis

Second

the

confounds

enumerated

in

Section

Is

it

Really

Bilingualism

Lurking

Variables

Known

to

Affect

CR

could

be

more

effectively

controlled

using

instruments

which

assess

them

directly

For

instance

the

Composite

International

Diagnostic

Interview

Robins

et

al

assesses

habits

of

alcohol

tobacco

and

drug

use

It

also

considers

the

quality

severity

and

course

of

substance

dependence

while

offering

valuable

information

about

possible

impairment

and

comorbid

mental

disorders

Similarly

the

Sleep

Disorders

Inventory

Zammit

et

al

has

proved

helpful

in

AD

research

This

instrument

evaluates

a

wide

range

of

sleep

behaviors

as

well

as

the

frequency

severity

and

caregiver

burden

of

sleeping

disturbances

Tractenberg

et

al

Relevant

data

may

also

be

gleaned

through

the

Eating

Disorders

Examinationquestionnaire

Fairburn

and

Beglin

a

selfreport

instrument

assessing

restraint

weight

concern

and

shape

concern

As

these

tools

can

help

disentangle

the

role

of

lurking

variables

in

the

observed

effects

future

studies

should

include

at

least

abridged

versions

of

them

Furthermore

as

proposed

by

Hogervorst

et

al

all

patients

with

cognitive

impairment

should

be

assessed

for

hypothyroidism

as

this

condition

correlates

with

lower

MMSE

performance

at

baseline

independent

of

age

sex

education

mood

and

cardiovascular

factors

In

addition

given

that

immigrants

are

at

increased

risk

for

several

disorders

Geller

and

Thomas

White

et

al

Bulik

et

al

Zahuranec

et

al

Caetano

et

al

Voss

and

Tuin

Szaflarski

et

al

nonimmigrant

populations

should

be

prioritized

in

an

attempt

to

establish

clearer

associations

between

bilingualism

and

CR

FullerThomson

and

Kuh

Third

more

sensitive

indicators

of

general

cognitive

screening

should

be

incorporated

to

complement

the

MMSE

Robust

assessments

can

be

obtained

with

the

traditional

Mattis

dementia

rating

scale

Mattis

the

Alzheimers

Disease

Assessment

Scale

Mohs

et

al

Mohs

and

Cohen

Mohs

and

the

Montreal

Cognitive

Assessment

Nasreddine

et

al

The

latter

instrument

in

particular

is

brief

possesses

reliable

psychometric

properties

DalrympleAlford

et

al

and

successfully

detects

subtle

deficits

and

MCI

Hoops

et

al

Also

as

Bialystok

et

al

maintain

broad

assessments

of

cognitive

status

should

be

complemented

with

sensitive

measures

of

executive

function

as

this

domain

is

specifically

modulated

by

bilingualism

A

good

option

would

be

the

INECO

Frontal

Screening

battery

Torralva

et

al

a

brief

tool

for

assessing

neurodegenerative

conditions

Torralva

et

al

Gleichgerrcht

et

al

in

general

and

medial

frontal

executive

functions

Roca

et

al

in

particular

Over

a

maximum

total

score

of

points

a

cutoff

score

has

shown

a

sensitivity

of

and

a

specificity

of

in

detecting

patients

with

dysexecutive

syndrome

Torralva

et

al

Its

application

may

be

particularly

informative

since

CR

may

be

modulated

by

executive

skills

both

in

AD

and

MCI

Buckner

In

brief

the

relationship

between

bilingualism

and

CR

may

be

more

clearly

explored

by

incorporating

reliable

measures

of

bilingual

proficiency

lifestyle

substance

use

cognitive

status

and

executive

functioning

These

would

be

particularly

useful

in

studies

featuring

intentional

samples

Moreover

they

could

yield

crucial

data

to

explore

associations

with

patients

performance

on

experimental

tasks

as

described

below

Incorporating

experimental

tasks

In

addition

to

improving

the

toolkit

used

in

nonexperimental

research

the

field

would

greatly

benefit

from

incorporating

controlled

experiments

In

particular

future

research

should

focus

on

domains

that

are

sensitive

to

the

impact

of

bilingualism

The

literature

shows

that

different

tasks

yield

distinctive

results

for

bilinguals

relative

to

monolinguals

disadvantages

in

verbal

processing

effects

in

working

memory

and

advantages

in

other

executive

functions

Bialystok

et

al

Accordingly

if

bilinguals

have

higher

CR

these

tasks

should

yield

predictable

patterns

of

performance

when

used

with

demented

samples

First

throughout

the

lifespan

bilinguals

show

disadvantages

in

singlelanguage

verbal

tasks

Bialystok

This

has

been

systematically

shown

through

the

Peabody

Picture

Vocabulary

Test

Dunn

and

Dunn

in

which

participants

must

decide

which

of

four

pictures

corresponds

to

a

noun

uttered

by

the

experimenter

Experiments

using

this

test

with

children

and

adults

show

that

bilinguals

are

outperformed

by

monolinguals

Bialystok

Thus

if

bilingualism

increases

CR

such

disadvantages

could

be

expected

to

attenuate

or

disappear

if

the

task

is

performed

by

demented

samples

Second

other

domains

seem

indifferent

to

the

effects

of

bilingualism

Bialystok

For

example

overall

working

memory

performance

seems

to

be

similar

in

bilinguals

and

monolinguals

This

result

is

particularly

robust

in

verbal

span

tasks

Bialystok

et

al

Feng

Bonifacci

et

al

Namazi

and

Thordardottir

Engel

de

Abreu

Accordingly

it

would

be

interesting

to

explore

whether

such

results

in

nondemented

samples

turn

into

bilingual

advantages

when

AD

samples

are

compared

Third

bilingualism

enhances

inhibitory

control

in

nonverbal

tasks

Studies

using

the

Simon

task

or

the

Stroop

task

have

reported

better

performance

in

bilinguals

than

in

agedmatched

monolinguals

Bialystok

et

al

Also

bilinguals

seem

to

have

stronger

intrinsic

functional

connectivity

in

the

frontoparietal

control

network

and

the

default

mode

network

which

may

be

beneficial

in

aging

Grady

et

al

At

the

same

time

performance

on

tests

of

executive

function

decline

more

rapidly

around

years

before

AD

diagnosis

Grober

et

al

Thus

longitudinal

research

with

AD

samples

could

examine

whether

executive

subdomains

eg

inhibitory

skills

relative

to

other

domains

are

less

affected

by

disease

progression

in

bilinguals

Finally

tasks

not

widely

used

in

the

field

of

bilingualism

may

also

shed

light

on

the

issue

Consider

for

example

proactive

interference

PI

paradigms

PI

refers

to

the

disruptive

effect

of

prior

information

on

retrieval

of

more

recent

information

Lustig

and

Hasher

That

is

PI

occurs

when

information

stored

in

longterm

memory

proactively

interferes

with

newly

learned

information

PI

resolution

involves

proactive

and

reactive

control

mechanisms

which

appear

to

be

better

managed

by

bilinguals

Morales

et

al

b

PI

skills

are

susceptible

to

age

and

cognitive

decline

in

normal

aging

Lustig

et

al

Bowles

and

Salthouse

and

they

may

deteriorate

in

early

stages

of

AD

Ebert

and

Anderson

and

amnestic

MCI

Crocco

et

al

note

that

premorbid

subjects

may

show

cognitive

decline

several

years

before

AD

diagnosis

Amieva

et

al

Second

PI

tasks

are

different

from

other

memory

measures

in

that

items

posed

for

recall

are

explicitly

presented

and

interference

effects

can

be

assessed

while

controlling

for

initial

levels

of

memory

impairment

Crocco

et

al

The

earliest

neuroanatomical

changes

in

aMCI

involve

the

hippocampus

and

the

entorhinal

cortex

two

structures

implicated

in

the

integration

and

learning

of

associative

information

Troyer

et

al

In

this

respect

PI

paradigms

may

be

worth

considering

as

aMCI

may

involve

increased

sensitivity

to

PI

effects

independently

of

other

associative

and

semantic

impairment

Hanseeuw

et

al

Moreover

default

mode

network

connectivity

is

altered

in

prodromal

AD

including

preMCI

individuals

with

cognitive

complaints

Sorg

et

al

Wang

et

al

Indeed

specific

regions

of

the

default

network

are

selectively

vulnerable

to

early

amyloid

deposition

in

AD

Sperling

et

al

Note

that

activation

of

the

default

network

has

been

proved

to

enhance

performance

on

executive

control

tasks

when

control

processes

engage

longterm

memory

representation

Spreng

et

al

and

proactive

control

has

been

associated

to

theta

frontoparietal

connectivity

Cooper

et

al

Thus

since

proactive

control

is

greatly

taxed

during

bilingual

processing

and

bilinguals

haven

shown

to

have

enhanced

connectivity

than

monolinguals

in

both

networks

Grady

et

al

PI

tasks

can

reveal

specific

aspects

of

memory

variance

in

the

onset

and

evolution

of

MCI

and

AD

in

bilinguals

Also

increased

PI

demands

in

bilinguals

may

bring

about

neuroplastic

changes

that

are

beneficial

in

aging

Ansaldo

et

al

As

this

mechanism

is

vulnerable

to

brain

dysfunction

Braver

et

al

and

the

PI

effect

has

been

linked

to

hippocampal

activity

in

neurogenesis

Frankland

et

al

it

may

also

constitute

another

critical

source

of

data

for

the

hypothesis

that

lifelong

bilingualism

enhances

CR

However

it

is

highly

likely

that

CR

relies

on

plastic

changes

other

than

neurogenesis

which

represents

a

rather

negligible

phenomenon

More

plausible

candidates

are

dendritic

sprouting

synaptogenesis

and

dendritic

arborization

which

have

been

shown

to

occur

more

prolifically

LealGalicia

et

al

Gelfo

et

al

Moreover

CR

may

impact

neural

plasticity

in

AD

patients

by

diminishing

Aβ

deposition

Jagust

and

Mormino

Besides

clinically

silent

pathology

in

normal

aging

suggests

that

CR

can

ameliorate

brain

dysfunction

via

plastic

mechanisms

even

when

brain

pathology

growths

In

fact

postmortem

studies

of

highpathology

nondemented

subjects

have

revealed

preserved

density

of

synaptophysinlabeled

presynaptic

terminals

and

dendritic

spines

relative

to

AD

patients

with

a

similar

burden

of

plaques

and

tangles

Jellinger

and

Attems

Although

evidence

for

these

phenomena

so

far

comes

mostly

from

animal

models

they

are

probably

more

pervasive

and

relevant

in

humans

as

well

Future

methodological

developments

may

help

clarify

the

putative

neuroplastic

mechanisms

supporting

CR

in

humans

and

more

specifically

in

bilinguals

Further

considerations

A

prospective

renewed

framework

to

assess

the

relationship

between

bilingualism

and

CR

should

also

contemplate

additional

issues

First

more

homogeneous

approaches

should

be

encouraged

for

AD

diagnosis

So

far

only

some

studies

have

considered

clinimetrics

and

cultural

differences

Future

studies

should

systematically

factor

in

both

aspects

Moreover

it

would

be

crucial

to

combine

behavioral

paradigms

with

different

techniques

revealing

possible

biomarkers

of

AD

across

genetic

anatomical

and

networkconnectivity

levels

First

note

that

wellestablished

risk

genes

eg

APOE

and

causative

genes

eg

APP

for

AD

have

been

expanded

to

more

than

risk

loci

eg

The

pathological

changes

induced

by

genetic

factors

could

be

better

understood

by

considering

cerebrospinal

fluid

biomarkers

Zhang

et

al

Kovacs

et

al

Ghidoni

et

al

Craft

et

al

A

challenge

for

the

field

is

to

explore

correlations

between

these

factors

and

differential

neurodegenerative

patterns

between

bilingual

and

monolingual

AD

patients

Also

neuroimaging

evidence

indicates

that

AD

is

characterized

by

alterations

in

the

default

mode

network

Sheline

and

Raichle

which

has

been

found

to

feature

stronger

intrinsic

functional

connectivity

in

bilinguals

than

in

monolinguals

Grady

et

al

Interestingly

proactive

control

has

been

associated

to

theta

frontoparietal

connectivity

Cooper

et

al

and

bilinguals

have

proved

to

have

better

resolution

of

control

mechanisms

Morales

et

al

b

So

it

would

be

useful

to

assess

whether

this

differential

pattern

holds

when

comparing

AD

patients

from

both

groups

Additionally

the

research

focus

should

move

beyond

detecting

delays

in

AD

symptoms

onset

It

would

be

useful

to

assess

the

impact

of

bilingualism

in

the

progression

of

AD

and

associated

cognitive

deficits

While

typical

measures

such

as

the

MMSE

are

blind

to

these

changes

experimental

tasks

including

PI

paradigms

may

reveal

progressive

patterns

in

the

course

of

disease

Thus

neuroimaging

or

electrophysiological

markers

could

be

obtained

during

active

tasks

to

assist

the

detection

progressive

monitoring

of

cognitive

changes

linked

to

normal

aging

MCI

and

AD

For

instance

shortterm

memory

binding

tasks

Parra

et

al

prove

sensitive

to

early

and

even

preclinical

AD

This

would

be

a

particularly

revealing

paradigm

to

track

the

onset

and

progression

of

early

AD

as

shortterm

memory

binding

is

not

affected

by

normal

aging

Brockmole

et

al

Parra

et

al

Brown

and

Brockmole

Brockmole

and

Logie

Moreover

PI

paradigms

may

reveal

memory

variance

and

CR

in

normal

aging

as

well

as

through

the

course

of

AD

PI

performance

decreases

throughout

healthy

aging

Lustig

et

al

Bowles

and

Salthouse

MCI

Crocco

et

al

and

AD

Ebert

and

Anderson

Thus

important

insights

could

be

gained

by

comparing

biomarkers

of

these

tasks

between

bilinguals

and

monolinguals

with

MCI

or

AD

Finally

the

field

should

expand

its

horizons

beyond

AD

and

assess

CR

in

bilinguals

exhibiting

other

disorders

In

this

sense

it

would

be

interesting

to

explore

other

conditions

characterized

by

both

linguistic

eg

primary

progressive

aphasia

and

nonlinguistic

eg

amyotrophic

lateral

sclerosis

behavioral

variant

frontotemporal

dementia

symptoms

This

would

pave

the

way

for

more

refined

insights

into

the

possible

impact

of

bilingualism

on

domainspecific

CR

Go

to

Conclusion

Research

on

CR

in

bilinguals

proves

very

challenging

because

of

the

multiple

variables

involved

The

limitations

underlying

inconsistencies

across

studies

could

be

largely

circumvented

through

experimental

approaches

to

the

issue

and

with

more

stringent

control

of

relevant

variables

Also

the

field

could

be

broadened

through

approaches

which

explore

not

just

the

delay

of

AD

in

bilinguals

but

the

changes

occurring

throughout

the

course

of

disease

These

considerations

could

help

us

tease

apart

the

potential

contributions

of

bilingualism

to

preserved

functioning

across

cognitive

domains

Moreover

they

may

shed

light

not

just

on

the

relationship

between

bilingualism

and

CR

but

also

on

Go

to

Author

contributions

All

authors

contributed

equally

to

this

work

Go

to

Funding

This

work

was

partially

supported

by

grants

from

CONICET

CONICYTFONDECYT

Regular

FONCyTPICT

and

the

INECO

Foundation

Conflict

of

interest

statement

The

authors

declare

that

the

research

was

conducted

in

the

absence

of

any

commercial

or

financial

relationships

that

could

be

construed

as

a

potential

conflict

of

interest

The

reviewer

Stefan

Elmer

and

handling

Editor

Lutz

Jäncke

declared

their

shared

affiliation

and

the

handling

Editor

states

that

the

process

nevertheless

met

the

standards

of

a

fair

and

objective

review

Go

to

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