Neural

Mechanisms

of

Visual

Attention

How

Top-Down

Feedback

Highlights

Relevant

Locations

Yuri

B.

Saalmann

et

al.

Science

-LRB-

-RRB-

DOI

science

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interesting

features

First

the

effective

interaction

pattern

could

be

modified

very

dynamically

Second

the

mechanism

would

act

connectionwise

Third

a

transient

interaction

would

lead

to

spike-time

dependent

plasticity

-LRB-

-RRB-

and

thus

a

long-term

trace

And

fourth

synchronization

might

emerge

in

a

self-organized

manner

between

matching

neuronal

groups

In

the

visual

cortex

synchronization

is

stronger

among

neurons

activated

by

the

same

visual

stimulus

-LRB-

-RRB-

This

principle

might

generalize

to

the

handshaking

between

cognitive

top-down

control

and

matching

sensory

bottom-up

information

in

which

case

consecutive

synchronization

could

contribute

to

the

selective

routing

of

sensory

information

to

behavioral

control

-LRB-

-RRB-

Our

results

suggest

that

synchronization

has

consequences

for

neuronal

interactions

providing

a

putative

mechanism

through

which

synchronization

contributes

to

cognitive

functions

References

and

Notes

C.

M.

Gray

P.

K

nig

A.

K.

Engel

W.

Singer

Nature

-LRB-

-RRB-

A.

Bragin

et

al.

J.

Neurosci

-LRB-

-RRB-

P.

Fries

J.

H.

Reynolds

A.

E.

Rorie

R.

Desimone

Science

-LRB-

-RRB-

J.

Fell

et

al.

Nat

Neurosci

-LRB-

-RRB-

B.

Pesaran

J.

S.

Pezaris

M.

Sahani

P.

P.

Mitra

R.

A.

Andersen

Nat

Neurosci

-LRB-

-RRB-

J.-M

Schoffelen

R.

Oostenveld

P.

Fries

Science

-LRB-

-RRB-

G.

Buzs

ki

Rhythms

of

the

Brain

-LRB-

Oxford

Univ.

Press

Oxford

-RRB-

H.

Markram

J.

L

bke

M.

Frotscher

B.

Sakmann

Science

-LRB-

-RRB-

G.

Q.

Bi

M.

M.

Poo

J.

Neurosci

-LRB-

-RRB-

V.

Wespatat

F.

Tennigkeit

W.

Singer

J.

Neurosci

-LRB-

-RRB-

P.

K

nig

A.

K.

Engel

W.

Singer

Trends

Neurosci

-LRB-

-RRB-

R.

Azouz

C.

M.

Gray

Neuron

-LRB-

-RRB-

E.

Salinas

T.

J.

Sejnowski

Nat

Rev.

Neurosci

-LRB-

-RRB-

P.

Fries

Trends

Cognit

Sci

-LRB-

-RRB-

A.

Hasenstaub

et

al.

Neuron

-LRB-

-RRB-

I.

Vida

M.

Bartos

P.

Jonas

Neuron

-LRB-

-RRB-

M.

Bartos

I.

Vida

P.

Jonas

Nat

Rev.

Neurosci

-LRB-

-RRB-

P.

Fries

P.

R.

Roelfsema

A.

K.

Engel

P.

K

nig

W.

Singer

Proc

Natl.

Acad

Sci

U.S.A.

-LRB-

-RRB-

P.

Fries

J.

H.

Schr

der

P.

R.

Roelfsema

W.

Singer

A.

K.

Engel

J.

Neurosci

-LRB-

-RRB-

T.

Womelsdorf

P.

Fries

P.

P.

Mitra

R.

Desimone

Nature

-LRB-

-RRB-

Materials

and

methods

are

available

as

supporting

material

on

Science

Online

Positive

and

negative

departures

from

the

good

phase

relation

toward

the

bad

phase

relation

were

pooled

because

our

previous

analyses

had

demonstrated

symmetric

effects

in

both

directions

P.

K

nig

A.

K.

Engel

P.

R.

Roelfsema

W.

Singer

Neural

Comput

-LRB-

-RRB-

J.

Csicsvari

B.

Jamieson

K.

D.

Wise

G.

Buzs

ki

Neuron

-LRB-

-RRB-

J.

Mishra

J.

M.

Fellous

T.

J.

Sejnowski

Neural

Networks

-LRB-

-RRB-

A.

K.

Engel

A.

K.

Kreiter

P.

K

nig

W.

Singer

Proc

Natl.

Acad

Sci

U.S.A.

-LRB-

-RRB-

G.

Buzs

ki

Z.

Horv

th

R.

Urioste

J.

Hetke

K.

Wise

Science

-LRB-

-RRB-

P.

R.

Roelfsema

A.

K.

Engel

P.

K

nig

W.

Singer

Nature

-LRB-

-RRB-

C.

Tallon-Baudry

S.

Mandon

W.

A.

Freiwald

A.

K.

Kreiter

Cereb

Cortex

-LRB-

-RRB-

J.

Gross

et

al.

Proc

Natl.

Acad

Sci

U.S.A.

-LRB-

-RRB-

We

thank

P.

K

nig

P.

R.

Roelfsema

and

J.

H.

Schr

der

for

help

during

the

cat

experiments

and

J.

H.

Reynolds

A.

E.

Rorie

and

A.

F.

Rossi

for

help

during

the

monkey

experiments

This

work

was

supported

by

the

Human

Frontier

Science

Program

and

the

Netherlands

Organization

for

Scientific

Research

-LRB-

P.F.

-RRB-

the

Volkswagen

Foundation

-LRB-

A.K.E.

and

P.F

-RRB-

the

Max

Planck

Society

-LRB-

P.F.

A.K.E.

and

W.S.

-RRB-

European

Union

grants

EU

and

EU

-LRB-

A.K.E.

-RRB-

and

NIH

grant

and

the

National

Institute

of

Mental

Health

Intramural

Research

Program

-LRB-

R.D.

-RRB-

Supporting

Online

Material

Materials

and

Methods

SOM

Text

Figs

to

References

January

accepted

May

science

Neural

Mechanisms

of

Visual

Attention

How

Top-Down

Feedback

Highlights

Relevant

Locations

Yuri

B.

Saalmann

Ivan

N.

Pigarev

Trichur

R.

Attention

helps

us

process

potentially

important

objects

by

selectively

increasing

the

activity

of

sensory

neurons

that

represent

the

relevant

locations

and

features

of

our

environment

This

selection

process

requires

top-down

feedback

about

what

is

important

in

our

environment

We

investigated

how

parietal

cortical

output

influences

neural

activity

in

early

sensory

areas

Neural

recordings

were

made

simultaneously

from

the

posterior

parietal

cortex

and

an

earlier

area

in

the

visual

pathway

the

medial

temporal

area

of

macaques

performing

a

visual

matching

task

When

the

monkey

selectively

attended

to

a

location

the

timing

of

activities

in

the

two

regions

became

synchronized

with

the

parietal

cortex

leading

the

medial

temporal

area

Parietal

neurons

may

thus

selectively

increase

activity

in

earlier

sensory

areas

to

enable

focused

spatial

attention

ttention

allows

us

to

engage

with

our

environment

by

selecting

information

relevant

for

behavior

-LRB-

-RRB-

This

enables

preferential

processing

of

particular

locations

in

the

visual

field

or

specific

features

of

objects

Attention

maintained

on

a

location

is

usually

referred

to

as

spatial

attention

and

that

on

a

A

Department

of

Optometry

and

Vision

Sciences

The

University

of

Melbourne

Parkville

Australia

for

Information

Transmission

Problems

Russian

Academy

of

Sciences

Bol

shoy

Karetniy

Moscow

Russia

To

whom

correspondence

should

be

addressed

E-mail

trv@unimelb.edu.au

feature

as

feature-based

attention

-LRB-

-RRB-

Both

types

of

attention

manifest

in

visual

cortical

areas

as

increased

activity

of

neurons

representing

the

attended

location

or

feature

and

reduced

activity

of

other

neurons

-LRB-

-RRB-

This

may

require

topdown

feedback

about

what

is

relevant

in

the

environment

however

such

feedback

has

not

been

empirically

demonstrated

There

is

evidence

-LRB-

-RRB-

that

the

posterior

parietal

cortex

-LRB-

PPC

-RRB-

is

critical

for

spatial

attention

The

PPC

is

a

higher-order

structure

along

the

dorsal

stream

of

visual

areas

-LRB-

Fig.

-RRB-

which

are

particularly

concerned

with

spatial

aspects

of

a

scene

It

has

been

suggested

that

the

spatial

information

about

VOL

SCIENCE

a

scene

extracted

by

the

PPC

forms

the

basis

for

feedback

signals

to

earlier

levels

of

the

visual

pathway

highlighting

spatial

locations

of

potential

interest

-LRB-

-RRB-

and

gating

responses

depending

upon

the

state

of

attention

We

simultaneously

measured

the

activity

in

a

part

of

the

macaque

PPC

called

the

lateral

intraparietal

area

-LRB-

LIP

-RRB-

and

the

immediately

earlier

stage

of

the

dorsal

pathway

the

medial

temporal

area

-LRB-

MT

Fig.

-RRB-

We

tested

whether

LIP

feedback

increases

MT

responses

to

attended

visual

stimuli

The

monkeys

performed

a

delayed

match-to-sample

-LRB-

DMS

-RRB-

task

which

manipulated

both

where

they

were

attending

and

what

stimulus

feature

they

were

attending

to

-LRB-

Fig.

-RRB-

-LRB-

-RRB-

We

recorded

pairs

of

neurons

from

MT

and

LIP

each

pair

having

overlapping

receptive

fields

-LRB-

RFs

-RRB-

and

the

same

preferred

orientation

Local

field

potentials

-LRB-

LFPs

-RRB-

from

the

two

sites

were

also

recorded

We

first

tested

whether

our

paradigm

resulted

in

increased

responses

of

MT

neurons

to

attended

stimuli

Figure

shows

the

effect

of

spatial

attention

on

a

single

MT

neuron

and

Fig.

the

average

population

response

For

both

data

sets

the

MT

response

to

the

second

stimulus

was

significantly

increased

in

the

spatial

and

featurebased

attention

and

spatial

attention

conditions

compared

to

the

neutral

control

When

attention

was

elsewhere

the

MT

response

to

the

second

stimulus

was

significantly

reduced

-LRB-

Holm

's

controlled

Wilcoxon

test

P

-RRB-

These

attentional

effects

on

MT

neurons

are

consistent

with

those

reported

in

other

types

of

cognitive

JUNE

Downloaded

from

on

May

REPORTS

tasks

and

other

cortical

areas

-LRB-

-RRB-

and

are

not

due

to

simple

stimulus

repetition

-LRB-

fig

-RRB-

If

LIP

neurons

code

attention

priorities

then

their

activity

should

differentiate

between

attention

conditions

Figure

C

and

D

show

the

activity

of

a

single

LIP

neuron

and

the

population

respectively

Both

show

a

significantly

increased

response

to

the

second

stimulus

with

spatial

and

feature-based

attention

compared

to

the

neutral

first

stimulus

but

a

significantly

reduced

response

when

attention

was

elsewhere

-LRB-

Holm

's

controlled

Wilcoxon

test

P

-RRB-

For

the

spatial

attention

condition

the

increased

response

to

the

second

stimulus

was

significantly

different

from

the

attention

elsewhere

control

though

not

the

neutral

control

The

activity

of

LIP

neurons

increased

through

the

delay

period

after

the

first

stimulus

with

the

overall

delay

period

activity

significantly

greater

in

those

cases

where

attention

included

the

RF

location

-LRB-

Holm

's

controlled

Wilcoxon

test

P

-RRB-

Because

LIP

activity

increased

before

the

MT

response

to

an

attended

stimulus

LIP

is

in

a

position

to

provide

feedback

to

MT.

If

LIP

causes

the

effect

of

attention

on

MT

then

the

activity

in

the

two

areas

should

be

correlated

and

spikes

from

LIP

neurons

should

be

closely

followed

by

spikes

from

MT

neurons

We

calculated

the

coherence

of

MT

and

LIP

activities

-LSB-

using

multi-taper

spectral

methods

-LRB-

-RRB-

-RSB-

which

measures

the

degree

of

association

between

two

oscillatory

processes

-LRB-

here

the

spike

trains

or

LFPs

in

MT

and

LIP

-RRB-

as

a

function

of

oscillation

frequency

We

generally

observed

increased

coherence

between

MT

and

LIP

LFPs

in

the

spatial

and

feature-based

attention

and

spatial

attention

conditions

-LRB-

Fig.

A

and

B

-RRB-

The

coherence

in

the

to

range

increased

when

the

first

stimulus

appeared

in

the

RF

It

was

also

significantly

elevated

during

the

delay

period

-LRB-

Student

's

t

test

P

-RRB-

increasing

just

before

the

second

stimulus

The

coherence

peaked

around

the

second

stimulus

and

remained

elevated

for

up

to

ms

around

the

stimulus

Figure

shows

the

coherence

when

the

first

stimulus

was

flashed

outside

the

RF

and

thus

spatial

attention

was

not

drawn

to

the

receptive-field

location

The

coherence

is

much

weaker

in

this

case

particularly

around

the

second

stimulus

Figure

shows

the

average

coherence

of

the

population

of

paired

recordings

for

the

two

attention

conditions

and

two

control

states

The

coherence

was

significantly

greater

-LRB-

Holm

's

controlled

Wilcoxon

test

P

-RRB-

when

attention

was

focused

on

the

receptive-field

location

compared

to

the

neutral

and

attention

elsewhere

controls

The

significant

coherence

of

LFPs

in

MT

and

LIP

during

spatial

attention

means

that

there

was

correlated

activity

between

ensembles

of

MT

and

LIP

neurons

To

determine

the

relative

timing

of

action

potentials

between

the

two

areas

we

calculated

the

coherence

between

simultaneously

recorded

spike

trains

from

single

neurons

in

MT

and

LIP

-LRB-

to

ms

after

stimulus

onset

-RRB-

The

coherence

between

the

spikes

elicited

by

MT

and

LIP

neurons

was

generally

low

but

nonetheless

significantly

above

zero

-LRB-

Student

's

t

test

P

-RRB-

in

the

gammafrequency

range

for

of

neuron

pairs

The

lower

coherence

between

spike

trains

than

between

LFPs

is

expected

because

any

particular

sampled

pair

of

neurons

has

a

low

probability

of

being

strongly

connected

Nevertheless

the

spatial

and

feature-based

attention

and

spatial

attention

conditions

produced

significant

coherence

-LRB-

Fig.

-RRB-

In

contrast

there

were

no

cases

of

significant

coherence

in

the

neutral

and

attention

elsewhere

controls

If

LIP

has

a

top-down

influence

on

MT

responses

during

focal

attention

then

the

phase

of

the

coherence

should

show

LIP

leading

MT.

Figure

shows

the

phase

when

the

coherence

was

significantly

above

zero

which

occurred

only

during

the

two

attention

conditions

The

phase

of

the

peak

coherence

showed

the

LIP

preceding

MT

by

ms

for

the

spatial

Fig.

Attention

increased

activity

in

LIP

before

MT.

Examples

of

single-neuron

activity

-LRB-

SE

-RRB-

in

the

MT

-LRB-

A

-RRB-

and

LIP

-LRB-

C

-RRB-

during

the

DMS

task

with

interstimulus

delay

Three

types

of

trials

are

colorcoded

red

-LRB-

neutral

then

spatial

and

featurebased

attention

on

-RRB-

green

-LRB-

spatial

attention

on

-RRB-

and

blue

-LRB-

attention

elsewhere

for

-RRB-

Population

activity

in

the

MT

-LRB-

B

-RRB-

and

LIP

-LRB-

D

-RRB-

represents

the

average

of

cells

for

each

area

simultaneously

recorded

pairs

from

each

of

two

monkeys

recorded

at

delay

The

percentage

change

-LRB-

SE

-RRB-

in

the

population

response

-LRB-

to

ms

after

stimulus

onset

-RRB-

of

the

MT

-LSB-

-LRB-

B

-RRB-

right

-RSB-

and

LIP

-LSB-

-LRB-

D

-RRB-

right

-RSB-

evoked

by

compared

to

neutral

shown

are

the

combined

data

from

cells

at

delay

and

cells

at

delay

SCIENCE

VOL

JUNE

Downloaded

from

on

May

Fig.

The

experimental

paradigm

-LRB-

A

-RRB-

Areas

MT

and

LIP

are

connected

as

shown

We

simultaneously

recorded

from

the

MT

and

LIP

while

the

monkey

performed

the

DMS

task

-LRB-

B

-RRB-

The

monkey

is

required

to

match

both

the

orientation

and

location

of

two

stimulus

gratings

to

obtain

a

reward

The

monkey

maintained

fixation

throughout

each

trial

while

we

manipulated

his

attentional

state

Two

attention

conditions

were

compared

to

two

controls

When

both

gratings

-LRB-

and

-RRB-

have

the

neurons

preferred

orientation

and

both

appear

at

the

RF

location

-LRB-

here

the

lower

left

quadrant

-RRB-

the

period

after

onset

of

is

the

spatial

and

feature-based

attention

condition

-LRB-

left

cascade

-RRB-

When

and

are

both

at

the

RF

but

has

the

nonpreferred

orientation

and

the

preferred

the

period

after

onset

of

is

the

spatial

attention

condition

-LRB-

middle

cascade

-RRB-

The

two

controls

are

the

attention

elsewhere

state

which

is

the

period

after

onset

of

when

is

outside

the

RF

and

preferred-orientation

is

at

the

RF

-LRB-

right

cascade

-RRB-

and

the

neutral

state

the

period

after

onset

of

when

preferred-orientation

is

at

the

RF

and

has

not

yet

been

presented

-LRB-

left

cascade

-RRB-

FP

fixation

point

REPORTS

and

feature-based

attention

condition

and

by

ms

for

the

spatial

attention

condition

-LRB-

mean

SE

of

the

of

neuron

pairs

showing

significant

coherence

-RRB-

This

phase

relationship

is

physiologically

plausible

for

feedback

from

the

LIP

to

MT

assuming

a

conduction

velocity

of

m/s

-LRB-

-RRB-

for

intracortical

connections

To

ensure

that

the

coherence

we

saw

was

due

to

within-trial

physiological

interactions

we

shifted

across

time

the

LIP

spike

train

relative

to

the

MT

train

by

integer

multiples

of

trials

for

each

recording

session

and

recalculated

the

coherence

-LRB-

Fig.

-RRB-

This

control

abolished

the

attention-enhanced

coherence

We

next

tested

whether

LIP

spikes

preceded

enough

MT

spikes

to

cause

the

increased

MT

activity

during

spatial

attention

We

observed

a

significant

increase

in

the

percentage

of

MT

spikes

preceded

by

LIP

spikes

in

the

spatial

attention

conditions

compared

with

the

neutral

and

attention

elsewhere

controls

-LRB-

Holm

's

controlled

Wilcoxon

test

P

Fig.

-RRB-

The

magnitude

of

this

effect

-LRB-

percentage

of

MT

spikes

preceded

by

LIP

spikes

within

ms

spatial

and

featural

attention

spatial

attention

-RRB-

could

potentially

account

for

a

substantial

amount

of

the

increase

in

MT

activity

-LRB-

spatial

and

featural

attention

spatial

attention

-RRB-

However

a

greater

increase

in

LIP

activity

relative

to

MT

activity

could

lead

to

the

results

in

Fig.

without

LIP

feedback

to

MT.

This

possibility

is

discounted

by

the

finding

of

a

significant

increase

in

the

percentage

of

LIP

spikes

followed

by

MT

spikes

with

attention

-LRB-

Holm

's

controlled

Wilcoxon

test

P

Fig.

-RRB-

Both

increased

coherence

of

oscillatory

LFPs

and

LIP

spikes

preceding

MT

spikes

in

the

attention

conditions

are

evident

in

the

raw

data

from

single

trials

-LRB-

fig

-RRB-

Synchronization

between

LIP

neurons

may

be

a

fundamental

mechanism

ensuring

that

the

output

from

LIP

neurons

has

an

increased

impact

on

sensory

areas

such

as

MT.

We

calculated

the

spike-field

coherence

in

LIP

which

indicates

the

degree

of

synchronization

between

spike

times

and

the

LFP

The

mean

spike-field

coherence

between

and

Hz

was

significantly

increased

in

the

two

spatial

attention

conditions

-LRB-

Fig.

-RRB-

compared

to

the

attention

elsewhere

control

-LRB-

Holm

's

controlled

Wilcoxon

test

P

-RRB-

This

suggests

that

spike

timing

in

addition

to

spike

rate

may

be

important

for

increased

efficacy

of

attentional

feedback

Our

results

show

that

LIP

feedback

can

account

for

attention-enhanced

MT

responses

This

feedback

manifests

in

the

coherent

activities

of

MTand

LIP

neurons

within

the

gamma-frequency

range

-LRB-

to

Hz

-RRB-

supporting

the

role

of

gamma

synchronization

in

information

processing

-LRB-

-RRB-

The

phase

of

the

observed

coherence

is

such

that

LIP

feedback

can

potentially

arrive

at

MT

during

a

depolarizing

phase

of

membrane-potential

oscillations

increasing

the

probability

of

spike

generation

Synchronization

of

feedback

may

also

increase

sensory

activity

during

attention

The

response

of

LIP

neurons

to

the

second

stimulus

of

preferred

orientation

depended

upon

whether

the

first

stimulus

though

at

the

same

location

was

of

the

preferred

or

orthogonal

orientation

In

MT

neurons

however

there

was

no

significant

difference

in

response

to

the

second

Fig.

Coherent

neural

activity

between

MT

and

LIP

The

coherence

-LRB-

color-coded

-RRB-

of

the

MT

LFP

and

LIP

LFP

from

a

pair

of

recording

sites

during

the

DMS

task

The

coherence

was

calculated

in

successive

windows

with

a

step

size

of

ms.

is

the

preferred

stimulus

in

the

RF

and

is

the

same

in

each

panel

-LRB-

A

-RRB-

and

match

for

location

and

orientation

-LRB-

B

-RRB-

and

match

for

location

only

and

-LRB-

C

-RRB-

and

differ

in

location

-LRB-

D

-RRB-

Population

average

of

the

transformed

coherence

-LRB-

-RRB-

between

the

MT

LFP

and

LIP

LFP

to

ms

after

stimulus

onset

-LRB-

solid

lines

-RRB-

and

the

control

where

the

LIP

LFP

was

shifted

relative

to

the

MT

LFP

-LRB-

dotted

lines

-RRB-

Fig.

Synchronized

LIP

feedback

to

MT

during

attention

-LRB-

A

-RRB-

Coherence

of

spikes

from

a

pair

of

LIP

and

MT

neurons

to

ms

after

stimulus

onset

Color

coding

as

in

Fig.

-LRB-

B

-RRB-

Phase

of

significant

coherence

between

the

pair

of

neurons

in

-LRB-

A

-RRB-

Only

two

traces

are

shown

because

neither

control

showed

significant

coherence

in

the

gamma

range

-LRB-

C

-RRB-

Relative

shifts

between

spike

trains

by

integer

multiples

of

trials

abolished

attention-enhanced

coherence

compare

with

-LRB-

A

-RRB-

-LRB-

D

-RRB-

Population

median

of

the

percentage

of

MT

spikes

preceded

by

LIP

spikes

in

the

ms

after

stimulus

onset

-LRB-

E

-RRB-

Population

median

of

the

percentage

of

LIP

spikes

followed

by

MT

spikes

in

the

ms

after

stimulus

onset

-LRB-

F

-RRB-

Population

average

of

the

transformed

spike-field

coherence

in

LIP

-LRB-

solid

lines

-RRB-

Increased

coherence

is

seen

for

the

two

attention

conditions

in

the

gamma

range

Shifting

spike

trains

relative

to

the

LFP

in

LIP

abolished

attention-enhanced

coherence

-LRB-

dotted

lines

-RRB-

VOL

SCIENCE

JUNE

Downloaded

from

on

May

REPORTS

stimulus

between

these

two

attention

conditions

This

is

consistent

with

the

idea

that

the

parietal

cortex

uses

both

spatial

and

feature-based

information

to

determine

purely

spatial

priorities

for

its

feedback

-LRB-

-RRB-

Such

a

scheme

provides

a

neural

framework

for

guided

search

models

of

attention

-LRB-

-RRB-

and

is

consistent

with

feedback

to

auditory

and

somatosensory

systems

-LRB-

-RRB-

being

spatial

The

dorsal

and

ventral

cortical

pathways

are

said

to

represent

the

spatial

and

feature-based

aspects

of

a

visual

scene

respectively

and

LIP

is

part

of

the

dorsal

pathway

However

the

feature

selectivity

shown

by

LIP

neurons

in

our

and

other

studies

-LRB-

-RRB-

means

that

LIP

could

be

involved

in

processing

object

features

through

its

direct

connections

with

the

ventral

pathway

-LRB-

-RRB-

or

by

gating

neuronal

activity

at

the

level

of

via

MT

-LRB-

-RRB-

The

attentional

modulation

of

activity

in

ventral

cortical

areas

-LRB-

-RRB-

and

even

in

-LRB-

-RRB-

may

have

its

origin

in

LIP

as

the

gain

controller

References

and

Notes

A.

M.

Treisman

G.

Gelade

Cognit

Psychol

-LRB-

-RRB-

R.

Desimone

J.

Duncan

Annu

Rev.

Neurosci

-LRB-

-RRB-

J.

M.

Wolfe

Psychon

Bull

Rev.

-LRB-

-RRB-

S.

Yantis

J.

T.

Serences

Curr

Opin

Neurobiol

-LRB-

-RRB-

J.

H.

R.

Maunsell

S.

Treue

Trends

Neurosci

-LRB-

-RRB-

M.

C.

Bushnell

M.

E.

Goldberg

D.

L.

Robinson

J.

Neurophysiol

-LRB-

-RRB-

J.

Moran

R.

Desimone

Science

-LRB-

-RRB-

B.

C.

Motter

J.

Neurophysiol

-LRB-

-RRB-

S.

Treue

J.

H.

R.

Maunsell

Nature

-LRB-

-RRB-

T.

R.

Vidyasagar

Neuroreport

-LRB-

-RRB-

J.

W.

Bisley

M.

E.

Goldberg

Science

-LRB-

-RRB-

J.

A.

Brefczynski

E.

A.

DeYoe

Nat

Neurosci

-LRB-

-RRB-

D.

C.

Somers

A.

M.

Dale

A.

E.

Seiffer

R.

B.

H.

Tootell

Proc

Natl.

Acad

Sci

U.S.A.

-LRB-

-RRB-

S.

Kastner

P.

De

Weerd

R.

Desimone

L.

G.

Ungerleider

Science

-LRB-

-RRB-

M.

M.

Mesulam

Ann

Neurol

-LRB-

-RRB-

M.

Corbetta

F.

M.

Miezin

G.

L.

Shulman

S.

E.

Petersen

J.

Neurosci

-LRB-

-RRB-

M.

A.

Steinmetz

C.

Constantinidis

Cereb

Cortex

-LRB-

-RRB-

T.

R.

Vidyasagar

Brain

Res

Rev.

-LRB-

-RRB-

J.

Bullier

Brain

Res

Rev.

-LRB-

-RRB-

Materials

and

methods

are

available

as

supporting

material

on

Science

Online

P.

P.

Mitra

B.

Pesaran

Biophys

J.

-LRB-

-RRB-

M.

R.

Jarvis

P.

P.

Mitra

Neural

Comput

-LRB-

-RRB-

J.

Bullier

M.

E.

McCourt

G.

H.

Henry

Exp

Brain

Res

-LRB-

-RRB-

R.

Eckhorn

et

al.

Biol

Cybern

-LRB-

-RRB-

W.

Singer

C.

M.

Gray

Annu

Rev.

Neurosci

-LRB-

-RRB-

T.

J.

Sejnowski

O.

Paulsen

J.

Neurosci

-LRB-

-RRB-

G.

J.

Blatt

R.

A.

Andersen

G.

R.

Stoner

J.

Comp

Neurol

-LRB-

-RRB-

J.

W.

Lewis

D.

C.

Van

Essen

J.

Comp

Neurol

-LRB-

-RRB-

J.

Gottlieb

M.

Kusunoki

M.

E.

Goldberg

Nature

-LRB-

-RRB-

P.

F.

Balan

J.

Gottlieb

J.

Neurosci

-LRB-

-RRB-

We

thank

P.

R.

Martin

J.

Victor

J.

Bisley

and

L.

Horowitz

for

useful

comments

E.

Henry

and

E.

Duff

for

programming

assistance

J.

Cappello

for

help

training

monkeys

and

the

Department

of

Anatomy

and

Cell

Biology

University

of

Melbourne

for

laboratory

facilities

Supported

by

the

National

Health

and

Medical

Research

Council

and

Australian

Research

Council

Supporting

Online

Material

Materials

and

Methods

Figs

and

References

December

accepted

May

science

a-Klotho

as

a

Regulator

of

Calcium

Homeostasis

Akihiro

Imura

Yoshihito

Tsuji

Miyahiko

Murata

Ryota

Maeda

Koji

Kubota

Akiko

Iwano

Chikashi

Obuse

Kazuya

Togashi

Makoto

Tominaga

Naoko

Kita

Ken-ichi

Tomiyama

Junko

Iijima

Yoko

Nabeshima

Makio

Fujioka

Ryo

Asato

Shinzo

Tanaka

Ken

Kojima

Juichi

Ito

Kazuhiko

Nozaki

Nobuo

Hashimoto

Tetsufumi

Ito

Takeshi

Nishio

Takashi

Uchiyama

Toshihiko

Fujimori

Yo-ichi

a-klotho

was

identified

as

a

gene

associated

with

premature

aging

like

phenotypes

characterized

by

short

lifespan

In

mice

we

found

the

molecular

association

of

a-Klotho

-LRB-

a-Kl

-RRB-

and

K

adenosine

triphosphatase

-LRB-

K

ATPase

-RRB-

and

provide

evidence

for

an

increase

of

abundance

of

K

ATPase

at

the

plasma

membrane

Low

concentrations

of

extracellular

free

calcium

-LRB-

-LSB-

-RSB-

e

-RRB-

rapidly

induce

regulated

parathyroid

hormone

-LRB-

PTH

-RRB-

secretion

in

an

a-Kl

and

K

ATPase

dependent

manner

The

increased

gradient

created

by

K

ATPase

activity

might

drive

the

transepithelial

transport

of

in

cooperation

with

ion

channels

and

transporters

in

the

choroid

plexus

and

the

kidney

Our

findings

reveal

fundamental

roles

of

a-Kl

in

the

regulation

of

calcium

metabolism

lotho

mutant

mice

are

short-lived

and

the

gene

responsible

for

the

phenotype

is

called

klotho

-LRB-

-RRB-

A

homolog

has

also

been

identified

and

named

b-klotho

-LRB-

-RRB-

To

avoid

confusion

we

refer

to

the

original

gene

as

a-klotho

The

a-klotho

-LRB-

a-kl

-RRB-

gene

encodes

a

type

I

membrane

protein

with

considerable

similarity

to

b-glycosidase

that

is

predominantly

expressed

in

tissues

that

are

involved

with

calcium

homeostasis

that

is

the

parathyroid

glands

kidney

and

choroid

plexus

-LRB-

-RRB-

-LRB-

supporting

description

-RRB-

Although

a-Kl

has

been

predicted

to

be

present

on

the

cell

surface

large

amounts

of

a-Kl

are

detectable

in

the

cytoplasm

and

the

cleaved

extracellular

domain

is

secreted

into

the

blood

and

cerebrospinal

fluid

-LRB-

CSF

-RRB-

-LRB-

-RRB-

In

this

paper

we

show

a

complex

-LRB-

Fig.

-RRB-

These

molecules

also

associated

in

mouse

kidney

and

in

human

parathyroid

glands

-LRB-

Fig.

C

and

D

-RRB-

In

these

tissues

the

majority

of

a-Kl

immunoreactivity

was

detectable

in

the

cytoplasm

whereas

K

ATPase

immunoreactivity

was

observed

at

or

near

the

cell

surface

and

diffusely

in

the

cytoplasm

-LRB-

fig

-RRB-

We

verified

the

above

histological

observations

by

the

surface

biotinylation

and

subcellular

fractionation

using

the

choroid

plexus

and

the

HeLa

cells

introduced

with

both

a-Kl

and

K

ATPase

fused

with

enhanced

green

fluorescence

protein

-LRB-

K

ATPase-EGFP

-RRB-

respectively

a-Kl

was

primarily

detected

in

the

nonbiotinylated

Department

of

Pathology

and

Tumor

Biology

Graduate

School

of

Medicine

Kyoto

University

Kyoto

Japan

Medical

Research

Organization

Graduate

School

of

Medicine

Kyoto

University

Kyoto

Japan

Brain

Science

Graduate

School

of

Medicine

Kyoto

University

Kyoto

Japan

Department

of

Otolaryngology

Head

and

Neck

Surgery

Graduate

School

of

Medicine

Kyoto

University

Kyoto

Japan

of

Neurosurgery

Graduate

School

of

Medicine

Kyoto

University

Kyoto

Japan

of

Hematology

and

Oncology

Graduate

School

of

Medicine

Kyoto

University

Kyoto

Japan

Microscopy

Center

Graduate

School

of

Medicine

Kyoto

University

Kyoto

Japan

Core

Research

for

Evolutional

Science

and

Technology

Japan

Science

and

Technology

Corporation

Saitama

Japan

of

Functional

Networks

for

Chromosome

Inheritance

Graduate

School

of

Life

Science

Hokkaido

University

Sapporo

Japan

of

Cell

Signaling

Okazaki

Institute

for

Integrative

Bioscience

National

Institutes

of

Natural

Sciences

Aichi

Japan

of

Anatomy

Faculty

of

Medical

Sciences

University

of

Fukui

Fukui

Japan

K

pivotal

role

of

a-Kl

in

calcium

homeostasis

-LRB-

mouse

breeding

conditions

are

described

in

supporting

description

and

fig

-RRB-

We

identified

the

subunit

of

K+ATP

ase

-LRB-

K

ATPase

-RRB-

as

an

a-Kl

binding

protein

-LRB-

-RRB-

-LRB-

supporting

description

-RRB-

and

further

confirmed

the

binding

by

Western

blot

analysis

and

with

reciprocal

immunoprecipitation

-LRB-

Fig.

A

and

B

-RRB-

a-Kl

precipitated

by

monoclonal

antibody

to

K

ATPase

contained

proteins

that

migrated

as

two

bands

of

and

kD

indicating

that

K

ATPase

binds

to

a-Kl

regardless

of

its

sugar

moieties

-LRB-

Fig.

-RRB-

-LRB-

-RRB-

The

b

subunit

of

K

ATPase

which

has

a

major

role

in

the

regulation

of

membrane

recruitment

of

K

ATPase

-LRB-

-RRB-

was

included

in

the

a-Kl-Na

K

ATPase

SCIENCE

VOL

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O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B B O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O B O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O B O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O B O O O O O O O O B O O B O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O B O O O B O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O B O O O O B O O O O O O O O O O O O O B O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O B O O O O O O O O B O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O B O O O O B O O O O O O B O O O O O O O O B O B O O O O B O B O O O O O O O O O O O O O O B O O O O O O O O B O O O O O O O B O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O B O O O O O O O O O O O O O O O B O B O O O O O O O B O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O B O O O O O O O O O O B O B O O B O O O O O O O O O B O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O B O O O O O O O O O O O O O O O O O B O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O B O O O O O B O O O B O O O O O O O O O B O B O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O B O B O O O O O O O O O O O B O O O B O B O O O O O O O O O B O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O B O O O O O O O O O B O O O O O O O O O O B O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O B O O O O O O O O O O B O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O B O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O B O O O O O B O O O B O O O O O O O O O O B O O O B O O O O B O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O B O O O O O O O O B O O O O O B O O O O O O O O O O O O O O O B O O O O O B O O O O O B O O O O O O O O O O O B O O O O B O O O O O O O O O O O B O O B O O O O O O O O O O O O O O O B O O O B O O B O O O O O O O O O O O O O O O O O O O O O O B O O B O O O B O O O O O O O O O O O O O O O O B O B O O O O O O O O O O O B O O O O O O O O O O B O O O O O O B O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O B O O O O O O O O O O O B O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O B O O O O O B O O O O O O O O O O O O O O O B O O O O O O O O B O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O B O B O O O O O O O O B O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O B O O O O O O O O O O O O O O O O O O O O B O O O O O O B O O O O O O O O O O B O O B O B O O O O O O O O O O O B O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O B O O O O O O O O O O O O O O O O O O O B O O O B O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O B O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O B O O O O O O O O O O O O O O B O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O


Do

Infants

Understand

False

Beliefs

Kristine

H.

Onishi

et

al.

Science

-LRB-

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We

thank

M.

Davis

for

critical

review

of

the

manuscript

Y.

Konigshofer

K.

Jensen

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October

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February

science

Do

Infants

Understand

False

Beliefs

Kristine

H.

and

Renee

For

more

than

two

decades

researchers

have

argued

that

young

children

do

not

understand

mental

states

such

as

beliefs

Part

of

the

evidence

for

this

claim

comes

from

preschoolers

failure

at

verbal

tasks

that

require

the

understanding

that

others

may

hold

false

beliefs

Here

we

used

a

novel

nonverbal

task

to

examine

infants

ability

to

predict

an

actor

's

behavior

on

the

basis

of

her

true

or

false

belief

about

a

toy

's

hiding

place

Results

were

positive

supporting

the

view

that

from

a

young

age

children

appeal

to

mental

states

goals

perceptions

and

beliefs

to

explain

the

behavior

of

others

Consider

the

following

situation

A

child

who

has

surreptitiously

eaten

the

last

cookies

in

a

box

sees

her

brother

reach

into

the

box

To

make

sense

of

his

behavior

she

must

understand

that

he

falsely

believes

the

box

still

contains

cookies

As

adults

we

readily

understand

that

others

may

hold

and

act

on

false

beliefs

this

ability

is

widely

held

to

be

a

cornerstone

of

social

competence

and

its

neuronal

correlates

have

recently

begun

to

be

examined

-LRB-

-RRB-

What

are

the

origins

of

this

ability

Within

the

field

of

psychology

there

has

been

a

longstanding

controversy

regarding

this

issue

-LRB-

-RRB-

Some

researchers

have

suggested

that

at

about

years

of

age

a

fundamental

change

occurs

in

understanding

of

others

behavior

or

Btheory

of

mind

-LSB-

They

begin

to

realize

that

mental

states

such

as

beliefs

are

not

direct

reflections

of

reality

which

must

always

be

accurate

but

representations

which

may

or

may

not

be

accurate

-LRB-

-RRB-

Part

of

the

evidence

for

this

change

from

a

nonrepresentational

to

a

representational

theory

of

mind

has

come

from

young

well-documented

failure

at

false-belief

tasks

-LRB-

i.e.

tasks

that

require

the

understanding

that

others

may

hold

and

act

on

false

beliefs

-RRB-

-LRB-

-RRB-

In

a

standard

task

-LRB-

-RRB-

children

listen

to

a

story

as

it

is

enacted

with

dolls

and

toys

The

first

character

hides

a

toy

in

one

location

and

leaves

the

room

while

she

is

gone

a

second

character

hides

the

toy

in

a

different

location

When

Department

of

Psychology

McGill

University

Montreal

Quebec

Canada

of

Psychology

University

of

Illinois

Champaign

IL

USA

asked

where

the

first

character

will

look

for

her

toy

year

olds

typically

say

she

will

look

in

the

first

location

and

provide

appropriate

justifications

for

their

answers

In

contrast

most

year

olds

say

she

will

look

in

the

second

-LRB-

actual

-RRB-

location

thus

failing

to

demonstrate

an

understanding

that

the

first

character

will

hold

a

false

belief

about

the

location

Other

researchers

have

suggested

that

a

representational

theory

of

mind

is

present

much

earlier

and

that

young

difficulties

with

the

standard

false-belief

task

stem

primarily

from

excessive

linguistic

computational

and

other

task

demands

-LRB-

-RRB-

Support

for

these

claims

comes

in

part

from

evidence

that

year

olds

and

even

some

year

olds

succeed

at

a

modified

false-belief

task

-LRB-

-RRB-

In

this

version

of

the

task

after

listening

to

the

story

and

watching

it

enacted

children

are

simply

probed

by

the

experimenter

to

look

where

the

first

character

will

search

for

her

toy

upon

her

return

-LRB-

BI

wonder

where

she

will

look

-LSB-

-RRB-

Most

children

look

to

the

correct

location

suggesting

that

they

possess

some

implicit

understanding

that

others

may

hold

and

act

on

false

beliefs

We

examined

whether

infants

tested

with

a

simpler

entirely

nonverbal

task

would

also

show

some

implicit

understanding

of

false

belief

We

used

the

violation-of-expectation

method

which

has

been

used

extensively

to

investigate

infants

understanding

of

others

goals

-LRB-

-RRB-

For

example

in

one

experiment

-LRB-

-RRB-

infants

were

familiarized

with

an

actor

reaching

for

and

grasping

one

of

two

toys

-LRB-

defined

as

the

target

toy

-RRB-

Next

the

locations

of

the

two

toys

were

reversed

and

the

actor

reached

for

the

target

or

the

nontarget

toy

The

infants

looked

reliably

longer

at

nontarget

reaches

This

and

control

results

suggested

that

the

infants

encoded

the

target

toy

as

the

goal

object

expected

her

to

reach

for

it

in

its

new

location

and

responded

with

increased

attention

when

she

did

not

Similar

results

were

found

when

the

target

toy

was

hidden

rather

than

visible

and

was

retrieved

by

meansend

action

sequences

rather

than

by

a

simple

reach

-LRB-

-RRB-

Our

research

built

on

these

results

In

our

experiment

infants

first

watched

an

actor

hide

a

toy

in

one

of

two

locations

Next

a

change

occurred

that

resulted

in

the

actor

holding

either

a

true

or

a

false

belief

about

the

location

The

experiment

asked

whether

the

infants

would

expect

the

actor

to

search

for

her

toy

based

on

her

belief

about

its

location

whether

that

belief

was

true

or

false

Fig.

Events

shown

during

-LRB-

A

-RRB-

the

first

familiarization

and

-LRB-

B

-RRB-

the

second

and

third

familiarization

trials

The

light

gray

box

represents

the

yellow

box

the

dark

gray

box

represents

the

green

box

To

whom

correspondence

should

be

addressed

E-mail

kris.onishi@mcgill.ca

SCIENCE

VOL

APRIL

Downloaded

from

on

May

REPORTS

The

infants

first

received

three

familiarization

trials

-LRB-

Fig.

-RRB-

At

the

start

of

the

first

trial

a

toy

watermelon

slice

rested

on

the

apparatus

floor

between

two

boxes

one

yellow

and

one

green

the

boxes

openings

faced

each

other

and

were

covered

with

fringe

An

actor

-LRB-

wearing

a

beige

visor

and

a

denim

shirt

-RRB-

opened

doors

in

the

back

wall

of

the

apparatus

grasped

the

toy

played

with

it

for

a

few

seconds

and

then

hid

it

inside

the

green

box

After

this

pretrial

the

actor

paused

with

her

hand

inside

the

box

until

the

trial

ended

-LRB-

a

curtain

was

lowered

in

front

of

the

apparatus

between

trials

-RRB-

During

the

second

and

third

familiarization

trials

the

actor

opened

the

doors

reached

inside

the

green

box

-LRB-

as

though

to

grasp

the

toy

she

had

previously

hidden

there

-RRB-

and

then

paused

until

the

trial

ended

In

all

trials

looking

times

during

the

pretrial

and

paused

portions

of

the

trial

were

computed

separately

Next

the

infants

received

a

single

beliefinduction

trial

-LRB-

Fig.

-RRB-

During

this

trial

the

infants

witnessed

a

change

that

resulted

in

the

actor

holding

a

true

or

a

false

belief

about

the

location

There

were

four

versions

of

this

trial

designed

to

yield

two

true-belief

-LRB-

TB

-RRB-

and

two

false-belief

-LRB-

FB

-RRB-

conditions

The

actor

could

believe

truly

or

falsely

that

the

toy

was

hidden

in

the

green

or

in

the

yellow

box

In

the

TB-green

condition

the

actor

was

induced

to

have

a

true

belief

that

the

toy

was

in

the

green

box

The

upper

halves

of

the

doors

in

the

back

wall

of

the

apparatus

were

open

The

actor

leaned

into

this

opening

and

watched

as

the

yellow

box

moved

half

the

distance

toward

the

green

box

and

then

returned

to

its

original

position

the

infant

and

the

actor

thus

observed

no

change

in

the

location

and

could

assume

that

it

remained

in

the

green

box

In

the

TByellow

condition

the

actor

watched

through

the

opening

in

the

back

wall

as

the

toy

moved

from

the

green

into

the

yellow

box

thus

both

the

infant

and

the

actor

saw

the

toy

change

location

The

FB-green

condition

was

identical

to

the

TB-yellow

condition

except

that

the

opening

in

the

back

wall

remained

shut

throughout

the

trial

because

only

the

infant

saw

the

toy

move

into

the

yellow

box

the

actor

should

have

a

false

belief

about

the

location

The

FB-yellow

condition

began

as

in

the

TB-yellow

condition

The

actor

watched

through

the

opening

in

the

back

wall

as

the

toy

moved

from

the

green

to

the

yellow

box

Next

the

actor

shut

the

opening

and

then

the

toy

returned

to

the

green

box

thus

only

the

infant

observed

the

second

displacement

leaving

the

actor

with

a

false

belief

that

the

toy

was

still

in

the

yellow

box

In

each

condition

following

the

pretrial

the

infants

watched

the

final

paused

scene

until

the

trial

ended

All

but

five

infants

-LRB-

distributed

among

three

conditions

-RRB-

looked

continuously

during

the

pretrial

which

lasted

either

s

-LRB-

TB-green

TB

Fig.

Events

shown

during

the

belief-induction

trial

in

the

-LRB-

A

-RRB-

TB-green

condition

-LRB-

B

-RRB-

TB-yellow

condition

-LRB-

C

-RRB-

FB-green

condition

and

-LRB-

D

-RRB-

FB-yellow

condition

yellow

and

FB-green

-RRB-

or

s

-LRB-

FB-yellow

-RRB-

the

maximum

time

spent

looking

away

for

any

individual

was

s

The

infants

were

thus

very

attentive

throughout

the

pretrial

After

the

belief-induction

trial

the

infants

received

a

single

test

trial

-LRB-

Fig.

-RRB-

For

half

of

the

infants

in

each

belief

condition

the

actor

opened

the

doors

reached

into

the

green

box

and

paused

until

the

trial

ended

-LRB-

green-box

condition

-RRB-

for

the

other

infants

the

event

was

the

same

except

that

the

actor

reached

into

the

yellow

box

-LRB-

yellow-box

condition

-RRB-

Our

predictions

for

the

test

trial

were

as

follows

If

the

infants

expected

the

actor

to

search

for

her

toy

on

the

basis

of

her

belief

about

its

location

rather

than

on

the

basis

of

-LRB-

their

knowledge

of

-RRB-

its

actual

location

then

they

should

look

reliably

longer

when

that

expectation

was

violated

Thus

when

the

actor

VOL

SCIENCE

had

a

true

belief

that

the

toy

was

hidden

in

the

green

box

the

infants

should

expect

her

to

reach

into

that

box

and

they

should

look

reliably

longer

when

she

reached

into

the

yellow

box

instead

conversely

when

the

actor

had

a

true

belief

that

the

toy

was

hidden

in

the

yellow

box

the

infants

should

look

reliably

longer

when

she

searched

the

green

as

opposed

to

the

yellow

box

Exactly

the

same

predictions

held

when

the

actor

had

a

false

belief

about

the

location

The

infants

should

look

reliably

longer

at

the

yellow-box

event

when

the

actor

falsely

believed

that

the

toy

was

hidden

in

the

green

box

and

at

the

green-box

event

when

she

falsely

believed

that

the

toy

was

hidden

in

the

yellow

box

Within

both

the

true

and

the

false-belief

conditions

an

interaction

was

thus

predicted

between

the

belief

about

the

location

APRIL

Downloaded

from

on

May

REPORTS

be

used

to

predict

the

behavior

rather

than

guide

their

own

We

prefer

our

interpretation

to

the

alternative

interpretation

just

discussed

for

two

reasons

The

first

is

theoretical

Similar

to

other

researchers

-LRB-

-RRB-

we

assume

that

children

are

born

with

an

abstract

computational

system

that

guides

their

interpretation

of

others

behavior

In

this

view

even

young

children

appeal

to

others

mental

states

goals

perceptions

and

beliefs

to

make

sense

of

their

actions

development

involves

primarily

learning

which

states

underlie

which

actions

and

not

coming

to

understand

that

such

states

exist

at

all

The

second

reason

is

empirical

Recent

results

of

ours

have

indicated

that

infants

can

predict

where

an

actor

will

search

for

a

hidden

toy

even

when

she

does

not

see

it

disappear

but

must

infer

its

location

based

on

various

-LRB-

useful

or

misleading

-RRB-

cues

-LRB-

-RRB-

To

explain

these

and

the

present

results

it

is

more

parsimonious

to

assume

that

infants

attribute

to

others

beliefs

that

can

be

shaped

and

updated

by

multiple

sources

of

information

than

to

assume

that

infants

form

an

extensive

series

of

superficial

expectations

linking

different

perceptions

to

different

actions

In

short

we

propose

that

the

present

results

suggest

that

infants

expect

an

actor

to

search

for

a

toy

where

she

believes

rightly

or

wrongly

that

it

is

hidden

Such

an

interpretation

calls

into

question

the

notion

that

preschoolers

undergo

a

fundamental

change

from

a

nonrepresentational

to

a

representational

theory

of

mind

Beyond

these

immediate

conclusions

the

present

findings

have

potential

implications

for

two

fields

of

research

The

first

is

atypical

development

Autistic

children

generally

fail

standard

false-belief

tasks

and

as

a

result

are

often

described

as

possessing

a

deficient

theory

of

mind

-LRB-

-RRB-

If

nonverbal

falsebelief

tasks

could

be

adapted

for

use

with

this

population

it

would

open

new

avenues

of

research

into

the

nature

and

early

detection

of

autism

The

second

field

of

research

is

that

of

animal

cognition

Since

the

pioneering

work

of

Premack

and

Woodruff

-LRB-

-RRB-

the

issue

of

whether

animals

possess

a

theory

of

mind

has

attracted

much

attention

-LRB-

-RRB-

The

development

of

various

nonverbal

false-belief

tasks

may

lead

to

new

insights

in

the

field

of

animal

cognition

-LRB-

-RRB-

References

and

Notes

R.

Saxe

N.

Kanwisher

Neuroimage

-LRB-

-RRB-

A.

Gopnik

Behav

Brain

Sci

-LRB-

-RRB-

J.

H.

Flavell

Annu

Rev.

Psychol

-LRB-

-RRB-

H.

M.

Wellman

D.

Cross

J.

Watson

Child

Dev

-LRB-

-RRB-

J.

H.

Flavell

F.

L.

Green

E.

R.

Flavell

Cogn

Dev

-LRB-

-RRB-

J.

W.

Astington

A.

Gopnik

Br

J.

Dev

Psychol

-LRB-

-RRB-

J.

Perner

Understanding

the

Representational

Mind

-LRB-

MIT

Press

Cambridge

MA

-RRB-

A.

Gopnik

H.

M.

Wellman

in

Domain

Specificity

in

Cognition

and

Culture

L.

Hirschfeld

S.

Gelman

Eds

-LRB-

Cambridge

Univ.

Press

New

York

-RRB-

pp.

Fig.

Events

shown

during

the

test

trial

Fig.

Mean

-LRB-

TSE

-RRB-

looking

times

during

the

test

trial

-LRB-

after

the

actor

reached

into

the

green

or

yellow

box

-RRB-

in

the

four

belief

conditions

and

her

action

in

the

test

In

each

case

the

infants

should

look

reliably

longer

when

the

location

the

actor

searched

was

inconsistent

with

her

belief

about

the

location

Participants

were

healthy-term

infants

female

and

male

with

a

mean

age

of

months

days

-LRB-

range

months

days

to

months

days

-RRB-

Seven

infants

were

randomly

assigned

to

each

of

the

eight

groups

formed

by

crossing

the

three

experimental

factors

the

belief

about

the

location

-LRB-

green

or

yellow

box

-RRB-

the

status

of

the

belief

-LRB-

true

or

false

-RRB-

and

the

location

the

actor

searched

during

test

-LRB-

green

or

yellow

box

-RRB-

Another

infants

were

tested

but

eliminated

due

to

inattentiveness

-LRB-

-RRB-

looking

more

than

SD

beyond

the

condition

mean

-LRB-

-RRB-

fussiness

-LRB-

-RRB-

parental

interference

-LRB-

-RRB-

or

observer

error

-LRB-

-RRB-

-LRB-

-RRB-

The

infants

looking

times

during

the

test

trial

-LRB-

Fig.

-RRB-

were

compared

by

means

of

an

analysis

of

variance

with

belief

about

the

location

-LRB-

green

or

yellow

box

-RRB-

belief

status

-LRB-

true

or

false

-RRB-

and

action

-LRB-

green

or

yellow

box

-RRB-

as

between-subject

factors

The

predicted

interaction

between

belief

and

action

was

reliable

EF

-LRB-

-RRB-

P

G

indicating

that

the

infants

expected

the

actor

to

reach

where

she

believed

the

toy

to

be

and

looked

longer

when

she

did

not

This

interaction

was

also

reliable

within

the

true-belief

EF

-LRB-

-RRB-

P

G

and

the

false-belief

EF

-LRB-

-RRB-

P

G

conditions

Finally

planned

comparisons

indicated

that

in

each

of

the

four

belief

conditions

infants

expected

the

actor

to

search

for

her

toy

where

she

believed

it

to

be

hidden

and

looked

reliably

longer

when

she

did

not

-LRB-

for

all

conditions

F

P

G

-RRB-

-LRB-

see

supporting

online

material

text

for

analyses

-RRB-

Whether

the

actor

believed

the

toy

to

be

hidden

in

the

green

or

the

yellow

box

and

whether

this

belief

was

in

fact

true

or

false

the

infants

expected

the

actor

to

search

on

the

basis

of

her

belief

about

the

location

These

results

suggest

that

infants

already

possess

-LRB-

at

least

in

a

rudimentary

and

implicit

form

-RRB-

a

representational

theory

of

mind

They

realize

that

others

act

on

the

basis

of

their

beliefs

and

that

these

beliefs

are

representations

that

may

or

may

not

mirror

reality

Could

our

results

be

explained

in

terms

of

low-level

strategies

the

infants

might

have

used

to

predict

the

behavior

Together

the

four

conditions

demonstrate

that

the

infants

did

not

simply

expect

the

actor

to

search

where

the

toy

was

actually

hidden

-LRB-

FB-green

and

FB-yellow

-RRB-

where

she

had

previously

searched

-LRB-

TB-yellow

and

FB-yellow

-RRB-

or

where

she

had

last

attended

-LRB-

TB-green

-RRB-

In

addition

the

results

make

clear

that

the

infants

did

not

simply

become

confused

when

the

actor

held

a

false

belief

and

expect

her

to

repeat

whatever

action

she

had

last

performed

-LRB-

FB-yellow

-RRB-

Could

the

infants

have

used

a

more

sophisticated

strategy

that

still

fell

short

of

attributing

to

the

actor

a

belief

about

the

location

Perhaps

the

infants

brought

to

the

task

a

superficial

expectation

-LRB-

acquired

through

repeated

observations

-RRB-

that

a

person

looking

for

an

object

will

search

for

it

where

she

last

saw

it

disappear

This

interpretation

-LRB-

which

could

also

be

offered

for

the

modified

falsebelief

task

described

earlier

-RRB-

assumes

that

the

infants

-LRB-

i

-RRB-

distinguished

between

their

own

and

the

perceptions

-LRB-

ii

-RRB-

kept

track

of

what

the

actor

did

and

did

not

see

and

-LRB-

iii

-RRB-

understood

that

the

perceptions

-LRB-

rather

than

their

own

-RRB-

should

be

used

to

predict

her

behavior

On

this

interpretation

our

research

would

add

to

previous

findings

on

the

ability

of

young

children

to

keep

track

of

others

perceptions

For

example

year

olds

kept

track

of

whether

their

parent

was

present

or

absent

when

a

toy

was

hidden

in

a

room

if

the

parent

was

absent

children

were

more

likely

to

point

to

the

location

when

the

parent

returned

-LRB-

-RRB-

According

to

this

alternative

interpretation

our

research

would

extend

these

results

by

showing

that

infants

respond

appropriately

even

when

the

actor

is

mistaken

as

opposed

to

simply

ignorant

about

the

location

and

even

when

this

information

must

SCIENCE

VOL

APRIL

Downloaded

from

on

May

REPORTS

H.

Wimmer

J.

Perner

Cognition

-LRB-

-RRB-

S.

Baron-Cohen

A.

M.

Leslie

U.

Frith

Cognition

-LRB-

-RRB-

H.

M.

Wellman

K.

Bartsch

Cognition

-LRB-

-RRB-

L.

J.

Moses

J.

H.

Flavell

Child

Dev

-LRB-

-RRB-

D.

Zaitchik

Cognition

-LRB-

-RRB-

A.

M.

Leslie

Psychol

Rev.

-LRB-

-RRB-

M.

Chandler

A.

S.

Fritz

S.

Hala

Child

Dev

-LRB-

-RRB-

J.

A.

Fodor

Cognition

-LRB-

-RRB-

D.

Premack

A.

J.

Premack

in

The

Cognitive

Neurosciences

M.

S.

Gazzaniga

Ed

-LRB-

MIT

Press

Cambridge

MA

-RRB-

pp.

P.

Bloom

T.

P.

German

Cognition

-LRB-

-RRB-

W.

A.

Clements

J.

Perner

Cogn

Dev

-LRB-

-RRB-

W.

A.

Garnham

T.

Ruffman

Dev

Sci

-LRB-

-RRB-

G.

Gergely

Z.

Nadasdy

G.

Csibra

S.

Biro

Cognition

-LRB-

-RRB-

A.

L.

Woodward

Cognition

-LRB-

-RRB-

K.

H.

Onishi

R.

Baillargeon

A.

L.

Woodward

in

preparation

Materials

and

methods

are

available

as

supporting

material

on

Science

Online

D.

K.

O'Neill

Child

Dev

-LRB-

-RRB-

K.

H.

Onishi

R.

Baillargeon

paper

presented

at

the

International

Conference

on

Infant

Studies

Chicago

IL

to

May

R.

Baillargeon

paper

presented

at

Munich

Encounters

in

Cognition

and

Action

Max

Planck

Institute

for

Human

Cognitive

and

Brain

Sciences

Munich

Germany

November

S.

Baron-Cohen

Mindblindness

An

Essay

on

Autism

and

Theory

of

Mind

-LRB-

MIT

Press

Cambridge

MA

-RRB-

D.

Premack

G.

Woodruff

Behav

Brain

Sci

-LRB-

-RRB-

C.

M.

Heyes

Behav

Brain

Sci

-LRB-

-RRB-

B.

Hare

J.

Call

M.

Tomasello

Anim

Behav

-LRB-

-RRB-

We

thank

K.

Chambers

G.

DeJong

C.

Fisher

and

G.

L.

Murphy

for

comments

and

suggestions

H.

Song

and

the

staff

of

the

Infant

Cognition

Laboratory

at

the

University

of

Illinois

for

their

help

with

the

data

collection

and

analyses

and

the

parents

who

kindly

agreed

to

participate

in

the

research

This

work

was

supported

by

a

predoctoral

traineeship

from

the

National

Institute

of

Mental

Health

-LRB-

-RRB-

to

K.O.

and

by

a

grant

from

the

National

Institute

of

Child

Health

and

Human

Development

-LRB-

-RRB-

to

R.B.

Supporting

Online

Material

Materials

and

Methods

SOM

Text

November

accepted

February

science

Thibaut

Malausa

Marie-Therese

Bethenod

Arnaud

Bontemps

Denis

Bourguet

Jean-Marie

Cornuet

Sergine

Although

a

growing

body

of

work

supports

the

plausibility

of

sympatric

speciation

in

animals

the

practical

difficulties

of

directly

quantifying

reproductive

isolation

between

diverging

taxa

remain

an

obstacle

to

analyzing

this

process

We

used

a

combination

of

genetic

and

biogeochemical

markers

to

produce

a

direct

field

estimate

of

assortative

mating

in

phytophagous

insect

populations

We

show

that

individuals

of

the

same

insect

species

the

European

corn

borer

Ostrinia

nubilalis

that

develop

on

different

host

plants

can

display

almost

absolute

reproductive

isolation

the

proportion

of

assortative

mating

was

even

in

the

absence

of

temporal

or

spatial

isolation

The

evolution

of

host

races

in

phytophagous

insects

provides

opportunities

for

studying

processes

that

may

ultimately

lead

to

sympatric

speciation

-LRB-

-RRB-

In

the

absence

of

geographic

isolation

postzygotic

barriers

may

contribute

to

genetic

differentiation

but

the

key

mechanism

ensuring

reproductive

isolation

over

time

is

assortative

mating

-LRB-

-RRB-

This

mechanism

may

be

selected

per

se

via

reinforcement

-LRB-

-RRB-

or

as

a

by-product

of

host

specialization

-LRB-

pleiotropy

-RRB-

-LRB-

-RRB-

Despite

its

pivotal

function

in

speciation

the

overall

level

of

assortative

mating

between

sympatric

populations

has

never

been

quantified

directly

in

natural

populations

of

phytophagous

insects

First

it

is

often

difficult

to

detect

individuals

in

the

field

at

the

Laboratoire

Dynamique

de

la

Biodiversite

Universite

P.

Sabatier

Toulouse

III

UMR

CNRS

Toulouse

Cedex

France

de

Biologie

et

de

Gestion

des

Populations

-LRB-

CBGP

-RRB-

Institut

National

de

la

Recherche

Agronomique

Campus

International

de

Baillarguet

Montferrier/Lez

France

Genetique

Microbienne

et

Environnement

Institut

National

de

la

Recherche

Agronomique

La

Miniere

Guyancourt

France

To

whom

correspondence

should

be

addressed

E-mail

malausa@cict.fr

very

moment

they

mate

Second

morphological

or

genetic

markers

often

provide

insufficient

resolution

for

the

assignment

of

individuals

to

host

races

Hence

even

the

most

comprehensive

studies

on

insect

host

races

-LRB-

-RRB-

provided

indirect

estimates

of

assortative

mating

These

estimates

were

obtained

from

experiments

carried

out

in

the

laboratory

or

with

laboratory-reared

individuals

-LRB-

-RRB-

and/or

derived

from

the

measurement

of

factors

thought

to

favor

assortative

mating

such

as

temporal

isolation

-LRB-

-RRB-

and

host

fidelity

-LRB-

-RRB-

However

assortative

mating

probably

results

from

flexible

behavioral

decisions

influenced

by

interactions

between

physiological

and

environmental

factors

-LRB-

e.g.

related

to

host

plants

-RRB-

A

combination

of

genetic

-LRB-

-RRB-

and

biogeochemical

-LRB-

-RRB-

markers

was

used

to

produce

a

global

direct

quantitative

field

estimate

of

assortative

mating

between

sympatric

phytophagous

insect

host

races

Populations

of

the

European

corn

borer

-LRB-

ECB

-RRB-

Ostrinia

nubilalis

H

-LSB-

bner

-LRB-

Lepidoptera

Crambidae

-RRB-

feed

on

more

than

weeds

and

cultivated

plants

-LRB-

-RRB-

and

must

have

colonized

maize

-LRB-

Zea

mays

L.

-RRB-

after

its

introduction

into

Europe

about

years

ago

In

France

ECB

VOL

SCIENCE

APRIL

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from

on

May

Assortative

Mating

in

Sympatric

Host

Races

of

the

European

Corn

Borer

populations

can

be

separated

into

at

least

two

genetically

different

taxa

that

exhibit

all

core

characteristics

-LRB-

-RRB-

of

host

races

-LRB-

-RRB-

the

so-called

Bhop-mugwort-E

race

-LSB-

which

feeds

on

mugwort

-LRB-

Artemisia

vulgaris

L.

-RRB-

and

hop

-LRB-

Humulus

lupulus

L.

-RRB-

and

communicates

with

the

BE

-LSB-

blend

of

sex

pheromone

isomers

and

the

Bmaize-Z

race

-LSB-

which

feeds

on

maize

and

communicates

with

the

BZ

-LSB-

pheromone

blend

-LRB-

-RRB-

Although

both

races

display

host

fidelity

for

oviposition

-LRB-

-RRB-

mating

does

not

occur

primarily

on

the

host

plant

itself

but

on

various

other

species

sometimes

several

hundred

meters

from

the

nearest

host

plant

-LRB-

-RRB-

As

for

most

model

taxa

in

hostrace

studies

-LRB-

-RRB-

it

is

uncertain

whether

ECB

host

races

originally

diverged

in

sympatry

However

they

presently

co-occur

over

a

large

geographical

range

-LRB-

-RRB-

Thus

they

can

provide

insight

into

how

genetic

differentiation

is

maintained

in

sympatry

a

necessary

condition

for

sympatric

speciation

Some

hybrids

between

ECB

host

races

were

obtained

in

experimental

settings

-LRB-

-RRB-

and

some

pheromonal

hybrids

were

found

in

natura

-LRB-

-RRB-

but

both

were

rare

pointing

at

assortative

mating

as

a

key

mechanism

maintaining

genetic

differentiation

The

level

of

assortative

mating

between

host

races

in

the

field

had

however

never

been

quantified

Over

weeks

of

the

July

breeding

season

we

caught

a

total

of

moths

at

five

sites

located

within

km

of

each

other

Their

wings

were

subjected

to

stable

carbon

isotope

analysis

-LRB-

-RRB-

Because

the

value

of

animal

tissues

closely

mirrors

that

of

the

food

-LRB-

-RRB-

ECB

adults

that

emerged

from

larvae

fed

on

the

two

types

of

host

plant

can

be

distinguished

according

to

the

value

of

their

tissues

-LRB-

-RRB-

The

values

obtained

here

showed

a

bimodal

distribution

with

no

overlap

-LRB-

Fig.

-RRB-

Values

of

to

are

typical

for

individuals

feeding

on

plants

with

photosynthesis

such

as

mugwort

and

hop

whereas

values

of

to

are

typical

of

individuals

feeding

on

plants

such

as

maize

-LRB-

-RRB-

This

method

therefore

resulted

in

the

unambiguous

assignment

of

each

moth

to

one

of

the

two

host-plant

types

O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O B I I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O B O O O O O O O O O O O O B O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O B O O O O O O O O O O O O O O B O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O B O O O O O O O O O O O O O O B O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O B O O O O O O O O O O B O O O O O O O O O O B O O O O O O O O O O O O O O B I I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O B O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O B O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O

infants
belief
theory of mind
psychology