Agent-Specific

Responses

in

the

Cingulate

Cortex

During

Economic

Exchanges

Damon

Tomlin

et

al.

Science

-LRB-

-RRB-

DOI

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The

title

Science

is

a

registered

trademark

of

AAAS

REPORTS

Agent-Specific

Responses

in

the

Cingulate

Cortex

During

Economic

Exchanges

Damon

Tomlin

M.

Amin

Kayali

Brooks

King-Casas

Cedric

Anen

Colin

F.

Camerer

Steven

R.

Quartz

P.

Read

Interactions

with

other

responsive

agents

lie

at

the

core

of

all

social

exchange

During

a

social

exchange

with

a

partner

one

fundamental

variable

that

must

be

computed

correctly

is

who

gets

credit

for

a

shared

outcome

this

assignment

is

crucial

for

deciding

on

an

optimal

level

of

cooperation

that

avoids

simple

exploitation

We

carried

out

an

iterated

two-person

economic

exchange

and

made

simultaneous

hemodynamic

measurements

from

each

player

's

brain

These

joint

measurements

revealed

agent-specific

responses

in

the

social

domain

-LRB-

me

and

not

me

-RRB-

arranged

in

a

systematic

spatial

pattern

along

the

cingulate

cortex

This

systematic

response

pattern

did

not

depend

on

metrical

aspects

of

the

exchange

and

it

disappeared

completely

in

the

absence

of

a

responding

partner

S

ocial

exchange

occurs

in

species

ranging

from

insects

to

humans

-LRB-

-RRB-

In

primates

reciprocal

interactions

with

nonkin

occur

repeatedly

thus

necessitating

the

capacity

to

assign

social

credit

or

blame

for

shared

outcomes

and

to

act

appropriately

according

to

these

assignments

-LRB-

-RRB-

In

humans

reciprocity

is

a

central

feature

of

the

collection

of

psychological

mechanisms

necessary

to

support

social

exchange

-LRB-

-RRB-

yet

the

underlying

neural

representations

of

these

mechanisms

remain

murky

In

almost

all

social

exchanges

one

must

detect

and

accurately

track

which

social

agent

-LRB-

who

-RRB-

gets

credit

for

an

outcome

Should

credit

for

an

outcome

be

assigned

to

own

actions

or

those

of

partner

Perhaps

such

assignments

are

more

a

matter

of

degree

assigning

the

degree-of-credit

to

some

shared

outcome

Understanding

such

agentspecific

mechanisms

is

important

because

the

assignment

of

social

agency

-LRB-

-RRB-

appears

to

break

down

in

a

range

of

mental

illnesses

-LRB-

-RRB-

Social

agency

computations

are

also

a

prerequisite

for

generating

models

of

mental

states

This

latter

capacity

called

theory-of-mind

is

highly

developed

in

humans

and

has

been

shown

to

activate

a

consistent

set

of

brain

regions

in

neuroimaging

experiments

-LRB-

-RRB-

Recent

work

has

complemented

these

theory-of-mind

experiments

by

using

interactive

economic

games

as

ecologically

realistic

models

for

human

exchange

-LRB-

-RRB-

These

experiments

have

elicited

not

only

brain

responses

in

previously

described

theory-of-mind

networks

-LRB-

-RRB-

but

also

have

elicited

formerly

unreported

activations

along

the

cingulate

cortex

that

correlate

with

the

revelation

of

a

social

decision

-LRB-

-RRB-

Although

evoked

during

an

economic

exchange

with

another

human

these

cingulate

activations

did

not

modulate

as

a

function

of

the

fairness

of

the

exchange

nor

did

they

occur

in

exchanges

with

computer

partners

-LRB-

-RRB-

This

lack

of

sensitivity

to

measures

of

outcome

suggests

that

these

responses

do

not

encode

some

metrical

aspect

of

the

trade

instead

they

are

consistent

with

the

social

agency

computation

described

above

To

test

this

possibility

directly

we

scanned

both

Human

Neuroimaging

Laboratory

Department

of

Neuroscience

of

Psychiatry

Center

for

Theoretical

Neuroscience

Baylor

College

of

Medicine

Baylor

Plaza

Houston

TX

USA

Cognitive

Neuroscience

Laboratory

California

Institute

of

Technology

Division

of

Humanities

and

Social

Sciences

California

Institute

of

Technology

Pasadena

CA

USA

These

authors

contributed

equally

to

this

work

Fig.

Cross-cingulate

correlations

reveal

complementary

activity

patterns

across

investment

and

repayment

phase

of

game

-LRB-

A

-RRB-

trust

game

In

each

round

the

investor

contributes

some

amount

I

between

monetary

units

and

monetary

units

which

is

tripled

-LRB-

I

-RRB-

and

sent

to

the

trustee

who

then

repays

some

fraction

f

of

the

tripled

amount

-LRB-

f

I

-RRB-

-LRB-

B

-RRB-

Cross-cingulate

principal

component

analysis

-LRB-

PCA

-RRB-

revealed

distinct

but

complementary

patterns

when

applied

to

the

cross-correlations

between

cingulate

cortices

of

investor

and

trustee

-LRB-

-RRB-

A

similar

result

was

found

using

independent

component

analysis

on

the

same

data

-LRB-

fig

-RRB-

SCIENCE

VOL

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from

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brains

of

two

subjects

interacting

in

a

trust

game

-LRB-

-RRB-

This

game

has

been

used

to

identify

neural

correlates

of

reputation

building

and

reciprocity

-LRB-

-RRB-

Because

the

trust

game

is

a

multiround

economic

exchange

it

allows

us

to

estimate

brain

responses

in

both

subjects

to

multiple

revelations

of

a

choice

and

multiple

instances

of

own

choice

The

trust

game

is

illustrated

in

Fig.

In

each

round

one

player

-LRB-

investor

-RRB-

invests

some

amount

I

-LRB-

investment

phase

-RRB-

that

is

tripled

and

sent

to

the

other

player

-LRB-

trustee

-RRB-

who

decides

to

repay

some

fraction

f

of

the

tripled

amount

-LRB-

repayment

phase

-RRB-

-LRB-

-RRB-

Players

maintain

their

roles

for

consecutive

rounds

and

information

about

outcomes

within

each

phase

is

presented

simultaneously

to

both

subjects

We

parameterized

social

context

within

the

trust

game

by

implementing

two

separate

versions

of

the

task

in

different

subject

cohorts

personal

-LRB-

n

subjects

-RRB-

and

impersonal

En

previously

reported

in

-LRB-

-RRB-

In

the

personal

version

subjects

met

before

the

task

were

instructed

together

saw

a

picture

of

their

partner

during

each

round

of

the

game

and

met

their

partner

afterward

where

they

were

paid

in

front

of

each

other

In

the

impersonal

version

subjects

never

met

had

no

chance

of

subsequent

encounter

and

received

no

information

about

one

another

Given

the

previously

reported

activations

in

the

anterior

and

posterior

portions

of

the

medial

cingulate

during

a

social

exchange

-LRB-

-RRB-

a

detailed

analysis

of

the

cingulate

cortex

in

each

pair

of

subjects

was

per

REPORTS

formed

We

segmented

the

medial

cingulate

and

the

surrounding

paracingulate

cortex

into

separate

spatial

domains

-LRB-

-RRB-

computed

cross-cingulate

and

cross-paracingulate

correlation

matrices

for

different

lags

in

each

phase

of

the

task

-LRB-

investment

phase

and

repayment

phase

-RRB-

and

carried

out

temporal

principal

component

analysis

-LRB-

PCA

-RRB-

on

the

resulting

three-dimensional

correlation

matrix

-LRB-

Fig.

-RRB-

-LRB-

-RRB-

Analysis

yielded

complementary

spatial

patterns

for

cingulate

cortices

-LRB-

Fig.

-RRB-

that

is

patterns

of

activation

in

one

phase

were

transposed

across

role

when

analysis

was

performed

for

the

other

phase

Similar

results

were

found

using

independent

component

analysis

-LRB-

ICA

-RRB-

on

the

cross-cingulate

correlation

matrix

-LRB-

fig

-RRB-

-LRB-

-RRB-

The

cross-cingulate

analysis

led

us

to

examine

the

hemodynamic

time

series

in

each

cingulate

segment

This

region-of-interest

analysis

revealed

three

distinct

response

types

-LRB-

Fig.

-RRB-

The

first

followed

the

submission

of

a

own

decision

-LRB-

unimodal

Bown

-LSB-

dominated

response

-RRB-

the

second

followed

the

visual

presentation

of

a

decision

-LRB-

unimodal

Bother

-LSB-

dominated

response

-RRB-

This

is

a

remarkable

finding

because

visual

presentation

of

the

own

decision

elicited

little

response

in

the

cingulate

cortex

The

third

response

type

was

bimodal

yielding

approximately

equal

responses

after

submission

of

own

decision

and

revelation

of

the

decision

However

the

peak

amplitude

of

these

distinct

response

types

was

not

uniform

across

the

anteriorposterior

axis

of

the

cingulate

Instead

they

displayed

a

systematic

spatial

variation

that

was

complementary

across

the

basic

response

types

-LRB-

Bown

-LSB-

and

Bother

-LSB-

-RRB-

Specifically

the

submission

of

own

decision

elicited

maximal

activation

in

middle

cingulate

regions

-LRB-

Fig.

segment

G

-RRB-

whereas

viewing

the

revelation

of

a

decision

yielded

maximal

activation

in

anterior

and

posterior

cingulate

-LRB-

an

example

of

an

anterior

response

is

shown

in

Fig.

segment

K

-RRB-

This

result

was

in

stark

contrast

to

the

results

of

the

paracingulate

analysis

which

indicated

that

although

the

dorsal

anterior

cingulate

cortex

was

highly

activated

during

the

experiment

there

was

no

spatial

selectivity

for

either

stimulus

In

fact

the

dorsal

anterior

cingulate

cortex

responded

strongly

to

the

submission

of

decisions

and

the

revelation

of

partner

choices

and

it

was

the

only

paracingulate

region

significantly

activated

by

either

-LRB-

fig

-RRB-

-LRB-

-RRB-

The

distinct

response

types

and

the

systematic

spatial

variation

of

peak

amplitudes

across

the

anterior-posterior

axis

disappeared

completely

in

motor

control

-LRB-

n

Fig.

-RRB-

and

sensory

control

experiments

-LRB-

n

Fig.

-RRB-

not

involving

exchange

with

another

agent

-LRB-

-RRB-

In

the

motor

control

subjects

reiterated

the

motor

responses

of

randomly

selected

investors

We

applied

the

same

region-of-interest

analysis

to

the

control

data

-LRB-

Fig.

and

fig

-RRB-

Statistical

comparison

of

responses

in

each

of

the

cingulate

domains

showed

that

responses

differed

significantly

between

the

normal

trust

task

and

the

control

tasks

-LRB-

-RRB-

In

particular

no

significant

response

was

present

in

the

middle

cingulate

-LRB-

Fig.

-RRB-

ruling

out

the

possibility

that

middle

cingulate

activation

in

the

trust

game

was

the

result

of

motor

activity

produced

by

button

tapping

In

the

sensory

control

partner

reveal

screens

from

the

trust

game

were

viewed

passively

by

a

separate

cohort

of

subjects

-LRB-

n

-RRB-

Because

partner

reveal

screens

Fig.

Agent-specific

responses

and

their

pattern

disappear

outside

of

economic

exchange

-LRB-

A

-RRB-

Calculation

of

response

pattern

diagrams

Traces

are

the

average

magnetic

resonance

-LRB-

MR

-RRB-

signal

during

subject

decision

phases

-LRB-

magenta

lines

-RRB-

and

during

partner

decision

phases

-LRB-

black

lines

-RRB-

error

bars

represent

the

standard

error

of

the

mean

-LRB-

n

subjects

-RRB-

To

compute

the

magnitude

of

responses

to

submitting

a

decision

MR

values

were

selected

from

the

time

of

peak

response

and

the

peak

's

two

flanking

points

-LRB-

teal

boxes

-RRB-

These

values

when

averaged

represent

the

responsiveness

of

a

segment

to

the

submission

of

the

decision

This

measure

was

performed

for

all

segments

and

a

pseudo

color

image

was

produced

as

depicted

in

Figs.

and

For

responses

to

partner

reveal

screens

MR

values

corresponding

to

the

peak

activity

after

screen

onset

and

the

peak

's

two

flanking

points

-LRB-

red

boxes

-RRB-

were

averaged

and

compiled

into

a

similar

pseudo

color

map

-LRB-

B

-RRB-

The

average

response

to

submitting

a

decision

is

shown

for

subjects

playing

the

linked

trust

game

-LRB-

n

-RRB-

and

a

predominance

of

the

middle

cingulate

is

apparent

-LRB-

C

-RRB-

Average

response

profile

to

submitting

decisions

in

the

unlinked

motor

control

experiment

-LRB-

n

-RRB-

No

significant

differentiation

was

observed

across

the

cingulate

of

subjects

in

this

task

but

response

levels

in

the

middle

cingulate

were

significantly

different

than

those

in

the

linked

trust

game

-LRB-

P

-RRB-

-LRB-

D

-RRB-

Subjects

from

the

linked

trust

experiment

-LRB-

n

-RRB-

demonstrate

the

average

response

to

viewing

a

social

partner

's

decision

The

predominance

of

responses

in

the

anterior

and

posterior

poles

of

the

cingulate

is

apparent

in

this

group

-LRB-

E

-RRB-

Average

response

to

viewing

screens

in

the

unlinked

visual

control

experiment

-LRB-

n

-RRB-

No

significant

differentiation

was

observed

across

cingulate

domains

but

responses

in

both

anterior

and

posterior

regions

were

significantly

different

than

those

in

the

linked

trust

game

-LRB-

P

G

-RRB-

Maximum

activation

in

-LRB-

B

-RRB-

and

-LRB-

C

-RRB-

is

change

in

MR

signal

maximum

activation

in

-LRB-

D

-RRB-

and

-LRB-

E

-RRB-

is

minimum

activation

for

each

is

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REPORTS

in

the

trust

game

had

novel

content

and

had

been

generated

by

an

external

agent

we

could

not

use

the

original

data

set

to

separate

responses

to

social

or

novel

stimuli

Thus

subjects

in

the

sensory

control

task

were

informed

that

their

compensation

depended

on

money

shown

under

the

Bgave

-LSB-

label

on

the

screen

but

were

not

told

about

the

social

task

from

which

this

screen

was

derived

-LRB-

fig

-RRB-

This

manipulation

was

performed

so

that

a

content

still

held

novel

and

valuable

information

but

was

devoid

of

social

interaction

In

each

of

the

cingulate

domains

BOLD

responses

after

each

of

outcome

screens

did

not

resemble

those

obtained

during

the

analogous

presentation

in

the

linked

experiment

-LRB-

Fig.

and

fig

-RRB-

There

was

no

systematic

spatial

variation

in

response

amplitudes

across

the

cingulate

gyrus

To

verify

that

motor

control

and

sensory

control

effects

were

not

due

to

the

smaller

number

of

subjects

involved

in

the

control

manipulations

we

confirmed

this

finding

by

using

random

samples

of

the

existing

database

-LRB-

fig

-RRB-

The

results

provide

strong

support

for

three

new

findings

-LRB-

i

-RRB-

agent-specific

response

types

localized

on

the

medial

bank

of

cingulate

cortex

-LRB-

ii

-RRB-

a

systematic

spatial

variation

of

each

response

type

across

the

anterior-posterior

axis

of

cingulate

cortex

and

-LRB-

iii

-RRB-

a

dependence

of

both

signals

on

the

presence

of

a

responding

agent

Despite

the

relative

simplicity

of

this

economic

exchange

game

other

variable

-LRB-

s

-RRB-

related

to

this

task

may

have

been

the

underlying

cause

of

the

different

response

types

the

spatial

variation

across

the

cingulate

and

the

difference

in

response

to

visual

revelation

of

own

decision

and

decision

However

the

different

response

types

and

their

systematic

but

complementary

spatial

variation

across

the

cingulate

did

not

change

as

a

function

of

a

range

of

dimensions

-LRB-

Fig.

-RRB-

The

most

dramatic

dimensions

tested

in

Fig.

are

reciprocity

and

social

context

-LRB-

personal

versus

impersonal

-RRB-

In

previously

published

work

reciprocity

expressed

as

degree

of

tit-for-tat

behavior

across

rounds

acted

as

a

powerful

behavioral

signal

to

partner

and

elicited

strong

measurable

neural

correlates

-LRB-

-RRB-

Yet

as

illustrated

in

Fig.

-LRB-

bottom

three

rows

-RRB-

differences

in

reciprocity

had

no

effect

on

the

response

types

or

on

their

spatial

variation

along

the

cingulate

The

same

result

held

for

the

difference

in

social

context

-LRB-

personal

n

impersonal

n

-RRB-

where

prior

exposure

to

partner

the

sight

of

their

picture

in

each

round

and

the

knowledge

of

an

imminent

encounter

afterward

had

no

effect

Likewise

no

differences

were

observed

when

comparing

subject

role

-LRB-

investor

or

trustee

-RRB-

sex

of

subject

or

amount

of

money

sent

or

received

Using

an

iterated

economic

exchange

task

we

found

two

distinct

response

types

along

the

cingulate

cortex

consistent

with

agent-specific

responses

that

signal

Bme

-LSB-

and

Bnot

me

-LSB-

Rather

than

residing

in

strictly

demarcated

functional

zones

these

complementary

responses

types

exhibited

smooth

transitions

across

the

entire

medial

bank

of

the

cingulate

gyrus

It

is

difficult

to

probe

the

extent

to

which

a

subject

is

considering

outcomes

for

oneself

or

a

social

partner

individuals

in

a

social

exchange

must

necessarily

model

the

actions

of

both

agents

as

decisions

are

made

and

revealed

Despite

this

obstacle

the

pattern

of

activation

observed

in

these

data

was

clearly

sensitive

to

which

participant

was

responsible

for

a

given

action

The

response

types

and

their

variation

through

the

tissue

space

disappeared

in

control

experiments

where

money

sent

actions

taken

and

money

received

were

matched

to

those

experienced

during

the

normal

multiround

exchange

-LRB-

Fig.

and

fig

-RRB-

-LRB-

-RRB-

These

controls

provide

strong

evidence

that

the

response

types

were

due

to

neither

motor

and

premotor

responses

nor

to

sensory

responses

to

outcome

screens

One

question

deserves

separate

consideration

Did

the

reveal

screens

generate

simple

surprise

or

novelty

responses

along

cingulate

that

were

not

related

to

the

social

element

of

the

exchange

Although

this

reasonable

interpretation

is

possible

the

control

experiments

suggest

otherwise

The

response

pattern

along

the

cingulate

disappeared

in

the

control

experiments

where

subjects

received

stimuli

that

were

visually

identical

to

those

in

the

trust

game

and

were

composed

of

novel

rewardrelated

information

This

manipulation

used

novel

stimuli

with

economically

meaningful

content

to

probe

the

reveal

response

and

showed

neither

an

Bother

-LSB-

response

anywhere

along

the

cingulate

nor

the

spatial

variation

so

prominent

in

the

linked

trust

task

We

take

these

data

as

strong

support

that

the

responses

observed

in

the

linked

trust

game

were

not

the

mere

result

of

surprising

content

The

response

types

and

their

spatial

variation

along

the

cingulate

were

remarkably

stable

to

a

range

of

manipulations

They

survived

the

personal

and

impersonal

treatments

did

not

change

as

a

function

of

the

reciprocity

-LRB-

a

variable

previously

shown

to

be

the

major

behavioral

signal

in

this

game

-RRB-

-LRB-

-RRB-

and

were

not

Fig.

Cingulate

pattern

of

me

and

not

me

remains

constant

across

a

range

of

variables

All

responses

to

decision

submission

are

shown

in

the

left

column

whereas

those

responses

to

partner

reveal

screens

are

shown

in

the

right

column

With

the

exception

of

the

reciprocity

and

amount

diagrams

all

responses

were

averaged

across

rounds

before

compilation

Rows

labeled

Personal

and

Impersonal

separate

activity

across

social

context

the

personal

-LRB-

n

individuals

-RRB-

and

impersonal

-LRB-

n

individuals

-RRB-

tasks

Rows

labeled

Investors

and

Trustees

demonstrate

the

consistency

of

the

responses

across

the

two

different

roles

-LRB-

n

for

each

-RRB-

Rows

labeled

Males

and

Females

demonstrate

that

these

responses

do

not

differ

across

gender

-LRB-

n

for

each

-RRB-

Rows

labeled

Small

amount

and

Large

amount

show

that

these

patterns

do

not

depend

upon

the

amount

of

resource

sent

or

received

by

the

player

-LRB-

upper

versus

lower

of

payments

n

and

respectively

-RRB-

Finally

the

rows

labeled

Positive

Neutral

and

Negative

reciprocity

depict

responses

across

different

valences

of

a

behavioral

variable

of

already

known

interest

-LRB-

-RRB-

These

diagrams

correspond

to

average

BOLD

responses

to

positive

-LRB-

values

n

choices

-RRB-

neutral

-LRB-

e

values

e

n

choices

-RRB-

and

negative

-LRB-

values

G

n

choices

-RRB-

values

of

the

reciprocity

index

Left

column

maximum

is

change

in

MR

signal

right

column

maximum

is

minimum

activation

for

both

is

SCIENCE

VOL

MAY

Downloaded

from

on

May

REPORTS

changed

as

a

function

of

sex

role

amount

sent

or

amount

received

Lastly

these

signals

were

clear

even

in

individual

subject

pairs

as

shown

in

fig

for

a

single

interacting

dyad

The

observed

lack

of

change

as

a

function

of

reciprocity

is

extremely

important

because

it

reduces

the

likelihood

of

two

alternate

interpretations

of

these

data

The

average

behavior

in

this

game

is

initial

cooperation

followed

by

tit-for-tat

moves

a

strategy

conjectured

to

be

optimal

in

a

reciprocal

interaction

-LRB-

-RRB-

To

play

such

a

tit-for-tat

strategy

a

brain

must

compute

the

expected

next

move

of

their

partner

and

compare

this

to

the

actual

outcome

Consequently

large

deviations

in

reciprocity

would

also

carry

large

prediction

error

signals

a

signal

type

known

to

show

up

near

or

around

dorsal

anterior

cingulate

cortex

-LRB-

dACC

-RRB-

-LRB-

-RRB-

Two

possibilities

arise

The

error

signals

could

activate

dACC

because

they

reflect

directly

an

error

response

Alternately

large

deviations

in

reciprocity

represent

a

signal

with

a

large

amount

of

uncertainty

and

might

engage

an

output

conflict

response

typical

for

this

brain

region

-LRB-

-RRB-

However

neither

of

these

interpretations

would

anticipate

an

important

feature

of

the

data

actually

observed

There

was

no

difference

in

response

types

or

their

spatial

variation

as

a

function

of

positive

negative

or

neutral

reciprocity

One

would

at

least

expect

both

alternate

explanations

to

show

responses

that

differentiated

neutral

reciprocity

from

the

other

two

categories

-LRB-

positive

and

negative

-RRB-

One

possibility

is

that

our

current

analysis

missed

the

error

signals

altogether

for

some

unidentified

reason

However

by

using

this

same

behavioral

task

we

have

previously

identified

such

error-related

signals

elsewhere

in

the

brain

and

have

shown

these

regions

to

be

sensitive

to

reciprocity

-LRB-

-RRB-

Consequently

our

capacity

to

detect

these

error

signals

elsewhere

makes

it

less

likely

that

we

simply

missed

error

signals

in

cingulate

related

to

strong

deviations

in

reciprocity

However

it

remains

a

possibility

that

some

unprobed

behavioral

dimension

generated

an

error

signal

along

cingulate

cortex

during

this

task

In

a

two-person

social

exchange

it

is

crucial

for

each

agent

to

know

how

to

credit

an

outcome

Failure

to

assign

this

credit

accurately

will

compromise

an

capacity

to

decide

on

an

appropriate

level

of

cooperation

with

the

partner

a

mistake

that

could

prove

extremely

costly

when

averaged

over

multiple

encounters

-LRB-

-RRB-

Consequently

we

suspect

that

these

data

derive

from

a

neural

mechanism

dedicated

to

distinguishing

Bme

-LSB-

outcomes

from

Bnot

me

-LSB-

outcomes

The

systematic

spatial

progression

of

responses

suggests

to

us

that

this

social

agency

variable

may

be

arrayed

as

a

map

however

the

current

experiment

can

not

adequately

test

this

provocative

possibility

It

is

important

therefore

to

note

that

the

assignment

of

credit

-LRB-

or

agency

-RRB-

within

a

social

interaction

necessarily

implicates

a

variety

of

cognitive

and

emotional

mechanisms

Thus

although

agency

parsimoniously

characterizes

the

activations

seen

with

these

data

it

may

not

necessarily

be

congruent

to

the

underlying

functions

represented

along

the

cingulate

Extant

data

support

a

multifunctional

role

for

the

cingulate

cortex

particularly

in

light

of

the

extreme

diversity

of

information

that

impinges

on

this

region

Cingulate

and

paracingulate

cortices

have

long

been

hypothesized

as

sites

of

integration

of

information

sources

that

include

cognitive

emotional

and

interoceptive

signals

Consequently

a

range

of

functions

has

been

ascribed

to

cingulate

cortex

-LRB-

-RRB-

and

there

are

disagreements

over

the

exact

variables

processed

and

represented

in

these

regions

However

it

is

reasonably

clear

that

cingulate

and

paracingulate

cortices

contribute

to

normal

social

cognition

and

adaptive

decision-making

-LRB-

-RRB-

The

results

of

this

paper

add

the

important

possibility

that

many

other

variables

in

the

social

domain

may

be

arranged

in

such

a

systematic

fashion

through

the

spatial

domain

a

phenotype

that

could

be

disturbed

in

afflictions

where

the

capacity

to

distinguish

Bme

-LSB-

from

Bnot

me

-LSB-

is

impaired

-LRB-

-RRB-

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This

work

was

supported

by

the

Center

for

Theoretical

Neuroscience

at

Baylor

College

of

Medicine

-LRB-

P.R.M.

-RRB-

National

Institute

on

Drug

Abuse

-LRB-

NIDA

-RRB-

grant

-LRB-

P.R.M.

-RRB-

National

Institute

of

Neurological

Disorders

and

Stroke

grant

-LRB-

P.R.M.

-RRB-

National

Institute

of

Mental

Health

grant

-LRB-

P.R.M.

-RRB-

NIDA

grant

-LRB-

G.

Berns

-RRB-

the

Angel

Williamson

Imaging

Center

-LRB-

P.R.M.

-RRB-

The

Kane

Family

Foundation

-LRB-

P.R.M.

-RRB-

The

David

and

Lucile

Packard

Foundation

-LRB-

S.R.Q.

and

C.F.C.

-RRB-

and

The

Gordon

and

Betty

Moore

Foundation

-LRB-

S.R.Q.

and

C.F.C.

-RRB-

P.R.M.

also

acknowledges

support

from

the

Institute

for

Advanced

Study

-LRB-

Princeton

NJ

-RRB-

during

completion

of

this

work

We

thank

the

Hyperscan

Development

Team

at

Baylor

College

of

Medicine

for

Network

Experiment

Management

Object

-LRB-

NEMO

-RRB-

software

implementation

-LRB-

-RRB-

and

G.

Berns

for

early

discussions

and

efforts

leading

to

the

development

of

hyperscanning

We

also

thank

C.

Bracero

A.

Harvey

S.

Flaherty

J.

McGee

K.

Pfeiffer

R.

Pruitt

and

S.

Gleason

for

technical

assistance

Supporting

Online

Material

Materials

and

Methods

Figs

to

References

January

accepted

April

science

MAY

VOL

SCIENCE

Downloaded

from

on

May

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


Apes

Save

Tools

for

Future

Use

Nicholas

J.

Mulcahy

et

al.

Science

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on

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related

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Downloaded

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REPORTS

Apes

Save

Tools

for

Future

Use

Nicholas

J.

Mulcahy

and

Josep

Call

Planning

for

future

needs

not

just

current

ones

is

one

of

the

most

formidable

human

cognitive

achievements

Whether

this

skill

is

a

uniquely

human

adaptation

is

a

controversial

issue

In

a

study

we

conducted

bonobos

and

orangutans

selected

transported

and

saved

appropriate

tools

above

baseline

levels

to

use

them

hour

later

-LRB-

experiment

-RRB-

Experiment

extended

these

results

to

a

delay

between

collecting

and

using

the

tools

Experiment

showed

that

seeing

the

apparatus

during

tool

selection

was

not

necessary

to

succeed

These

findings

suggest

that

the

precursor

skills

for

planning

for

the

future

evolved

in

great

apes

before

million

years

ago

when

all

extant

great

ape

species

shared

a

common

ancestor

ulving

-LRB-

-RRB-

recounts

an

Estonian

tale

of

a

girl

who

dreamed

about

attending

a

party

but

was

unable

to

eat

her

favorite

dessert

because

there

were

no

spoons

available

Facing

the

possibility

of

attending

the

party

again

she

took

a

spoon

to

bed

Crucially

the

girl

took

the

spoon

not

because

she

currently

needed

it

but

because

she

would

need

it

in

the

future

Tulving

used

this

example

to

illustrate

the

putatively

unique

human

ability

to

think

about

the

past

and

plan

for

the

future

-LRB-

-RRB-

and

proposed

that

an

analogous

Bspoon

-LSB-

test

could

be

used

to

test

for

future

planning

in

nonhuman

animals

Future

planning

is

cognitively

demanding

because

it

imposes

a

long

delay

between

performing

an

action

and

getting

rewarded

for

it

a

skill

that

humans

use

when

preparing

a

suitcase

before

a

trip

or

by

making

a

cake

to

celebrate

birthday

Although

various

animals

can

plan

and

execute

multiple

actions

toward

a

goal

-LRB-

-RRB-

they

may

achieve

this

without

taking

into

account

future

needs

just

current

ones

-LRB-

-RRB-

Thus

when

chimpanzees

transport

stones

to

use

them

to

crack

open

nuts

or

New

Caledonian

crows

make

hook-shaped

tools

to

fish

for

insects

they

do

so

in

an

attempt

to

satisfy

their

current

hunger

state

not

some

future

one

T

Max

Planck

Institute

for

Evolutionary

Anthropology

Deutscher

Platz

Leipzig

Germany

To

whom

correspondence

should

be

addressed

E-mail

call@eva.mpg.de

To

date

the

only

evidence

suggesting

future

planning

in

animals

is

the

cache

protection

strategy

of

scrub

jays

-LRB-

-RRB-

These

birds

transport

food

from

old

sites

and

re-cache

it

in

new

ones

to

avoid

losing

their

caches

to

conspecifics

that

observed

the

initial

location

of

the

cache

sites

thus

saving

the

items

for

future

consumption

Some

researchers

argue

that

future

planning

may

have

evolved

independently

in

various

taxa

-LRB-

-RRB-

whereas

others

argue

that

the

nonhuman

data

do

not

truly

capture

the

essence

and

complexity

of

human

mental

time

travel

-LRB-

-RRB-

For

instance

it

is

unknown

whether

animals

would

also

transport

and

save

nonedible

items

that

would

enable

them

to

get

food

at

a

later

time

an

ability

that

may

have

played

a

crucial

role

in

human

evolution

-LRB-

-RRB-

Would

extant

apes

also

transport

tools

that

they

do

not

currently

need

anticipating

that

they

will

need

them

in

the

future

This

would

be

an

important

addition

to

the

complex

behavior

displayed

by

scrub

jays

because

what

is

saved

is

not

the

food

itself

but

a

means

to

get

the

food

which

is

one

step

removed

from

the

goal

itself

The

tool

has

no

value

in

itself

it

has

value

only

in

relation

to

the

food

We

investigated

future

planning

in

bonobos

and

orangutans

because

they

represent

our

closest

and

most

distant

great

ape

relatives

respectively

This

allowed

us

to

make

inferences

about

the

possible

time

of

emergence

of

the

precursor

skills

for

future

planning

in

this

group

If

both

species

showed

this

skill

this

would

suggest

that

it

may

have

evolved

before

million

years

ago

-LRB-

Ma

-RRB-

when

all

apes

shared

a

common

ancestor

-LRB-

-RRB-

whereas

if

only

bonobos

showed

it

it

may

have

evolved

within

the

past

My

Its

absence

in

both

species

would

suggest

that

future

planning

is

a

human

adaptation

that

appeared

within

the

past

My

We

tested

five

bonobos

and

five

orangutans

-LRB-

table

-RRB-

First

subjects

learned

to

use

a

tool

to

get

a

reward

from

an

apparatus

in

the

test

room

-LRB-

-RRB-

Then

we

placed

two

suitable

and

six

unsuitable

tools

in

the

test

room

but

blocked

subjects

access

to

the

baited

apparatus

After

min

subjects

were

ushered

outside

the

test

room

into

the

waiting

room

and

the

caretaker

removed

all

objects

left

in

the

test

room

while

subjects

watched

One

hour

later

subjects

were

allowed

to

return

to

the

test

room

and

were

given

access

to

the

apparatus

Thus

to

solve

the

problem

subjects

had

to

select

a

suitable

tool

from

the

test

room

bring

it

into

the

waiting

room

keep

it

there

for

hour

and

bring

it

back

into

the

test

room

upon

their

return

-LRB-

fig

-RRB-

The

trial

ended

after

the

subject

retrieved

the

reward

or

min

had

elapsed

Subjects

solved

the

problem

an

average

of

seven

times

-LRB-

SEM

-RRB-

with

all

subjects

succeeding

at

least

once

within

the

first

seven

trials

-LRB-

Table

-RRB-

Subjects

performed

the

key

behavior

of

transporting

tools

out

of

the

test

room

in

of

the

trials

targeting

suitable

tools

significantly

more

often

than

would

be

expected

by

chance

-LRB-

P

-RRB-

-LRB-

expected

observed

-RRB-

Moreover

they

returned

to

the

test

room

of

the

suitable

tools

but

only

of

the

unsuitable

tools

-LRB-

P

-RRB-

-LRB-

Fig.

-RRB-

Two

orangutans

-LRB-

Dokana

and

Toba

-RRB-

on

one

and

three

occasions

respectively

brought

back

an

inappropriate

tool

but

broke

off

some

small

piece

from

it

with

which

they

still

obtained

the

reward

Even

if

those

trials

are

excluded

from

the

analyses

subjects

still

initially

targeted

suitable

tools

-LRB-

P

-RRB-

and

brought

them

back

more

often

than

Table

Number

and

order

of

correct

trials

for

each

subject

for

each

experiment

NT

not

tested

Experiment

Subjects

Bonobos

Kuno

Joey

Limbuko

Yasa

Ulindi

Orangutans

Walter

Toba

Dokana

Dunja

Pini

Correct

trials

-LRB-

n

-RRB-

NT

NT

NT

NT

Trial

no

Experiment

Correct

trials

-LRB-

n

-RRB-

NT

NT

NT

NT

NT

NT

NT

NT

Trial

no

Correct

trials

-LRB-

n

-RRB-

NT

NT

NT

NT

NT

NT

Experiment

Trial

no

Experiment

Correct

trials

-LRB-

n

-RRB-

NT

NT

NT

NT

NT

NT

Trial

no

MAY

VOL

SCIENCE

Downloaded

from

on

May

REPORTS

unsuitable

tools

-LRB-

P

-RRB-

Tool

transport

did

not

occur

simply

because

subjects

were

already

holding

the

tool

when

the

door

was

opened

after

the

delay

period

Indeed

the

opposite

was

true

On

average

subjects

were

already

holding

the

tool

in

only

-LRB-

SEM

-RRB-

of

the

successful

trials

when

the

door

opened

to

return

to

the

test

room

-LRB-

this

figure

was

for

the

tools

taken

out

of

the

test

room

-RRB-

If

those

trials

are

excluded

subjects

still

solved

the

task

on

an

average

of

trials

-LRB-

out

of

-RRB-

In

experiment

we

increased

the

delay

between

tool

retrieval

and

reward

retrieval

to

hours

We

brought

the

subject

into

the

test

room

then

sent

her

to

the

sleeping

room

-LRB-

which

served

as

waiting

room

-RRB-

for

the

night

and

brought

her

back

to

the

test

room

in

the

morning

The

sleeping

room

was

not

contiguous

to

the

test

room

but

located

one

floor

above

it

We

tested

one

orangutan

and

one

bonobo

Neither

ape

took

any

tools

in

the

first

trial

The

orangutan

took

suitable

tools

in

all

remaining

trials

-LRB-

binomial

test

P

one-tailed

-RRB-

which

she

brought

back

and

used

in

trials

to

get

the

reward

The

bonobo

took

suitable

tools

in

of

the

remaining

trials

-LRB-

binomial

test

P

G

one-tailed

-RRB-

which

he

always

brought

back

to

the

testing

room

to

get

the

reward

In

experiment

two

bonobos

and

two

orangutans

had

to

use

a

hook

to

get

an

out-ofreach

juice

bottle

suspended

from

a

string

-LRB-

fig

-RRB-

After

subjects

had

learned

to

use

the

hook

appropriately

they

were

presented

with

the

hook

and

three

unsuitable

tools

in

the

absence

of

the

apparatus

-LRB-

or

the

reward

-RRB-

Five

minutes

later

subjects

were

ushered

outside

of

the

test

room

and

brought

back

hour

later

Once

subjects

were

inside

the

test

room

the

apparatus

was

installed

and

subjects

could

get

the

reward

if

they

had

returned

with

the

hook

This

experiment

addressed

two

outstanding

issues

It

tested

whether

subjects

would

select

the

suitable

tool

in

the

absence

of

the

apparatus

or

the

reward

It

controlled

for

the

possibility

that

subjects

took

the

tool

in

previous

experiments

to

reduce

their

current

hunger

state

because

the

hook

had

been

associated

only

with

liquid

procurement

Moreover

because

water

was

available

ad

libitum

it

is

unlikely

that

subjects

took

the

hook

to

reduce

their

thirst

Subjects

performance

was

comparable

to

that

in

experiment

Subjects

solved

the

task

on

an

average

of

trials

-LRB-

SEM

-RRB-

succeeding

at

least

once

within

the

first

six

trials

and

transporting

suitable

tools

more

often

than

would

be

expected

by

chance

-LRB-

P

one-tailed

-RRB-

-LRB-

expected

observed

-RRB-

Moreover

they

returned

more

suitable

than

unsuitable

tools

-LRB-

versus

-RRB-

but

the

difference

was

not

statistically

significant

-LRB-

P

one-tailed

-RRB-

-LRB-

Fig.

-RRB-

Experiment

established

the

baseline

probability

of

transporting

tools

in

the

absence

of

a

future

task

but

using

identical

reinforcement

contingencies

as

in

experiment

Two

bonobos

and

two

orangutans

received

the

same

treatment

as

in

experiment

except

that

no

apparatus

was

set

up

upon

their

return

to

the

test

room

although

they

were

rewarded

if

they

brought

the

suitable

tool

back

Subjects

solved

the

task

significantly

less

often

-LRB-

mean

SEM

-RRB-

than

did

those

in

experiment

-LRB-

P

-RRB-

In

fact

only

two

of

the

four

subjects

brought

back

the

suitable

tool

at

all

and

they

behaved

differently

from

other

successful

subjects

because

after

their

first

successful

trial

they

failed

the

next

and

trials

respectively

-LRB-

Table

-RRB-

Subjects

in

experiment

also

solved

the

task

significantly

less

often

than

those

in

experiment

-LRB-

P

-RRB-

thus

ruling

out

the

possible

confounding

effects

of

practice

because

both

groups

of

subjects

were

naBve

when

their

respective

experiments

began

Apes

selected

transported

and

saved

a

suitable

tool

not

because

they

currently

needed

it

but

because

they

would

need

it

in

the

future

These

data

taken

all

together

can

not

be

easily

Suitable

Unsuitable

Ku

Li

Jo

Wa

To

Do

Ku

Do

Ku

Li

To

Do

Ya

Ul

Pi

Du

Exp

Exp

Exp

Exp

Fig.

Percentage

of

suitable

and

unsuitable

tools

transported

into

the

test

room

by

each

subject

after

the

delay

period

in

each

experiment

Subject

name

abbreviations

are

as

follows

Ku

Kuno

Li

Limbuko

Jo

Joey

Wa

Walter

To

Toba

Do

Dokana

Ya

Yasa

Ul

Ulindi

Pi

Pini

Du

Dunja

SCIENCE

VOL

explained

by

invoking

traditional

operant

learning

because

there

was

at

least

a

delay

between

the

response

-LRB-

tool

selection

and

transport

-RRB-

and

the

reinforcement

Typically

instrumental

conditioning

fails

to

occur

if

the

response-reinforcement

interval

is

greater

than

a

few

seconds

in

the

absence

of

conditioned

reinforcers

-LRB-

-RRB-

as

evidenced

by

the

poor

performance

of

the

subjects

in

experiment

as

compared

to

other

experiments

Arguably

the

suitable

tool

could

have

acted

as

a

conditioned

reinforcer

However

this

still

does

not

explain

the

difference

between

experiment

and

the

other

three

experiments

-LRB-

fig

-RRB-

which

is

even

more

remarkable

because

subjects

were

reinforced

for

returning

with

the

tool

in

all

experiments

Perhaps

subjects

did

not

transport

the

tool

in

experiment

because

they

had

not

been

reinforced

to

do

so

However

subjects

in

experiment

faced

the

same

situation

and

all

of

them

transported

the

tool

before

any

reinforcement

had

occurred

Our

results

also

differ

from

the

phenomenon

of

taste

aversion

whereby

an

animal

learns

within

one

trial

to

avoid

the

ingestion

of

a

substance

after

becoming

sick

hour

later

-LRB-

-RRB-

because

taste

aversion

involves

learning

to

avoid

a

stimulus

not

acquiring

an

instrumental

response

Moreover

taste

aversion

shows

a

high

degree

of

stimulus

specificity

because

it

develops

when

gustatory

stimuli

are

paired

with

digestive

sickness

but

not

when

gustatory

stimuli

are

paired

with

other

modalities

of

aversive

stimuli

It

is

highly

unlikely

that

a

similar

form

of

specialized

learning

also

exists

for

tool

transportation

Another

alternative

is

that

our

results

represent

an

unlearned

biological

predisposition

Many

species

appear

to

plan

for

the

future

when

they

build

nests

to

lay

their

eggs

or

hoard

food

for

the

winter

-LRB-

-RRB-

However

unlike

tool

transportation

these

other

activities

have

obvious

fitness

consequences

-LRB-

channeled

by

strong

physiological

and

genetic

determinants

-RRB-

that

have

favored

their

selection

in

all

the

individuals

of

a

species

In

contrast

tool

transportation

even

tool

use

has

not

been

documented

in

most

wild

populations

of

bonobos

or

orangutans

-LRB-

-RRB-

More

important

apes

do

not

store

food

or

objects

in

their

natural

habitats

because

those

are

generally

available

throughout

the

year

It

is

therefore

unlikely

that

saving

and

transporting

tools

are

unlearned

biological

predispositions

Because

traditional

learning

mechanisms

or

certain

biological

predispositions

appear

insufficient

to

explain

our

current

results

we

propose

that

they

represent

a

genuine

case

of

future

planning

Subjects

executed

a

response

-LRB-

tool

transport

-RRB-

that

had

not

been

reinforced

during

training

in

the

absence

of

the

apparatus

or

the

reward

that

produced

no

consequences

or

reduced

any

present

needs

but

was

crucial

to

meet

future

ones

The

presence

of

future

planning

in

both

bonobos

and

orangutans

Tools

MAY

Downloaded

from

on

May

REPORTS

suggests

that

its

precursors

may

have

evolved

before

Ma

in

the

great

apes

Together

with

recent

evidence

from

scrub

jays

-LRB-

-RRB-

our

results

suggest

that

future

planning

is

not

a

uniquely

human

ability

thus

contradicting

the

notion

that

it

emerged

in

hominids

only

within

the

past

to

million

years

-LRB-

-RRB-

Indeed

its

presence

in

distantly

related

taxa

such

as

corvids

and

apes

reinforces

the

hypothesis

that

these

taxa

may

have

undergone

convergent

cognitive

evolution

-LRB-

-RRB-

Future

studies

should

investigate

whether

apes

like

corvids

will

not

only

transport

tools

for

future

use

but

also

protect

them

from

conspecifics

that

may

steal

them

References

and

Notes

E.

Tulving

in

The

Missing

Link

in

Cognition

Evolution

of

Self-Knowing

Consciousness

H.

Terrace

J.

Metcalfe

Eds

-LRB-

Oxford

Univ.

Press

New

York

-RRB-

pp.

E.

Tulving

Behav

Brain

Sci

-LRB-

-RRB-

W.

A.

Roberts

Psych

Bull

-LRB-

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T.

Suddendorf

J.

Busby

Trends

Cogn

Sci

-LRB-

-RRB-

C.

Boesch

H.

Boesch

Primates

-LRB-

-RRB-

J.

Chappell

A.

Kacelnik

Anim

Cogn

-LRB-

-RRB-

W.

Kohler

The

Mentality

of

Apes

-LRB-

Routledge

Kegan

Paul

London

-RRB-

N.

J.

Emery

N.

S.

Clayton

Nature

-LRB-

-RRB-

N.

S.

Clayton

J.

Bussey

A.

D.

Dickinson

Nat

Rev.

Neurol

-LRB-

-RRB-

K.

D.

Schick

N.

Toth

Making

Silent

Stones

Speak

-LRB-

Simon

and

Schuster

New

York

-RRB-

T.

Suddendorf

M.

C.

Corballis

Gen.

Soc

Gen.

Psych

Mon.

-LRB-

-RRB-

G.

Gergely

G.

Csibra

Inter

Stud

-LRB-

-RRB-

W.

J.

Bailey

et

al.

Mol

Phylogenet

Evol

-LRB-

-RRB-

Detailed

materials

and

methods

are

available

as

supporting

material

on

Science

Online

G.

A.

Kimble

Conditioning

and

Learning

-LRB-

AppletonCentury-Crofts

New

York

-RRB-

D.

A.

Lieberman

D.

C.

McIntosh

G.

V.

Thomas

J.

Exp

Psych

Anim

Behav

Proc

-LRB-

-RRB-

J.

Garcia

D.

J.

Kimeldorf

R.

A.

Koelling

Science

-LRB-

-RRB-

S.

B.

van

der

Wall

Food

Hoarding

in

Animals

-LRB-

Univ.

of

Chicago

Press

Chicago

IL

-RRB-

C.

P.

van

Schaik

E.

A.

Fox

L.

T.

Fechtman

J.

Hum

Evol

-LRB-

-RRB-

T.

Kano

The

Last

Ape

-LRB-

Stanford

Univ.

Press

Stanford

CA

-RRB-

N.

S.

Clayton

A.

D.

Dickinson

J.

Comp

Psychol

-LRB-

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J.

de

Heinzelin

et

al.

Science

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N.

J.

Emery

N.

S.

Clayton

Science

-LRB-

-RRB-

We

thank

M.

Carpenter

M.

Tomasello

B.

Hare

and

three

anonymous

reviewers

for

their

comments

on

a

previous

version

of

this

manuscript

the

keepers

of

the

Leipzig

Zoo

for

their

help

during

testing

and

K.

Finstermeier

for

drawing

fig

Supporting

Online

Material

Materials

and

Methods

Figs

and

Table

January

accepted

March

science

CO/FT

Regulatory

Module

Controls

Timing

of

Flowering

and

Seasonal

Growth

Cessation

in

Trees

Henrik

Bohlenius

Tao

Huang

Laurence

Charbonnel-Campaa

Amy

M.

Brunner

Stefan

Jansson

Steven

H.

Strauss

Ove

Forest

trees

display

a

perennial

growth

behavior

characterized

by

a

multiple-year

delay

in

flowering

and

in

temperate

regions

an

annual

cycling

between

growth

and

dormancy

We

show

here

that

the

CO/FT

regulatory

module

which

controls

flowering

time

in

response

to

variations

in

daylength

in

annual

plants

controls

flowering

in

aspen

trees

Unexpectedly

however

it

also

controls

the

short-day

induced

growth

cessation

and

bud

set

occurring

in

the

fall

This

regulatory

mechanism

can

explain

the

ecogenetic

variation

in

a

highly

adaptive

trait

the

critical

daylength

for

growth

cessation

displayed

by

aspen

trees

sampled

across

a

latitudinal

gradient

spanning

northern

Europe

rees

have

extended

juvenile

phases

that

can

last

for

decades

before

the

first

flower

is

formed

Trees

can

also

cycle

between

periods

of

growth

and

dormancy

In

temperate

regions

this

involves

a

short-day

induced

growth

cessation

and

bud

set

in

the

fall

after

which

the

tree

enters

a

dormant

state

characterized

by

an

enhanced

cold

tolerance

Tree

populations

-LRB-

provenances

-RRB-

from

northern

latitudes

typically

display

growth

cessation

at

a

longer

critical

daylength

leading

to

earlier

bud

set

during

fall

compared

with

southern

populations

-LRB-

-RRB-

This

is

a

high

T

Umea

Plant

Science

Centre

Department

of

Forest

Genetics

and

Plant

Physiology

Swedish

University

of

Agricultural

Sciences

Umea

Sweden

Tech

Department

of

Forestry

Virginia

Polytechnic

Institute

and

State

University

Blacksburg

VA

USA

Plant

Science

Centre

Department

of

Plant

Physiology

Umea

University

Umea

Sweden

Department

of

Forest

Science

Oregon

State

University

Corvallis

OR

USA

To

whom

correspondence

should

be

addressed

Email

Ove.Nilsson@genfys.slu.se

ly

adaptive

trait

because

it

ensures

that

bud

set

and

dormancy

have

been

induced

well

before

the

risk

of

frost

damage

This

response

is

under

strong

genetic

control

and

is

maintained

when

trees

are

moved

between

latitudes

-LRB-

-RRB-

The

molecular

mechanism

that

controls

growth

cessation

at

different

critical

daylengths

is

not

known

neither

is

the

mechanism

controlling

the

multiple-year

delay

in

flowering

In

the

annual

plant

Arabidopsis

the

genes

CONSTANS

-LRB-

CO

-RRB-

and

FLOWERING

LOCUS

T

-LRB-

FT

-RRB-

are

necessary

for

the

daylength

regulation

of

flowering

inducing

flowering

as

a

response

to

long

days

-LRB-

-RRB-

CO

displays

a

diurnal

regulation

in

which

the

mRNA

accumulation

peaks

at

the

end

of

the

day

in

long

days

and

during

the

night

in

short

days

-LRB-

-RRB-

Furthermore

the

CO

protein

is

extremely

labile

in

darkness

leading

to

an

accumulation

of

CO

protein

only

in

long

days

-LRB-

-RRB-

CO

then

induces

transcription

of

the

gene

FT

in

the

leaf

and

the

FT

mRNA

moves

from

leaf

to

VOL

SCIENCE

shoot

apex

-LRB-

-RRB-

where

the

translated

FT

protein

induces

the

formation

of

flowers

-LRB-

-RRB-

The

FT

mRNA

fulfills

many

of

the

criteria

characterizing

the

elusive

flowerinducing

molecule

Bflorigen

-LSB-

described

in

the

-LRB-

-RRB-

To

determine

whether

a

tree

FT

ortholog

is

also

involved

in

the

regulation

of

flowering

time

in

trees

a

process

that

is

not

obviously

regulated

by

daylength

because

of

their

long

juvenile

phase

or

whether

it

is

involved

in

the

daylength

regulation

of

perennial

growth

and

dormancy

we

have

investigated

the

role

of

the

FT

ortholog

in

Populus

trees

-LRB-

poplars

aspens

and

cottonwoods

-RRB-

We

isolated

the

Populus

trichocarpa

FT

ortholog

which

we

call

-LRB-

fig

-RRB-

and

showed

that

its

function

in

inducing

early

flowering

is

conserved

in

transgenic

Arabidopsis

-LRB-

fig

-RRB-

-LRB-

-RRB-

Populus

trichocarpa

is

difficult

to

transform

but

all

Populus

species

are

closely

related

and

the

sequence

identity

between

homologous

genes

in

different

Populus

species

is

often

-LRB-

-RRB-

Male

Populus

tremula

x

tremuloides

transformed

with

initiated

flowerlike

structures

directly

from

the

Agrobacterium-infected

stem

segments

within

weeks

-LRB-

Fig.

A

and

B

-RRB-

compared

with

the

normal

flowering

time

of

to

years

-LRB-

-RRB-

This

shows

that

is

a

powerful

inducer

of

flowering

in

Populus

Weaker

expressing

lines

could

be

regenerated

and

planted

in

the

greenhouse

These

trees

produced

inflorescences

-LRB-

catkins

-RRB-

-LRB-

Fig.

C

to

E

H

and

I

and

fig

A

to

C

-RRB-

containing

phenotypically

normal

male

flowers

-LRB-

Fig.

F

and

J

-RRB-

with

an

apparently

normal

pollen

development

-LRB-

Fig.

G

and

K

-RRB-

We

also

generated

early-flowering

female

Populus

tremula

with

normal

inflorescence

development

-LRB-

fig

-RRB-

This

is

the

first

report

of

juvenile

transgenic

trees

producing

inflorescences

In

contrast

early-flowering

Populus

ectopically

expressing

MAY

Downloaded

from

on

May

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