The

Perception

of

Rational

Goal-Directed

Action

in

Nonhuman

Primates

Justin

N.

Wood

et

al.

Science

-LRB-

-RRB-

DOI

science

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title

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AAAS

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on

May

REPORTS

genome

size

including

F.

verticillioides

F.

oxysporum

and

F.

solani

have

many

more

ranging

from

to

All

closely

related

species

in

the

F.

graminearum

species

complex

as

well

as

F.

culmorum

also

have

four

chromosomes

which

indicates

that

if

chromosome

fusion

occurred

it

was

not

a

recent

event

The

regions

of

highest

SNP

density

were

significantly

correlated

with

the

regions

of

highest

recombination

-LRB-

P

-RRB-

similar

to

correlations

of

SNP

distribution

or

nucleotide

diversity

with

recombination

frequency

observed

in

humans

and

Drosophila

-LRB-

-RRB-

Additionally

regions

of

high

SNP

density

have

significantly

lower

G+C

content

than

the

rest

of

the

genome

-LRB-

P

-RRB-

The

low

G+C

content

of

internal

regions

further

supports

the

idea

that

these

regions

may

represent

ancestral

telomeres

To

determine

whether

high

diversity

SNP

regions

evolved

recently

we

examined

the

sequence

divergence

of

genes

in

these

regions

We

compared

F.

graminearum

coding

regions

to

those

resulting

from

a

low

coverage

-LRB-

-RRB-

assembly

of

F.

verticillioides

-LRB-

-RRB-

Comparing

the

best

matches

for

F.

graminearum

proteins

from

high

and

low

SNP

density

regions

-LRB-

top

and

bottom

quartiles

-RRB-

to

the

F.

verticillioides

assembly

revealed

that

proteins

from

the

highest

SNP

density

regions

have

fewer

putative

orthologs

compared

with

the

rest

of

the

genome

and

that

these

orthologs

share

lower

identity

-LRB-

-RRB-

Although

variation

in

the

local

mutation

rate

is

expected

to

produce

a

correlation

between

polymorphism

and

divergence

more

polymorphisms

were

found

in

high

SNP

regions

than

predicted

on

the

basis

of

divergence

-LRB-

table

-RRB-

and

the

ratio

of

synonymous

to

nonsynonymous

polymorphisms

is

higher

than

that

of

less

diverse

regions

-LRB-

value

-RRB-

-LRB-

table

-RRB-

Blast

analysis

-LRB-

-RRB-

identified

genes

as

specific

to

F.

graminearum

and

these

show

significant

enrichment

in

the

high-density

SNP

regions

-LRB-

P

-RRB-

We

also

compared

F.

graminearum

with

the

closely

related

F.

asiaticum

F.

boothii

F.

culmorum

and

F.

pseudograminearum

using

genomic

DNA

hybridizations

to

a

F.

graminearum

microarray

-LRB-

-RRB-

and

identified

genes

that

are

F.

graminearum

specific

These

genes

were

overrepresented

-LRB-

by

a

factor

of

-RRB-

in

the

highdensity

SNP

regions

-LRB-

P

-RRB-

These

data

further

demonstrate

that

genomic

regions

exhibiting

the

highest

intraspecific

variability

also

exhibit

the

highest

interspecific

variability

F.

graminearum

genes

specifically

expressed

during

plant

infection

including

predicted

secreted

proteins

major

facilitator

transporters

amino

acid

transporters

and

cytochrome

are

all

overrepresented

in

high

SNP

density

regions

-LRB-

Fig.

table

and

SOM

text

-RRB-

Conversely

genes

predicted

to

be

highly

conserved

such

as

nuclear

encoded

mitochondrial

genes

or

genes

involved

in

translation

are

underrepresented

in

regions

of

high

diversity

-LRB-

table

and

SOM

text

-RRB-

Comparison

of

gene

expression

of

F.

graminearum

infection

on

barley

and

under

varied

nutritional

culture

conditions

-LRB-

-RRB-

identified

genes

as

exclusively

expressed

during

barley

infection

These

genes

are

highly

enriched

in

the

high-SNP-density

regions

-LRB-

P

-RRB-

and

are

predicted

to

be

secreted

representing

enrichment

by

a

factor

of

over

the

genome

as

a

whole

-LRB-

table

and

SOM

text

-RRB-

Four

of

these

genes

have

similarity

to

known

virulence

factors

and

another

genes

are

predicted

plant

cell-wall

degrading

enzymes

-LRB-

table

-RRB-

Among

these

enzymes

are

xylanases

which

degrade

xylan

the

major

hemicellulose

portion

of

monocot

cell

walls

pectate

lyases

which

cleave

pectin

another

essential

component

of

plant

cell

walls

and

cutinases

enzymes

that

hydrolyze

cutin

polyesters

that

coat

all

outer

plant

surfaces

Such

enzymes

may

function

in

the

penetration

and

maceration

of

plant

tissues

and

for

the

acquisition

of

nutrients

from

plant

polymers

-LRB-

-RRB-

and

may

be

involved

as

effector

molecules

that

trigger

host-plant

defense

responses

-LRB-

-RRB-

The

high

genetic

diversity

of

this

group

of

genes

suggests

that

the

fungus

has

a

great

capacity

for

adaptability

and

genetic

change

during

its

interaction

with

even

this

single

host

species

The

completed

genome

of

F.

graminearum

allowed

us

to

identify

distinct

regions

of

high

diversity

We

found

that

these

regions

are

enriched

for

infection-related

genes

which

may

allow

the

fungus

to

adapt

rapidly

to

changing

environments

or

hosts

Recognition

of

these

high-diversity

areas

of

the

genome

focuses

the

direction

of

future

work

toward

those

regions

that

may

have

the

greatest

potential

in

elucidating

the

dynamics

of

host

pathogen

interactions

References

and

Notes

J.

F.

Leslie

B.

A.

Summerell

The

Fusarium

Laboratory

Manual

-LRB-

Blackwell

Ames

Iowa

-RRB-

R.

S.

Goswami

H.

C.

Kistler

Mol

Plant

Pathol

-LRB-

-RRB-

J.

W.

Bennett

M.

Kilch

Clin

Microbiol

Rev.

-LRB-

-RRB-

D.

C.

Chang

et

al.

JAMA

-LRB-

-RRB-

M.

C.

Dignani

E.

Anaissie

Clin

Microbiol

Infect

-LRB-

Suppl

-RRB-

-LRB-

-RRB-

L.

R.

Gale

et

al.

Genetics

-LRB-

-RRB-

Materials

and

methods

are

available

as

supporting

material

on

Science

Online

E.

U.

Selker

E.

B.

Cambareri

B.

C.

Jensen

K.

R.

Haack

Cell

-LRB-

-RRB-

M.

K.

Watters

T.

A.

Randall

B.

S.

Margolin

E.

U.

Selker

D.

R.

Stadler

Genetics

-LRB-

-RRB-

H.

C.

Mefford

B.

J.

Trask

Nat

Rev.

Genet

-LRB-

-RRB-

M.

J.

Gardner

et

al.

Nature

-LRB-

-RRB-

E.

A.

Winzeler

et

al.

Genetics

-LRB-

-RRB-

D.

J.

Begun

C.

F.

Aquadro

Nature

-LRB-

-RRB-

A.

Kong

et

al.

Nat

Genet

-LRB-

-RRB-

U.

Guldener

et

al.

Fungal

Genet

Biol

-LRB-

-RRB-

P.

S.

Solomon

K.-C

Tan

R.

P.

Oliver

Mol

Plant

Pathol

-LRB-

-RRB-

J.

D.

Walton

Plant

Physiol

-LRB-

-RRB-

We

thank

the

Genome

Sequencing

Platform

at

the

Broad

Institute

A.

Rokas

M.

Borowsky

and

G.

Fink

for

critical

reading

of

the

manuscript

D.

Neafsey

M.-J

Daboussi

and

P.

Tiffin

for

helpful

discussions

S.

Gale

H.

Khalili

L.

Gaffney

and

D.

Park

for

technical

assistance

and

Syngenta

for

sharing

their

X

sequence

from

F.

graminearum

and

their

sequence

from

F.

verticillioides

Supported

by

the

National

Research

Initiative

of

the

USDA

Cooperative

State

Research

Education

and

Extension

Service

F.G.D.B.

was

supported

by

the

Austrian

genome

program

GEN-AU

the

Impuls

und

Vernetzungsfonds

der

Helmholtz-Gemeinschaft

and

a

grant

from

the

German

Federal

Ministry

of

Education

and

Research

Sequences

have

been

deposited

in

GenBank

F.

graminearum

assembly

Broad

F.

graminearum

annotation

-LRB-

-RRB-

F.

verticillioides

assembly

SNP

sequences

-LRB-

ss

to

-RRB-

and

hygromycin

Loss/gain

clones

to

Supporting

Online

Material

Materials

and

Methods

SOM

Text

Figs

to

Tables

to

References

April

accepted

July

science

The

Perception

of

Rational

Goal-Directed

Action

in

Nonhuman

Primates

Justin

N.

Wood

David

D.

Glynn

Brenda

C.

Phillips

Marc

D.

Humans

are

capable

of

making

inferences

about

other

individuals

intentions

and

goals

by

evaluating

their

actions

in

relation

to

the

constraints

imposed

by

the

environment

This

capacity

enables

humans

to

go

beyond

the

surface

appearance

of

behavior

to

draw

inferences

about

an

individual

's

mental

states

Presently

unclear

is

whether

this

capacity

is

uniquely

human

or

is

shared

with

other

animals

We

show

that

cotton-top

tamarins

rhesus

macaques

and

chimpanzees

all

make

spontaneous

inferences

about

a

human

experimenter

's

goal

by

attending

to

the

environmental

constraints

that

guide

rational

action

These

findings

rule

out

simple

associative

accounts

of

action

perception

and

show

that

our

capacity

to

infer

rational

goal-directed

action

likely

arose

at

least

as

far

back

as

the

New

World

monkeys

some

million

years

ago

central

characteristic

of

human

action

perception

is

the

capacity

to

read

beneath

the

surface

appearance

of

behavior

When

someone

acts

we

make

inferences

about

A

their

goals

and

intentions

by

referencing

each

action

against

a

backdrop

of

environmental

constraints

In

humans

this

capacity

appears

around

the

first

year

of

life

For

instance

Gergely

SEPTEMBER

VOL

SCIENCE

Downloaded

from

on

May

REPORTS

and

colleagues

-LRB-

-RRB-

showed

that

when

infants

watched

an

experimenter

use

her

head

to

illuminate

a

box

infants

imitated

this

precise

action

only

if

the

experimenter

's

hands

were

free

to

move

and

could

have

been

used

to

illuminate

the

box

if

the

experimenter

's

hands

were

occupied

and

could

not

be

used

then

the

infants

used

their

hands

Infants

most

likely

inferred

that

since

the

experimenter

could

have

used

her

hands

but

used

her

head

instead

the

head

must

confer

some

advantage

for

illuminating

the

box

These

results

and

others

-LRB-

-RRB-

suggest

that

human

infants

assess

whether

an

agent

's

actions

are

rational

by

evaluating

how

the

intervening

environmental

circumstances

constrain

the

achievement

of

a

target

goal

as

such

they

infer

properties

of

mental

life

that

are

not

transparent

from

the

surface

appearance

of

behavior

Presently

unclear

however

is

whether

this

capacity

is

the

product

of

human

evolution

or

uniquely

human

pedagogy

or

rather

is

shared

with

other

animals

Behavioral

and

neurophysiological

studies

show

that

nonhuman

primates

attend

to

subtle

details

of

the

surface

properties

of

actions

including

differences

in

the

gestures

used

to

achieve

a

goal

-LRB-

-RRB-

Further

there

is

suggestive

evidence

that

animals

go

beyond

the

mere

consequences

of

actions

distinguishing

intentional

from

accidental

consequences

-LRB-

-RRB-

For

example

captive

chimpanzees

show

more

heightened

signs

of

frustration

when

an

experimenter

appears

to

tease

intentionally

by

offering

and

then

taking

away

food

as

opposed

to

offering

and

then

clumsily

dropping

food

two

events

with

the

same

consequences

that

is

the

failure

to

obtain

food

-LRB-

-RRB-

In

addition

cotton-top

tamarins

are

more

likely

to

cooperate

with

a

partner

who

gives

food

altruistically

than

with

a

partner

who

gives

food

as

an

accidental

by-product

of

otherwise

selfish

behavior

-LRB-

-RRB-

Moreover

Hare

and

Tomasello

-LRB-

-RRB-

found

that

chimpanzees

can

use

information

about

an

agent

's

apparent

intentions

to

find

hidden

food

in

other

contexts

however

chimpanzees

have

considerable

difficulty

understanding

intentional

cues

by

humans

-LRB-

-RRB-

Thus

these

results

leave

three

questions

unanswered

-LRB-

i

-RRB-

To

what

extent

can

animals

spontaneously

use

information

about

an

agent

's

apparent

intentions

to

make

inferences

about

their

goals

-LRB-

ii

-RRB-

Are

their

inferences

based

solely

on

the

surface

appearance

of

behavior

as

opposed

to

information

about

whether

actions

are

rational

with

regard

to

current

environmental

constraints

-LRB-

iii

-RRB-

What

is

the

phylogenetic

distribution

of

these

capacities

especially

among

our

closest

living

relatives

the

monkeys

and

apes

Department

of

Psychology

Harvard

University

Cambridge

MA

USA

of

Organismic

and

Evolutionary

Biology

Harvard

University

Cambridge

MA

USA

of

Human

Evolutionary

Biology

Harvard

University

Cambridge

MA

USA

of

Psychology

Boston

University

Boston

MA

USA

To

whom

correspondence

should

be

addressed

E-mail

jwood@wjh.harvard.edu

Fig.

Performance

for

choosing

the

container

targeted

by

the

intentional

-LRB-

dark

gray

-RRB-

versus

accidental

-LRB-

light

gray

-RRB-

actions

by

tamarins

rhesus

and

chimpanzees

The

tamarin

data

illustrate

the

mean

percentage

of

trials

-LRB-

SEM

-RRB-

See

fig

for

the

mean

percentage

of

trials

as

measured

by

both

looking

and

grasping

behaviors

The

rhesus

and

chimpanzee

data

illustrate

the

percentage

of

subjects

choosing

the

container

targeted

by

each

action

type

The

dashed

line

indicates

chance

performance

SCIENCE

VOL

SEPTEMBER

Downloaded

from

on

May

To

begin

addressing

these

questions

we

adopted

a

broad

comparative

perspective

conducting

experiments

on

three

nonhuman

primate

species

-LRB-

cotton-top

tamarins

rhesus

macaques

and

chimpanzees

-RRB-

representing

the

three

major

groups

-LRB-

New

World

monkeys

Old

World

monkeys

and

apes

-RRB-

We

tested

all

three

species

in

largely

the

same

way

but

due

to

housing

conditions

and

sample

sizes

there

were

some

differences

-LRB-

-RRB-

In

experiment

we

asked

whether

members

of

these

species

perceive

actions

as

intentional

and

accidental

and

critically

use

this

information

when

making

inferences

about

the

apparent

goal

of

a

human

agent

We

used

a

forced-choice

method

designed

to

measure

subjects

spontaneous

foraging

behavior

in

response

to

actions

performed

by

a

human

experimenter

During

each

trial

an

experimenter

presented

subjects

with

two

potential

food

containers

performed

an

action

on

one

and

then

allowed

the

subject

to

select

one

of

the

containers

In

the

intentional

condition

the

experimenter

reached

directly

for

and

grasped

the

container

In

the

accidental

condition

the

experimenter

flopped

his

hand

onto

the

container

with

palm

facing

upwards

in

a

manner

that

appeared

from

a

human

perspective

accidental

and

non

goal-directed

-LRB-

-RRB-

If

nonhuman

primates

fail

to

distinguish

between

intentional

and

accidental

actions

when

making

inferences

about

others

goals

attending

to

the

mere

association

of

the

hand

and

container

then

they

should

show

the

same

pattern

of

searching

in

both

conditions

that

is

approach

the

experimenter-contacted

container

However

if

they

distinguish

between

intentional

and

accidental

actions

then

they

should

selectively

inspect

the

container

targeted

by

the

experimenter

's

intentional

action

but

not

that

targeted

by

accidental

action

Based

on

the

statistical

methodology

used

in

our

other

studies

of

rhesus

behavior

we

elected

to

use

one-tailed

tests

in

this

work

too

All

three

species

inspected

the

intentionally

targeted

container

a

greater

proportion

of

time

than

the

accidentally

targeted

container

tamarins

-LSB-

F

-LRB-

-RRB-

REPORTS

P

-RSB-

rhesus

-LSB-

-LRB-

N

-RRB-

P

-RSB-

chimpanzees

-LRB-

Wilcoxon

signed

ranks

test

z

P

-RRB-

All

species

selectively

inspected

the

targeted

container

after

observing

the

intentional

action

-LRB-

Fig.

-RRB-

tamarins

-LSB-

t

-LRB-

-RRB-

P

-RSB-

rhesus

-LRB-

out

of

subjects

binomial

probability

P

-RRB-

chimpanzees

-LRB-

out

of

subjects

binomial

probability

P

-RRB-

In

contrast

of

the

species

selectively

inspected

the

targeted

container

after

the

accidental

action

tamarins

-LSB-

t

-LRB-

-RRB-

P

-RSB-

rhesus

-LRB-

out

of

subjects

binomial

probability

P

-RRB-

chimpanzees

-LRB-

out

of

subjects

binomial

probability

P

-RRB-

Thus

tamarins

rhesus

monkeys

and

chimpanzees

spontaneously

distinguish

between

intentional

and

accidental

actions

and

use

this

information

to

make

inferences

about

others

goals

These

results

provide

further

support

for

studies

of

chimpanzees

-LRB-

-RRB-

and

extend

the

pattern

to

tamarins

and

rhesus

In

addition

they

suggest

that

these

three

species

go

beyond

the

mere

association

of

contact

or

the

attention

drawn

to

one

container

to

correctly

infer

the

agent

's

target

goal

How

do

these

species

distinguish

between

intentional

and

accidental

actions

Do

they

do

so

solely

on

the

basis

of

the

surface

appearance

of

behavior

or

like

humans

do

they

interpret

actions

in

relation

to

the

broader

environment

in

which

they

occur

That

is

did

the

subjects

tested

in

experiment

judge

the

hand

grasp

as

goaldirected

and

the

hand

flop

as

accidental

because

grasping

and

flopping

actions

are

automatically

interpreted

as

intentional

and

accidental

respectively

Alternatively

did

they

evaluate

the

hand

flop

as

accidental

because

in

this

particular

situation

the

experimenter

could

have

used

the

more

rational

grasping

action

In

experiment

we

asked

whether

these

three

species

integrate

information

about

the

surface

properties

of

an

action

with

the

environmental

constraints

facing

the

agent

in

order

to

make

inferences

about

rational

goal-directed

action

We

presented

subjects

with

an

experimenter

performing

very

similar

actions

under

two

contrasting

environmental

circumstances

In

the

first

condition

the

experimenter

touched

one

of

the

containers

with

his

elbow

while

the

associated

hand

was

occupied

-LRB-

hand-occupied

-RRB-

in

the

second

contrasting

condition

the

experimenter

performed

the

same

elbow

touch

action

while

the

associated

hand

was

free

-LRB-

handempty

-RRB-

One-half

of

both

the

chimpanzee

and

rhesus

subjects

observed

the

experimenter

perform

the

hand-occupied

elbow

touch

while

holding

an

object

in

his

acting

hand

only

the

other

hand

was

placed

behind

his

back

The

other

half

of

the

subjects

observed

the

experimenter

perform

the

action

while

holding

an

object

in

both

hands

If

nonhuman

primates

evaluate

actions

merely

on

the

basis

of

surface

appearance

-LRB-

e.g.

the

association

between

the

elbow

and

the

container

-RRB-

then

they

should

show

the

same

pattern

of

searching

in

both

the

hand-occupied

and

hand-empty

conditions

because

the

surface

properties

of

the

actions

are

very

similar

including

especially

the

structure

of

the

final

point

of

contact

However

if

these

species

take

into

account

the

environmental

constraints

facing

the

experimenter

then

only

the

hand-occupied

condition

should

be

perceived

as

a

rational

goaldirected

action

given

that

the

experimenter

's

acting

hand

was

occupied

at

the

moment

of

gesturing

his

elbow

provides

an

alternative

means

to

both

indicate

and

contact

the

target

goal

Accordingly

the

hand-empty

condition

would

not

be

perceived

as

a

rational

goal-directed

action

because

at

the

time

the

experimenter

could

have

used

his

unoccupied

acting

hand

to

grasp

and

indicate

the

target

container

-LRB-

as

in

the

intentional

condition

of

experiment

-RRB-

leaving

the

subject

uncertain

as

to

the

target

goal

Therefore

subjects

should

not

infer

that

the

experimenter

's

goal

was

to

contact

the

box

with

the

potentially

concealed

food

We

note

that

our

target

species

do

not

naturally

use

their

elbows

to

indicate

or

draw

attention

to

objects

or

events

in

their

environment

and

nor

have

they

been

trained

to

either

use

their

elbows

in

an

indicative

manner

or

respond

to

this

action

This

condition

therefore

also

explores

their

capacity

to

use

an

indicative

but

unfamiliar

gesture

to

make

inferences

about

goal-directed

action

under

specific

environmental

constraints

All

species

inspected

the

targeted

container

a

greater

proportion

of

the

time

after

observing

the

hand-occupied

versus

the

hand-empty

action

tamarins

-LSB-

F

-LRB-

-RRB-

P

-RSB-

rhesus

-LSB-

-LRB-

N

-RRB-

P

-RSB-

chimpanzees

-LRB-

Wilcoxon

signed

ranks

test

z

P

-RRB-

All

species

selectively

inspected

the

targeted

container

in

the

hand-occupied

condition

-LRB-

Fig.

-RRB-

tamarins

-LSB-

t

-LRB-

-RRB-

P

-RSB-

rhesus

-LRB-

out

of

subjects

binomial

probability

P

-RRB-

chimpanzees

-LRB-

out

of

subjects

binomial

probability

P

-RRB-

In

contrast

of

the

species

selectively

inspected

the

targeted

container

in

the

hand-empty

condition

tamarins

-LSB-

t

-LRB-

-RRB-

P

-RSB-

rhesus

-LRB-

out

of

subjects

binomial

probability

P

-RRB-

chimpanzees

-LRB-

out

of

subjects

binomial

probability

P

-RRB-

Thus

subjects

used

the

elbow

action

as

a

cue

to

find

hidden

food

only

when

the

experimenter

's

acting

hand

was

occupied

and

thus

unavailable

for

gesture

and

action

One

possibility

is

that

in

the

hand-empty

condition

subjects

attended

primarily

to

the

experimenter

's

hand

in

expectation

of

rational

goaldirected

action

when

this

did

not

occur

the

elbow

cue

could

have

gone

unnoticed

or

been

dismissed

as

irrational

and

accidental

In

contrast

when

the

experimenter

's

hands

were

occupied

subjects

may

have

been

particularly

attentive

to

other

body

parts

because

they

became

viable

alternatives

for

rational

goal-directed

action

These

results

-LSB-

along

with

other

evidence

recently

presented

-LRB-

-RRB-

-RSB-

suggest

that

all

these

primate

species

and

possibly

other

animals

as

well

go

beyond

the

surface

appearance

of

behavior

as

well

as

their

own

experiences

acting

on

or

indicating

objects

when

making

inferences

about

others

goals

Like

humans

they

evaluate

others

actions

with

respect

to

environmental

constraints

imposed

on

the

agent

It

is

interesting

that

these

species

perceived

the

hand-occupied

elbow

touch

as

goal-directed

given

that

it

is

impossible

to

pick

up

an

object

with

one

's

elbow

The

most

likely

explanation

for

Fig.

Performance

for

choosing

the

container

targeted

by

the

hand-occupied

-LRB-

dark

gray

-RRB-

versus

handempty

-LRB-

light

gray

-RRB-

elbow

actions

by

tamarins

rhesus

and

chimpanzees

The

tamarin

data

illustrate

the

mean

percentage

of

trials

-LRB-

SEM

-RRB-

See

fig

for

the

mean

percentage

of

trials

as

measured

by

both

looking

and

grasping

behaviors

The

rhesus

and

chimpanzee

data

illustrate

the

percentage

of

subjects

choosing

the

container

targeted

by

each

action

type

The

dashed

line

indicates

chance

performance

VOL

SCIENCE

SEPTEMBER

Downloaded

from

on

May

REPORTS

this

pattern

is

that

subjects

inferred

that

the

experimenter

's

goal

was

to

contact

or

indicate

the

presence

of

food

rather

than

to

grasp

the

food

Given

enough

time

and

leisure

human

adults

are

free

to

consider

almost

any

action

as

irrational

For

instance

the

subjects

in

our

study

and

the

human

infants

in

previous

studies

-LRB-

-RRB-

perceived

uncharacteristic

elbow

and

head

actions

as

rational

and

goal-directed

provided

that

the

experimenter

's

hands

were

occupied

this

response

obtained

even

though

the

experimenter

could

have

dropped

the

object

and

then

performed

the

more

efficient

hand

action

Similarly

our

subjects

showed

the

same

pattern

of

searching

regardless

of

whether

the

hand-occupied

elbow

touch

was

performed

with

both

hands

occupied

or

with

one

hand

behind

the

back

the

latter

condition

is

of

interest

because

the

experimenter

could

have

performed

the

grasping

action

with

the

hand

that

was

behind

his

back

We

suggest

that

at

the

initial

stage

of

action

analysis

rational

actions

are

defined

in

terms

of

current

and

immediate

constraints

on

the

agent

Thus

at

the

moment

the

experimenter

indicates

the

target

object

with

his

elbow

while

one

hand

is

occupied

and

the

other

rests

behind

his

back

the

subject

's

initial

interpretation

is

that

both

of

the

experimenter

's

hands

are

unavailable

This

amendment

to

current

theoretical

models

of

action

perception

makes

sense

of

both

human

-LRB-

-RRB-

and

nonhuman

animal

results

The

present

results

appear

to

contrast

with

previous

studies

indicating

that

chimpanzees

have

difficulty

using

human

pointing

looking

or

many

other

communicative

gestures

to

find

a

hidden

reward

In

particular

in

an

object

choice

task

in

which

an

experimenter

conceals

a

piece

of

food

in

one

of

two

or

more

hiding

locations

several

studies

reveal

that

captive

chimpanzees

-LRB-

-RRB-

as

well

as

other

primates

-LRB-

-RRB-

generally

fail

to

use

a

human

agent

's

pointing

gesture

and

direction

of

eye

gaze

to

correctly

infer

the

location

of

hidden

food

We

can

not

precisely

pinpoint

the

exact

nature

of

the

differences

between

these

studies

and

the

present

one

However

support

for

the

chimpanzee

results

is

aided

by

the

converging

evidence

from

tamarins

and

rhesus

based

on

similar

methods

Our

results

support

three

primary

conclusions

that

bear

on

the

origins

and

nature

of

action

perception

restricted

to

these

three

primate

species

but

potentially

generalizable

to

other

closely

and

distantly

related

species

First

the

species

tested

are

highly

sensitive

to

the

surface

properties

of

observed

actions

All

three

species

selectively

inspected

a

potential

food

source

targeted

by

the

experimenter

's

action

after

observing

the

hand

grasp

action

but

not

after

observing

the

hand

flop

action

A

low-level

explanation

in

terms

of

attention

via

eye

gaze

body

position

or

other

social

cues

can

not

explain

these

results

given

that

in

both

experiments

contact

with

the

target

container

and

the

experimenter

's

visual

attention

were

held

constant

but

subjects

patterns

of

search

differed

Second

results

show

that

tamarins

rhesus

and

chimpanzees

distinguish

between

goaldirected

and

accidental

behavior

based

on

the

relation

between

actions

and

environmental

constraints

This

finding

has

notable

implications

for

cognitive

and

neurobiological

models

of

action

understanding

Physiological

studies

of

macaque

mirror

neurons

in

area

of

the

premotor

cortex

indicate

that

these

cells

activate

both

when

the

subject

acts

and

when

this

same

subject

observes

another

acting

in

the

same

way

-LRB-

-RRB-

On

the

basis

of

these

activation

patterns

theorists

have

suggested

that

the

mirror

neuron

system

plays

a

critical

role

in

action

perception

where

organisms

interpret

the

actions

of

others

by

appealing

to

their

own

actions

-LRB-

-RRB-

Current

neurobiological

models

of

the

mirror

neuron

system

often

state

that

action

understanding

consists

of

mapping

the

surface

properties

of

observed

actions

onto

the

observer

's

motor

system

Our

results

show

however

that

action

perception

can

not

be

based

solely

on

a

mechanism

that

analyzes

the

surface

properties

of

actions

In

experiment

subjects

distinguished

between

hand-occupied

and

hand-empty

elbow

touches

even

though

these

actions

have

similar

surface

properties

and

are

not

within

the

repertoire

of

actions

performed

by

these

species

Thus

action

perception

must

also

consist

of

a

mechanism

that

evaluates

action

means

in

relation

to

goals

and

places

this

analysis

into

a

broader

context

that

entails

constraints

imposed

by

the

current

environmental

situation

As

a

result

some

system

must

supplement

the

mirror

neuron

circuitry

to

provide

a

fuller

account

of

action

perception

in

primates

Third

the

psychological

mechanisms

underlying

the

socio-cognitive

abilities

of

animals

have

been

widely

debated

often

acting

as

a

proxy

for

larger

debates

between

supporters

of

associative

as

opposed

to

more

mentalistic

accounts

of

animal

learning

and

behavior

Associative

models

classically

explain

behavior

as

a

result

of

direct

reinforcement

history

for

example

the

capacity

to

understand

actions

as

goal-directed

may

be

the

product

of

learning

acquired

by

forming

associations

between

observed

actions

and

the

objects

that

they

target

Such

models

can

not

explain

the

present

findings

without

modification

In

experiment

all

three

species

perceived

an

elbow

touch

as

goal-directed

despite

presumably

having

little

or

no

experience

witnessing

other

agents

manipulate

objects

with

their

elbow

when

their

hands

were

occupied

and

certainly

no

experience

with

other

conspecifics

indicating

objects

with

their

elbows

consequently

there

was

no

opportunity

to

form

an

association

between

this

action

and

object-directed

outcomes

Thus

we

suggest

that

nonhuman

primates

ability

to

perceive

actions

as

goal-directed

extends

beyond

these

associative

mechanisms

drawing

upon

inferences

about

an

agent

's

goals

in

the

context

of

particular

environmental

constraints

In

sum

our

results

show

that

both

closely

and

distantly

related

primate

species

distinguish

between

goal-directed

and

accidental

actions

when

making

inferences

about

another

individual

's

apparent

goals

Furthermore

they

do

so

by

SCIENCE

VOL

evaluating

the

rationality

of

the

action

in

relation

to

the

constraints

of

the

situation

The

fact

that

these

results

hold

across

three

different

primate

species

and

that

the

methods

entail

spontaneous

nontrained

responses

adds

substantially

to

the

robustness

of

our

findings

and

their

implications

for

thinking

about

the

evolution

of

action

perception

We

conclude

that

our

capacity

to

perceive

rational

goal-directed

actions

is

not

uniquely

human

having

evolved

at

least

as

far

back

as

the

New

World

monkeys

some

million

years

ago

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Notes

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Gergely

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G.

Csibra

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Cognition

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Schwier

C.

van

Maanen

M.

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M.

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Rizzolatti

L.

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M.

K.

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L.

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Behav

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R.

Anderson

M.

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R.

Anderson

P.

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H.

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Anim

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We

are

grateful

to

L.

Pharoah

R.

Atencia

K.

Brown

and

the

Jane

Goodall

Institute

USA

and

staff

to

Tchimpounga

Sanctuary

for

their

help

and

ethusiasm

with

our

research

In

particular

we

appreciate

the

hard

work

of

the

animal

caregivers

J.

Maboto

B.

Moumbaka

A.

Sitou

M.

Makaya

B.

Bissafi

C.

Ngoma

W.

Bouity

J.

Tchikaya

L.

Bibimbou

A.

Makosso

C.

Boukindi

G.

Nzaba

B.

Ngoma

We

also

appreciate

permission

from

the

Congolese

Ministere

de

la

Recherche

Scientifique

et

de

l'Innovation

Technique

for

allowing

us

to

conduct

our

research

in

their

country

This

publication

was

made

possible

by

grant

from

the

National

Center

for

Research

Resources

-LRB-

NCRR

-RRB-

a

component

of

NIH

Its

contents

are

solely

the

responsibility

of

the

authors

and

do

not

necessarily

represent

the

official

views

of

NCCR

or

NIH

Further

support

comes

from

an

NIH

National

Research

Service

Award

-LRB-

NRSA

-RRB-

to

J.N.W.

-LRB-

grant

-RRB-

a

National

Science

Foundation

Human

and

Social

Dynamics

-LRB-

NSF-HSD

-RRB-

grant

a

Guggenheim

Fellowship

and

gift

from

J.

Epstein

to

M.D.H.

We

thank

M.

Gerald

for

facilitating

our

work

on

Cayo

Santiago

and

F.

Cushman

B.

Hare

N.

Kanwisher

J.

Rubin

L.

Santos

and

R.

Saxe

for

comments

on

the

data

and

earlier

drafts

of

this

paper

Supporting

Online

Material

Materials

and

Methods

Figs

and

References

Movies

to

May

accepted

July

science

SEPTEMBER

Downloaded

from

on

May

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 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 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 O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O 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 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 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 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 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 O O O O O O O O O O O O O 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 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

rationality evolution primates cognition

imitation
reasoning
monkey
practical
non linguistic rationality
social cognition
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