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Abstract

: The concept of attention as central to human performance extends back to the start of experimental psychology, yet even a few years ago, it would not have been possible to outline in even a preliminary form a functional anatomy of the human attentional system. New developments in neuroscience have opened the study of higher cognition to physiological analysis, and have revealed a system of anatomical areas that appear to be basic to the selection of information for focal (conscious) processing. The importance of attention is its unique role in connecting the mental level of description of processes used in cognitive science with the anatomical level common in neuroscience. Sperry describes the central role that mental concepts play in understanding brain function. As is the case for sensory and motor systems of the brain, our knowledge of the anatomy of attention is incomplete. Nevertheless, we can now begin to identify some principles of organization that allow attention to function as a unified system for the control of mental processing. Although many of our points are still speculative and controversial, we believe they constitute a basis for more detailed studies of attention from a cognitive-neuroscience viewpoint. Perhaps even more important for furthering future studies, multiple methods of mental chronometry, brain lesions, electrophysiology, and several types of neuro-imaging have converged on common findings.
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The
Attention
System
of
the
Human
Brain
12.
PERSONAL
ALTi..ORM5
Michael
I.
Posner
and
Steven
E.
Petersen
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5
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Technical
mom
7/1/88
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February
28,
1989
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The
concept
of
attention
as
central
to
human
performance
extends
back
to
the
start
of
experimental
psychology
(James,
1890j,
yet
even
a
few
years
ago,
it
would
not
have
been
possible
to
outline
in
even
a
preliminary
form
a
functional
anatomy
of
the
human
attentional
system.
New
developments
in
newrmscience
(+H-lfnrd
&
Picton,
4987;
Raichle,
1983;
Wurtz,
Goldberg
&
Robinson,
1980)
have
opened
the
study
of
highcr
cognition
to
physiological
analysis,
and
have
revealed
a
system
of
anatomical areas
that
appear
to
be
basic
to
the
selection
of
information
for
focal
(conscious)
processing.
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1.
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89
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x
(Submitted
to
the
Annals
of
Neuroscience,
1989)
The
Attention
System
of
the
Human
Brain
ONR
Technical
Report
#89-1
Michael
I.
Posner
Department
of
Psychology
University
of
Oregon
Eugene,
OR
97403
and
Steven
E.
Petersen
Department
of
Neurology
and
Neurological
Surgery
Washington
University
School
of
Medicine
660
S.
Euclid,
Box
8111
St.
Louis,
MO
63110
B
-n
-n-o
Availability
Codes
;
-Avai'l
and/or
IDist
Special
/
INTRODUCTION
-
lrhe
concept
of
attention
as
central
to
human
performance
extends
back
to
the
start
of
experimental psychology,
(,&mes,-44W,90
yet
even
a
few
years
ago,
it
would
not have
been
possible
to
outline
in
even
a
preliminary
form
a
functional
anatomy
of
the
human
attentional
system.
New
developments
in
neuroscience
'-'.
2
-Picroa,--1-9S7,-
Raichk,-t983;
Wurtz-Goldberg-&
R
-
have
opened
the
study
of
higher
cognition
to
physiological
analysis,
and
have
revealed
a
system
of
anatomical
areas
that
appear
to
be
basic
to
the
selection
of information
for
focal
(conscious)
processing.
The
importance
of
attention
is
its
unique
role
in
connecting
the
mental
level
of
description
of
processes
used
in
cognitive
science
with
the
anatomical
level
common
in
nearoscience.
Sperry
tV98
'describes
the
central
role that
mental
concepts
play
in
understanding
brain
function.
as-
foHows:
"control
from below upward
is
retained
but
is
claimed
to
not
furnish
the
whole
story.
The
full
explanaticn
requires
that
one
take
into
account
new,
previously
nonexistent,
emergent
properties,
including
the
mental,
that interact
causally
at
their
own
higher
level
and
also
exert
causal
control
from
above
downward."
(p.
609)
If
there
is
hope
of
exploring causal
control of
brain systems
by
mental
states,
it
must
lie
through
an
understanding
of
how
voluntary
control
is
exerted
over
more
automatic
brain
systems.
We
argue
that
this
can
be
approached
through
understanding
the human
attentional
system
at
the
levels
of
both
cognitive
operations
and
of
neuronal
activity.
As
is
the
case
for
sensory
and
motor
systems
of
the brain,
our
knowledge
of
the
anatomy
of
attention
is
incomplete.
Nevertheless,
we
can
now
begin
to
identify
some
principles
of
organization
that
allow
attention
to
function
as
a
unified
system
for the
control
of
mental
processing.
Although
many
of
our
points
are
still
speculative
and
controversial,
we
believe
they
constitute
a
basis
for
more
detailed
studies
of attention
from
a
cognitive-neuroscience
viewpoint.
Perhaps
even
more
important
for
furthering
future
studies,
multiple
methods
of
mental
chronometry,
brain
lesions,
electrophysiology,
and
several
types
of
neuroimaging
have
converged
on
common
findings.
.
Three
fundamental
findings
are
basic
to
this
chapter.
First,
the
attention
system
of
the
brain
is
anatomically
separate
from
the
data
processing
systems
that
2
perform
operations
on
specific
inputs even
when
attention
is
oriented
elsewhere.
In
this
sense,
the
attention
system
is
like
other
sensory
and
motor systems.
It
interacts
with
other
parts
of
the
brain,
but
maintains
its
own
identity.
SeconC,
attention
is
carried
out
by
a
network of
anatomical
areas.
It
is
neither
the
property
of
a
single
center,
nor
is
it
a
general
function
of
the
brain operating
as
a
whole
(Mesulam,
1981;
Rizzolatti,
Gentilucci
&
Matelli,
1985).
Third,
the areas
involved
in
attention carry
out
different
functions,
and
these
specific
computations
can
be
specified
in
cognitive
terms
(Posner,
Petersen,
Fox
&
Raichle,
1988).
To
illustrate
these
principles,
it
is
important
to
divide
the
attenDti
systC
i-z
subsystems
that perform
different
but
interrelated
functions.
In
this
chapter,
we
consider
three
major
functions
that
have
been
prominent
in
cognitive
accounts
of
attention
(Posner
&
Boies,
1971):
(1)
orienting
to
sensory
events;
(2)
detecting
signals
for
focal
(conscious)
processing,
and
(3)
the
maintenance
of
a
vigilant
or
alert
state.
For
each
of
these subsystems,
we
adopt
an
approach that organizes
the
known
information
around
a
particular
example.
For orienting,
we use
visual locations
as
the
model,
because
of
the
large amount
of
work
done
with this
system.
For
detecting,
we
focus
on
reporting
the
presence
of
a
target
event.
We
think
this
system
is
a
general
one
that
is
important for
detection
of
information
from
sensory
processing
systems
as
well
as
information stored
in
memory.
However
the
extant
data
concern
primarily
the
detection
of
visual
locations
and
processing
of
auditory
and
visual
words.
For
alerting,
we
discuss
situations
in
which
one
is
required
to
prepare
for
processing
of
high
priority
target
events
(Posner,
1978).
For
the
subsystems
of
orienting,
detecting
and
alerting,
we
review
the
known
anatomy,
the
operations
performed,
and
the
relationship of attention
to
data
processing
systems
(e.g.
visual
word
forms,
semantic
memory)
upon
which
that
attentional
subsystem
is
thought
to
operate. Thus
for
orienting,
we
review
the
visual
attention
system
in
relationship
to
the
data
processing
systems
of
the
ventral
occipital
lobe.
For
detecting,
we
examine
an
anterior
attention
system
in
relationship
to
networks
that subserve
semantic
associations.
For
alerting,
we
examine
arousal
systems
in
relationship
to
the
selective
aspects
of
attention.
Insofar
as
possible,
we
draw
together evidence
from
a
wide
variety
of
methods,
rather
than
arguing for the
primacy
of
a
particular
method.
ORIENTING
Visual
Loations
3
Visual
orienting
is
usually
defined
in
terms
of
the
foveation
of
a
stimulus
(overt).
Foveating
a
stimulus
improves
efficiency
of
processing
targets
in
terms
of
acuity,
but
it
is
also
possible
to
change
the
priority
given
a
stimulus
by
attending
to
its
location covertly
without
any
change
in
eye
or
head
position
(Posner,
1988).
If
a
person
or monkey
attends
to
a
location,
events
occurring
at
that
location
are
responded
to
more
rapidly
(Eriksen
&
Hoffman,
1972;
Posner,
1988),
give
rise
to
enhanced
scalp
electrical activity
(Mangoun
&
Hillyard,
1987),
and
can
be
reported
at
a
lower
threshold (Bashinski
&
Bachrach,
1980;
Downing,
1988).
This
improvement
in
efficiency
is
found
within
the
first
150
millisec after
an
event
occurs
at
the
attended
location.
Similarly,
if
people
are
asked
to
move
their
eyes
to
a
target,
an
improvement
in
efficiency
at
the
target
location
begins well
before
the eyes
move
(Remington,
1980).
This
covert
shift
of
attention
appears
to
function
as
a
way
of
guiding
the
eye
to an
appropriate
area
of
the
visual
field
(Fischer
&
Breitmeyer,
1987;
Posner
&
Cohen,
1984).
The
sensory
responses
of
neurons
in
several
areas
of
the
brain
have
been
shown
to
have
a
greater
discharge
rate
when
a
monkey
attends
to
the
location
of
the
stimulus,
than
when
the monkey
attends
to
some
other
spatial
location.
Three
areas
particularly
identified
with
this
enhancement
effect
are
the
posterior
parietal
lobe
(Mountcastle,
1978;
Wurtz,
Goldberg
&
Robinson,
1980),
the
lateral
pulvinar
nucleus
of
the
postereolateral
thalamus
(Petersen,
Robinson
&
Morris,
1987) and the
superior
colliculus.
Similar
effects
in
the
parietal
cortex
have
been
shown
in
normal
humans
using
positron
emission
tomography
(Petersen,
Fox
&
Raichle,
1988).
While
brain
injuries
to
any
of
these
three
areas
in
human
subjects
will
cause
a
reduction
in
the
ability
to
shift
attention covertly
(Posner,
1988),
each
area
seems
to
produce
a
somewhat
different
type
of
deficit.
Damage
to
the
posterior
parietal
lobe
has
its
greatest
effect
on
the
ability
to
disengage
from
an
attentional
focus
to
a
target
located
in
a
direction opposite
to
the
side
of
the
lesion
(Posner,
1988).
Patients
with
a
progressive
deterioration
in
the
superior
colliculus
and/or
surrounding
areas
also show
a
deficit
in
the
ability
to
shift
attention.
In
this
case,
the
shift
is
slowed
whether
or
not
attention
is
first
engaged
elsewhere.
This finding
suggests
that
a
computation
involved
in
moving
attention
to
the
target
is
impaired.
Patients
with this
damage
also
return
to
former target
locations
as
readily
as
to
fresh
locations
that
have
not
recently
been
attended.
Normal
subjects
and
patients
with
parietal
and
other cortical
lesions
have
a
reduced
probability
of
returning
attention
to
already
examined
locations (Posner,
1988;
Posner
&
Cohen,
1984).
These
two
4
deficits
appear
to
be
those
most
closely
tied
to
the
mechanisms
involved
with
saccadic
eye
movements.
Patients
with
lesions
of
the thalamus
and
monkeys
with
chemical
injections
into
the
lateral pulvinar
also
show
difficulty
in
covert
orienting
(Petersen,
Robinson
&
Morris,
1987;
Posner,
1988).
This
difficulty
appears
to
be
in
engaging attention
on
a
target
on
the side
opposite
the lesion
so
as
to
avoid
being
distracted
by
events
at
other
locations.
A
study
of
patients
with
unilateral
thalamic
lesions
showed slowing
of
responses
to
a
cued
target
on
the
side
opposite
the
lesion
even
when
the subject
had
plenty
of
time
to
orient there.
This
contrasted
with
the
results
found
with
parietal
and
midbrain
lesions,
where
responses
are
nearly
normal
on
both
sides
once
attention
has
been
cued
to
that
location.
Alert
monkeys
with chemical
lesions
of
this
area
made
faster
than
normal
responses
when
cued
to
the
side
opposite
the
lesion
and
given
a
target
on
the
s:de
of
the
lesion,
as
though
the
contralateral
cue
was
not
effective
in
engaging
their
attention
(Petersen,
Robinson
&
Morris,
1987). They
were
also
worse
than
normal
when
given
a
target
on
the
side
opposite
the
lesion,
irrespective
of
the
side
of
the
cue.
It
appears
difficult
for
tbalamic lesioned
animals
to
respond
to
a
contralateral
target
when
another
competing
event
is
also
present
in
the
ipsilateral
field
(R.
Desimone,
personal
communication).
Data
from normal
human
subjects
required
to
filter
out irrelevancies,
showed
selective
metabolic
increases
in
the
pulvinar
contralateral
to
the
field
required
to
do
the
filtering
(LaBerge
&
Buchsbaum.
1988).
Thalamic
lesions
appear
to
give
problems
in
engaging
the
target
location
in
a
way
that allows
responding
to
be
fully
selective.
These
findings
make
two
important points.
First,
they
confirm
the
idea
that
anatomical
areas carry
out
quite
specific
cognitive
operations.
Second,
they suggest
a
hypothesis
about
the
circuitry
involved
in
covert
visual
attention
shifts
to
spatial
locations.
The
parietal
lobe
first
disengages
attention
from
its
present
focus,
then the
midbrain
area
acts to move
the
index
of
attention
to
the area
of
the
target
and the
pulvinar
is
involved
in
reading
out
data
from
the
indexed
locations.
Further
studies
of alert
monkeys
should
provide
ways
of
testing
and
modifying
this
hypothesis.
Hemispheric
Differences
The
most
accepted
form
of
cognitive
localization,
resultiag
from
studies
of
split
brain
patients
(Gazzaniga,
1970),
is
the
view
that
the
two
hemispheres
perform
different
functions.
Unfortunately,
in
the
absence
of
methods
to
study
more
detailed
localization,
the
literature
has
tended
to
divide
cognition
into
various
dichotomies
assigning
one
to
each
hemisphere.
As
we
develop
a
better
understanding
of
how
5
cognitive
systems
(e.g.
attention)
are
localized,
hemispheric
dominance
may
be
treated
in
a
more
differentiated
manner.
Just
as
we
can
attend
to
locations
in
visual
space,
it
is
also
possible
to
concentrate attention
on
a
narrow
area
or
to
spread
it
over
a
wider
area
(Eriksen
&
Yeh,
1985).
To
study
this
issue,
Navon
(1978)
formed
large
letters
out
of
smaller
ones.
It
has
been
found
in
many
studies
that
one
can
concentrate
attention
on
either
the
small
or
large
letters
and
that
the
attended
stimulus
controls
the
output
even
though
the
unattended
letter still
influences
performance.
The
use
of
small
and
large
letters
as
a
method
of
directing
local
and
global
attention
turns
out
to
be
related
to
allocation
of
visual
channels
to
different
spatial
frequencies.
Shulman
&
Wilson.
(1987)
showed
that
when
attending
to
the
large
letters,
subjects
are
relatively
more
accurate
in
the
perception
of
probe
grating
of
low
spatial
frequency
and
this
reverses
when
attending
to
the small
letters.
There
is
evidence
from the
study
of
patients
that
the
right
hemisphere
is
biased toward
global
processing
(low
spatial
frequencies)
and
the
left
for
local
processing
(high
spatial
frequencies)
(Robertson
&
Delis,
1986;
Sergent,
1987).
Right
hemisphere patients
may
copy
the
small
letters
but miss
the
overall
form,
while
those
with
left
hemisphere lesions
copy
the
overall
form
but
miscopy
the
constituent
small
letters.
Detailed
chronometric
studies
of
parietal
patients
reveal
difficulties
in
attentional
allocation
so
that
right hemisphere
patients attend poorly
to
the
global
aspects
and
left
hemisphere
to
the local
aspects
(Robertson,
Lamb
&
Knight,
1988).
These
studies
support
a
form
of
hemispheric
specialization within
the
overall
structure
of
the
attention
system.
The
left
and
right hemisphere
both
carry
out
the
operations
needed
for
shifts
of
attention
in
the
contralateral
direction,
but
they have
more
specialized
functions
in
the
level
of
detail
to
which
attention
is
allocated.
It
is
likely
that
these
hemispheric
specializations
are not
absolute
nor
innate.
Rather
they
are
probably
relative
and
emerge
over
time,
perhaps
in
conjunction
with
the
development
of
literacy.
The
general
anatomy
of
the
attention
system
that
we
have
been
describing
lies
in
the
dorsal visual
pathway
that
has its
primary
cortical
projection
area
in
V1
and
extends
into
the
parietal
lobe (see
figure
1).
A
major
aspect
of
the
study
INSERT
FIG
1
of
attention
is
to
see
how
attention
could
influence
the
operations
of
other
cognitive
systems
such
as
are
involved
in
the
recognition
of
visual
patterns.
The
visual
6
pattern
recognition
system
is
thought
to
involve
a
ventral
pathway,
stretching
from
V1
to
th:
infratemporal
cortex. Anatomically,
these
two
areas
of
the
brain
can
be
coordinated
through
the
thalamus
(pulvinar)
(Petersen,
Robinson
&
Morris,
1987),
or
through
other
pathways
(Zeki
&
Shipp,
1988).
Functionally,
attention
might
be
involved
in
various
levels
of
pattern recognition,
from
the
initial
registration
of
the
features
to
the
storage
of
new
visual
patterns.
Pattern
Recoanition
VISUAL
SEARCH
All
neurons
are
selective
in
the
range
of
activation
to
which
they
will respond.
The
role
of
the
attention
system
is
to
modulate
this
selection
for
those
types
of
stimuli
that
might
be
most
important
at
a
given
moment.
To
understand
how
this
form
of
modulation
operates,
it
is
important
to
know how
a
stimulus
would
be
processed without
the
special
effects
of
attention.
In
cognition, unattended
processing
is
called
"automatic"
to
distinguish
it from
the
special
processing
that
becomes
available
with
attention.
We
have
learned
quite
a
bit
about
the automatic
processing
that
occurs
in
humans along
the
ventral
pathway
during recognition
of
visual
objects
(Posner,
1988;
Treisman
&
Gormican,
1988).
Treisman
has
shown
that search
of
complex
visual
displays
for
single
features
can
take
place
in
parallel
with
relatively little
effect
of
the
number
of
distractors.
When
a
target
is
defined
as
a
conjunction
of
attributes
shared with
distractors that
are
themselves
heterogeneous
(Duncan
&
Humph
reys,
in
press),
the
search
process
becomes
slow,
effortful
and
serial.
We
know
from
cognitive studies
(LaBerge
&
Brown,
1988;
Treisman
&
Gormican,
1988)
that
cueing
people
to
locations
influences
a
number
of
aspects
of
visual
perception.
Treisman
has
shown
that
when
attempting
to
conjoin features,
subjects
use
focal
attention,
and
it has
also
been
shown
that
spreading
focal
attention
among
several
objects
leads
to
a
tendency
for
misconjoining
features
within
those
objects,
regardless
of
the
physical
distance
between
them (Cohen
&
Ivry,
1989).
Thus,
attention
not
only
provides
a
high
priority
to
attended
features,
but
does
so
in
a
way
that
overrides
even
the
physical
distance
between
objects within
the
focus
of
attention.
While
these
reaction
time
results
are
by
no
means
definitive
markers
of
attention,
there
is
also
evidence
from
studies
with brain
lesioned
patients
that
support
a
role
of
the
visual
spatial
attention
system.
These
clinical studies
examine
the
ability
of
patients
to
bisect
lines
(Riddoch
&
Humphreys,
1983),
search
complex
visual
patterns
(Riddoch
&
Humphreys,
1987),
or
report
strings
of
letters
(Friedrich,
7
Valker
&
Posner,
1985;
Sieroff, Pollatsek
&
Posner,
1988).
Damage
to
the
posterior
)arietal
lobe
appears
to
have
specific influences
on
these
tasks.
Patients
with
right
)arietal
lesions
frequently
bisect
lines
too
far
to
the
right
and
fail
to
report
the
left
nost
letters
of
a
random
letter
string
(Sieroff,
Pollatsek
&
Posner,
1988).
However,
hese
effects
are
attentional
not
in
the
recognition
process
itself.
Evidence for
this
is
hat
they
can
frequently
be
corrected
by
cueing
the
person
to
attend
covertly
to
the
,eglected
side
(Riddoch
&
Humphreys,
1983;
Sieroff,
Pollatsek
&
Posner,
1988).
The
:ues
appear
to
provide
time
for
the
damaged
parietal
lobe
to
disengage
attention
and
thus
compensates
for
the
damage.
It
is
also
possible
to
compensate
by
substituting
a
word
for
a
random
letter
string.
Patients
who
fail
to
report
the
left
most
letters
of
a
random
string
will
often
do
so
correctly
when
it
makes
a
word. If
cues work
by
directing
attention,
they
should
also
influence
normal
performance.
Cues
presented
prior
to
a
letter
string
do
improve
the
performance of
normals for
nearby
letters,
but
cues
have
little
or
no
influence
on
the
report
of
letters
making
words
(Sieroff
&
Posner,
1988).
Blood
flow
studies
of
normal
humans
show
that
an
area
of
the
left
ventral occipital
lobe
is
unique
to
strings
of letters
that
are
either
words
or
orthographically
regular
nonwords
(A.
Snyder,
S.E.
Petersen,
P.T.
Fox,
&
M.E.
Raichle,
personal
communication).
This
visual
word form area
(see
Figure
1)
appears
to
operate
without
attention,
and
this confirms
other
data
that
recognition
of
a
word
may
be
so
automated
as
not
to
require
spatial attention,
while
the
related
tasks
of
searching
for
a
single
letter,
forming
a
conjunction,
or
reporting
letters
from
a
random
string
do
appear
to
rely
upon
attention.
Studies
of
recording
from
individual
cells
in
aiert
monkeys
confirm
that
attention
can
play
a
role
in
the
operation
of
the
ventral
pattern
recognition system
(Wise
&
Desimone,
1988).
It
appears
likely
that
the
pathway
by
which
the
posterior
a.:ention
system
interacts
with
the
pattern
recognition
systew
is
through
the
thalamus
(Petersen,
Robinson,
&
Morris,
1987).
This
interaction
appears
to
require
about
90
millisec since
cells
in
V4
begin
to
respond
to
unattended
ltermq
within their
receptive
field, but
shut
these
unattended
areas
off
after
90
msec
(Wise
&
Desimone,
1988).
Detailed
models
of
the
nature of
the
interaction
between
attention
and
pattern recognition
are
just
beginning
to
appear
(Crick,
1984;
LaBerge
&
Brown,
1988).
IMAGERY
In
most
studies
of
pattern recognition,
the
sensory
event begins
the
process.
However,
it
is
possible
to
instruct
human
subjects
to
take
information
from
their
long
term
memories
and
construct
a
visual
representation
(image)
that
they
might then
inspect
(Kosslyn,
1988).
This
higher
level
visual
function
is
called
imagery.
The
importance
of
imagery
as
a
means
of
studying
mechanisms
of
high
level
vision
has
not
been
well
recognized
in
neuroscience.
When
imagery
can
be
8
iployed
as
a
means
of
studying vision,
it
allows
more
direct
access
to
the
higher
vels
of
information processing
without
contamination
from lower
levels.
There
is
now
considerable
evidence
that
some
of
the
same
anatomical
mechanisms
are
ed
in
imagery
as
are
involved
in
some
aspects
of
pattern
recognition
(Farah,
1988;
3sslyn,
1988).
Patients
with
right
parietal
lesions,
who show
deficits
in
visual
ienting
of
the
type
that
we
have
described
above,
also
fail
to
report
the
intralesional
side
of
visual
images
(Bisiach,
Luzzatti
&
Perani,
1981). When
asked
imagine
a
familiar
scene, they
make
elaborate reports
of
the
right
side
but
not
the
ft. The
parts
of
the
image
that
are
reported
when
facing
in
one
direction
are
-glected
when
facing
in
the
other.
This
suggests
that
the
deficit
arises
at
the
time
scanning
the
image.
When
normal
subjects
imagine
themselves
walking
on
a
familiar
route,
blood
ow
studies
show
activation
of
the
superior parietal
lobe
on
both
sides
(Roland,
?85).
Although
many
other
areas
of
the
brain
are
also
active
in
this
study,
most
of
tern
are
common
to
other verbal
and
arithmetical
thoughts,
but
activation
of
the
iperior
parietal
lobe
seems more
unique
to
imagery.
As
discussed
previously,
the
arietal
lobe seems
to
be
central
to
spatial
attention
to
external
locations.
Thus,
it
ppears
likely
that
the
neural
systems
involved
in
attending
to
an
external
location
re
closely related
to
those
used
when
subjects
scan
a
visual
image.
,NTERIOR
ATTENTION
SYSTEM
In
her
paper
on
the
topography
of
cognition,
Goldman-Rakic
(1988)
describes
le
strong
connectionb
between the
posterior parietal
lobe
and
areas
of
the
lateral
ad
medial
frontal
cortex.
This
anatomical
organization
is
appealing
as
a
basis
for
elating
what
has
been
called
involuntary
orienting
by
Luria
(1973),
and
what
we
ave
called
the
posterior
attention
system,
to
focal
or
conscious
attention.
Cognitive
studies
of
attention
have
often
shown
that
detecting
a
target
roduces widespread
interference
with
most
other cognitive
operations
(Posner,
978).
It
has been
shown
that
monitoring
many
spatial
locations
or
modalities
roduces
little
or
no
interference
over
monitoring
a
single
modality,
unless
a
target
ccurs
(Duncan,
1980).
This
finding
supports
the
distinction
between
a
general
alert
Late,
and
one
in
which
attention
is
clearly
oriented
and
engaged
in
processing
,formation.
In
the
alert
but
disengaged
state,
any
target
of
sufficient
intensity
has
ttle
trouble
in
summoning
the
mechanisms
that
produce
detection.
Thus
monitoring
iultiple
modalities
or locations
produce only small
amounts
of
interference.
The
nportance
of
engaging
the
focal
attention
system
in
the
production
of
widespread
iterference
between
signals
supports
the
idea
that there
is
a
unified system
9
involved
in
detection
of
signals
regardless
of
their
source.
As
a
consequence
of
detection
of
a
signal
by
this
system,
we
can
produce
a
wide
range
of
arbitrary
responses
to
it.
We
take
this
ability
to
produce
arbitrary
responses
as
evidence
that
the
person
is
aware
of
the
signal.
Evidence
that there
are
attentional
systems
common
to
spatial orienting
as
well
as
orienting
to
language
comes
from
studies
of
cerebral
blood
flow
during cognitive
tasks.
Roland
(1985)
has
reported
a
lateral
superior frontal
area which
is
active
both
during
tasks
involving
language
and
in
spatial
imagery
tasks.
However,
these
studies
do
not
provide
any
clear
evidence
that
such
common
areas
are
part
of
an
attentional
system.
More
compelling
is
evidence
that
midline
frontal
areas,
including
the
anterior
cingulate
gyrus
and
the
supplementary
motor area,
are
active
during
semantic
processing
of
words
(Petersen,
et
al,
1988),
and
that
the
degree
of
blood
flow
in
the
anterior cingulate
increases
as
the number
of
targets
to
be
detected
increases (Posner
et
al,
1988).
Thus,
the
anterior
cingulate
seems
to
be
particularly
sensitive
to
the
operations
involved
in
target
detection.
The
anterior cingulate
gyrus
is
one
of
the
areas
reported
by
Goldman-Rakic
(1988)
to
have
alternating
bands
of
cells
that
are
labelled
by
injections
into
the
posterior
parietal
lobe
and
the
dorsolateral
prefrontal cortex.
These
findings
suggest
that
the
anterior cingulate
should
be
shown
to
be
important
in
tasks
requiring
the
posterior
attention
system
as
well
as
in
language
tasks.
It
has
often
been
argued
from
lesion
data
that
the
anterior cingulate
plays
an
important
role
in
aspects
of
attention
including
neglect
(Mesulam,
1980;
Mirsky,
1987).
Does
attention
involve
a
single unified
system,
or
should
we
think
of
its
functioning
as
being
executed
by
separate
independent
systems?
One
way
to
test
this
idea
is
to
determine whether
attention
in
one
domain
(e.g. language)
affects
the
ability
of
mechanisms
in
another
domain
(e.g.
orienting
toward
a
visual location).
If
the
anterior
cingulate
system
is
important
in
both
domains,
there
should
be
a
specific
interaction
between
even remote domains
such
as
these
two.
Studies
of
patients
with
parietal
lesions
(Posner,
Inhoff,
Freidrich
&
Cohen,
1987)
showed
that
when
they were
required
to
monitor
a
stream
of
auditory
information
for
a
sound,
they
were
slowed
in
their
ability
to
orient
toward
a
visual
cue.
The
effect of
the
language
task
was
rather
different
than
engaging
attention
at
a
visual
location
because
its
effects
were
bilateral rather
than being
mainly
on
the
side
opposite
the
lesion. Thus,
the
language task appeared
to
involve
some
but
not all
of
the
same
mechanisms that
were
used
in
visual
orienting.
10
This
result
is
compatible
with the view
that
visual
orienting
involves
separate
ut
interconnected systems
with those
used
for
language
processing.
A
similar
result
as
found with
normal
subjects
when
they
were
given
visual
cues while
shadowing
a
auditory
message
(Posner,
Sandson,
Dhawan
&
Shulman,
1989).
Here,
the
effects
f
the
language
task
were most marked
for
cues
in
the
right
visual
field,
as
though
ie
common
system might
have
involved
lateralized
mechanisms
of
the
left
emisphere. These
findings fit
with
the
close
anatomical
links between
the
anterior
ingulate
and
the
posterior
parietal
lobe on
the
one
hand
and
language
areas
of
the
iferal
frontal
lobe
on
the
other.
They
suggest
to
us
a
possible hierarchy
of
attention
ystems
in
which
the
anterior
system
can
pass
control
to
the
posterior
system
when
is
not occupied with
processing
other
material.
A
spotlight
analogy
has
often
been used
to
describe
the
selection
of
information
om
the
ventral
pattern
recognition
system
by
the
posterior
attention
system
rreisman
&
Gormican,
1988).
A
spotlight
is
a
very
crude
analogy
but
it
does
apture
some
of
the
dynamics
involved
in
disengaging,
moving
and
engaging
ttention.
This
analogy
can
be
stretched
still
further
to
consider
aspects
of
^he
iteraction
between
the
anterior
attention
system
and
the
associative
network
hown
to
be
active
during processing
of
semantic
associates
and
categories
by
studies
f
cerebral
blood
flow
(Petersen
et
al,
1988).
INSERT
FIG 2
ABOUT
HERE
'he
temporal dynamics
of
this
type
of
interaction
between
attention
and
semantic
ctivatign
has
been
described
in
some
detail
(Posner,
1978; 1982).
LERTING
An
important
atantional
function
is
the
ability
to
prepare
and
sustain
lertness
to
process
high
priority
signals.
The
relationship
between
the
alert
state
nd
other
aspects
of
information processing
has been
worked out
in
some
detail
for
-tter
and
word
matching
experiments
(Posner,
1978).
The
passive
activation
of
iternal
units
representing
the
physical
form
of
a
familiar
letter,
its
name,
and
even
s
semantic
classification
(e.g.
vowel)
appears
to
take
place
at
about
the
same
rate,
'hether
subjects
are
alert
and
expecting
a
target,
or
whether
they
are at
a
lower
:vel
of
alertness because
the
target
occurs
without warning.
The
alert
state
roduces
more
rapid
responding,
but
this
increase
is
accompanied
by
a
higher error
ite.
It
is
as
though
the
build-up
of
information
about
the
classification of
the
target
ccurs
at
the same
rate
regardless
of
alertness,
but
in
states
of
high
alertness,
the
election
of
a
response occurs
more
quickly,
based
upon
a
lower
quality
of
11
information,
thus
resulting
in
an
increase
in
errors.
These
results
led
to
the
conclusion
that
alertness
does
not
affect
the
build-up
of
information
in
the
sensory
or
memory
systems,
but
does
affect
the
rate
at
which
attention
can
respond
to
that
stimulus
(Posner,
1978).
Anatomical
evidence
has
accumulated
on
the
nature
of
the
systems producing
a
change
in
the
alert
state.
One
consistent
finding
is
that
the
ability
to
develop
and
maintain
the
alert
state
depends
heavily
upon
the
integrity
of
the
right
cerebral
hemisphere
(Heilman,
Watson
&
Valenstein,
1985).
This
finding
fits
very
well
with
the
clinical
observation
that
patients
with
right
hemisphere lesions
more
often
show
signs
of
neglect
and
has
sometimes
led
to
an
idea
that
all
of
spatial
attention
was
controlled
by
the
right hemisphere. However,
the
bulk
of
the
evidence
discussed
below seems
to
associate
right hemisphere
dominance
with
tasks
dependent
upon
the
alert state.
Lesions
of
the
right
cerebral
hemisphere
cause
difficulty
with
alerting.
This
has
been
shown
using
galvanic
skin
responses
in
humans
and
monkeys
(Heilman,
Watson,
&
Valenstein,
1985),
and
for
heart
rate
responses
to
warning
signals
(Yokoyama,
Jennings,
Acles,
Hood
&
Boiler,
1987).
Performance
in
vigilance
tasks
is
also
more
impaired
with
right
rather
than
left
lesions
(Coslett,
Bowers
&
Heilman,
1987;
Wilkins,
Shallice
&
McCarthy, 1987). It
has
also
been
observed
in
split
brain
patients
that
vigilanct
is
poor
when
information
is
presented
to
the
isolated
left
hemisphere,
out
is
reiatively
good when
presented
to
the
isolated
right
hemisphere
(Dimond
&
Beaumont,
1973).
In
summary,
it
is
as
though
the
isolated
right
hemisphere
contains
the
mechanism
needed
to
maintain
the
alert state
so
that
when
lesioned,
it
reduces
performance
of
the
whole organism.
Studies
of
cerebral
blood
flow
and
metabolism
involving vigilance
tasks
have
also
uniformly
shown
the
importance
of
areas
of
the
right
cerebral
hemisphere
(Cohen,
Semple, Gross, Holcomb,
Dowling
&
Nordahl,
1988;
Deutsch,
Papanicolaou,
Bourbon
&
Eisenberg,
1988;
J.
Pardo,
P.T.
Fox
&
M.E.
Raichle, personal
communication).
Other
attention
demanding activity,
for
example,
semantic
tasks,
and
even
imagery
tasks,
do
not
uniformly
show
greater activation
of
the
right
hemisphere (Petersen
et
al,
1988;
Roland, 1985)..
Thus, blood flow
and
metabolic
studies
also
argue
for
a
tie
between
the
right
cerebral
hemisphere
and
alerting.
Some
of
these
studies
provide
somewhat
better
localization.
Cohen
et
al.
found
an
area
of
the
midfrontal cortex
that
appears
to
be
the
most
active
during their
auditory
discrimination
task. This
is
an
area
also
found
to
be
active
in
both
visual
and
somatosensory vigilance conditions
(J.
Pardo,
et
al,
personal communication).
It
is
of
special
interest
that
Cohen
et
al.
report
that
the
higher metabolic
activation
they
"[I -
I
i
I
I
12
found
in
the
right
prefrontal cortex
was
accompanied
by
reduced
activation
in
the
anterior
cingulate.
If one
views
the
anterior
cingulate
as
related
to
target
detection,
this
makes
sense.
In
tasks
where
one
needs
to
suspend
activity
while
waiting
for
low
probability signals,
it
is
important
not
to
interfere
with
detecting
the
external
signal.
Subjectively,
one
feel.
empty
headed,
due to
the
effort
to
avoid
any
thinking
that
will
reduce the
ability
to
detect
the next signal.
There
is
evidence
that
the
maintenance
of
the
alert state
is
dependent
upon
right
hemisphere
mechanisms,
and
also
that
it
is
closely
tied
with
attention.
These
two
facts
both
suggest
the
hypothesis
that
the
norepinephrine
(NE)
system
arising
in
the
locus
coerulues
may
play
a
crucial role
in
the
alert
state.
In
a
review
of
animal
studies,
Aston-Jones, Foote
and
Bloom
(1984)
argue
that
NE
cells play
a
role
in
changes
in
arousal
or
vigilance. Moreover,
Robinson
(1985)
has
shown
that
lesions
of
the
right
cerebral
hemisphere
lead
to
depletion
of
NE
on
both
sides,
and
that
the
effects
are
strongest
with
lesions
near
the
frontal
pole.
These
findings
are
consistent
with
the
idea
that
NE
pathways
course
through
frontal
areas,
dividing
as
they
go
backward
toward
posterior
areas.
Thus,
an
anterior
lesion
would
have
a
larger
effect.
Recently,
Morrison
and
Foote
(1986) have
studied
the
parts
of
the
posterior
visual system
that are
most
strongly innervated
by
NE
pathways.
They find
that
in
monkeys
NE
innervation
is
most
strongly
present
in
the
posterior
parietal
lobe,
pulvinar
and
superior colliculus.
These
are
the
areas
related
to
the
posterior
attention
system.
Much
weaker
innervation
was
found
in
the
geniculo-striate
pathway
and
along the
ventral
pattern recognition
pathway.
These
findings
support
the
ideas
that
NE
pathways
provide
the
basis
for
maintaining
alertness,
and
that
they
act most
strongly
on
the
posterior
attention
systems
of
the
right cerebral
hemisphere.
In
accord with
these
ideas,
Posner
et
al.
(1987)
found
that
patients
with
right parietal
lesions
had
much
greater
difficulty
in
maintaining
their alertness
in
the
absence
of
a
warning
signal
than
those
with
left
parietal
lesions
or
normal
subjects
did.
Clark,
Geffen
&
Geffen
(1989)
have
found
that manipulation
of
NE
levels
by
drugs
had
specific
effects
on
attention
shifting.
In
smmary,
alertness
involves
a
specific
subsystem
of attention that
acts
on
the
posterior
attention
system
to
support
visual
orienting
and
probably
also
influences other
attentional
subsystems. Physiologically,
this
system depends
upon
the
NE
pathways
that
arise
in
the
LC
and
which
are
more
strongly
lateralized
in
the
right
hemisphere.
Functionally,
activation
of
NE
works
through
the
posterior
attention
system
to
increase
the
rate
at
which
high
priority
visual
information
can
be
t I I I I i . I i _ I J -I,
13
selected
for
further
processing.
This
more
rapid
selection
is
often
at
the
expense
of
lower
quality
information
and
produces
a
higher
error
rate.
CONSEQUENCES
Study
of
attention
from
a
neuroscience viewpoint
has
been impeded
because
attention
has
been
thought
of
as
a
vague,
almost
vitalistic
capacity,
rather
than
as
the
operation
of
a
separate
set
of
neural
areas
whose
interaction
with
domain
specific
systems
(e.g.
visual
word form,
or
semantic
association)
is
the
proper
subject
for
empirical
investigation.
Even
a
crude
knowledge
of
the
anatomy
of
the
selective
attention
system
has
a
number
of
important
consequences
for
research.
It
allows
closer coordination
between
brain
imaging
studies,
using
human
subjects
and
animal
studies
involving
recording
from
individual cells.
In
the
case
of
the
posterior
attention
system,
we
have
hypotheses about
the
connections
between
neural systems
that
can
best
be
tested
and
expanded
by
studies
designed
to
work
out
the
connections
at the
cellular
level.
At
higher levels,
coordinated
studies
of
PET
and
ERP
imaging
may
tell
us
more
details about communication
between
posterior
visual
word
form
systems
and
anterior
semantics,
and
how
attention
is
involved
in
this
form
of
information
transfer.
A
systems
level
analysis
provides
a
framework
for
the
more
detailed
studies
that
must
follow.
A
number
of
recent
observations
depend
upon
a
better
understanding of
how
attention
relates
to
semantic
activation.
In
the
psychological
literature,
there
is
a
continuing
effort
to
understand
the
limits
to
automatic priming
of
semantic
systems
(Posner,
1982).
In
the study
of
sleep,
we
find
challenging
new
hypotheses
that
tell
us
that
during
sleep,
ongoing
neural
activity
may
be
interpreted
semantically
by
networks
primed
by
daily
activity
(Hobson,
1988).
Similarly, research
on
split
brain
subjects
(Gazzaniga,
1970)
has
led
to
the
idea
of
an
interpreter
system
present
in
the
left hemisphere
that
attempts
to
impose
an
explanation
to
the
behavior
of
the self
and
others.
Patients
with lesions
of
the
hippocampus,
who show
no
memory
that
can
be
retrieved
consci.,usly,
are
able
to
demonstrate
detailed storage
by
their
performance
(Squire,
1986).
This implies
that
for
memory,
as
for
performance,
the
distinction
between
automatic
and
conscious processing
marks
different
neural
mechanisms.
Finally, there
are
many
disorders
of
higher
level
cognition
that
are said
to
be
due
to
deficits
of
attention.
These
include
neglect,
schizophrenia,
closed
head
injury,
and
attention
deficit
disorder,
among
others.
The
concept
of
an
attentional
system
of
the
brain
with
specific
operations allocated
to
distinct
anatomical
areas allows
new
14
approaches
to
these
pathologies.
One
such
example
is
the
proposal
that
a
core
deficit
in
schizophrenia
is
a
failure
of
the
anterior
attention
system
of
the
left
hemisphere
to
impose the
normal
inhibitory
pattern
on
the
left
lateralized
semantic network (Early,
Posner,
Reiman
&
Raichle,
1989).
This
proposal
provides
specific
ideas
on
integration
at
the level
of
neurotransmission,
anatomy
and
cognition.
Similar
ideas
may
link
attention
deficit
disorder
to
the
right
hemisphere
mechanisms
that control
sustaining
of
attention.
It
seems
apparent
that
a
combined
cognitive
and
anatomical
approach
may
be
useful
in
integrating
the
long
separate
physiological
and
psychosocial
influences
on
psychopathology.
REFERENCE
LIST
Aston-Jones,
G.,
Foote,
S.L.,
Bloom,
F.E.
1984.
Anatomy
and
physiology
of
locus
coeruleus
neurons:
functional implications.
In
Frontiers
of
Clinical
Neuroscience
Vol.
2,
ed.
M.G.
Ziegler.
Baltimore:
Williams
&
Wilkins.
Bashinski,
H.S.,
Bachrach,
R.T.
1984.
Enhancement
of
perceptual
sensitivity
as
the
result
of
selectively
attending
to
spatial
locations.
Percept
&
Psychophys.
2.'241-248.
Bisiach,
E.,
Luzzatti,
C.,
Perani,
D.
1981.
Unilateral neglect,
representational
schema
and
consciousness.
Brain.
102757-765.
Clark,
C.R.,
Geffen,
G.M.,
Geffen,
L.B.
In
press.
Catecholamines
and
the
covert
orienting
of
attention.
Neuropsvchol.
Cohen,
A.
&
Ivry,
R.
In
press.
Illusory
conjunctions
inside
and
outside
the
focus
of
attention.
J.
Exp.
Psychol:
Human
Perc.
&
Perf.
Cohen,
R.M.,
Semple,
W.E.,
Gross,
M.,
Holcomb,
H.J.,
Dowling,
S.M.
Nordahl,
T.E.
1988.
Functional
localization of sustained
attentin.
Neuropsych. Neuropsychol.
and
B
h
Nerl
L3-20.
Coslett,
H.B.,
Bowers,
D.,
Heilman,
K.M.
1987.
Reduction
in
cerebral
activation
after
right
hemisphere
stroke.
Neuro.L
37:957-962.
Crick,
F.
1984.
Function
of
the
thalamic
reticular
complex:
the
searchlight
hypothesis.
Proc.
Nat.
Acad.
of Sci,, 81:4586-4590.
Deutsch,
G.,
Papanicolaou,
A.C.,
Bourbon,
T.,
Eisenberg,
H.M.
1988.
Cerebral
blood
flow
evidence
of
right
cerebral
activation
in
attention
demanding
tasks.
Int.
J.
of.xrsLci
36:23-28.
Dimond,
S.J.,
Beaumont,
J.G.
1973.
Difference
in
the
vigilance
performance
of
the
right
and
left hemisphere.
Cortex.
9:259-265.
Downing,
C.J.
1988.
Expectancy
and
visual-spatial
attention
effects
on
vision. L
Exp.
Psycholh
Hum
Percep.
and
Perf.,
14:188-197.
Duncan,
J.
1980.
The
locus
of
interference
in
the
perception of
simultaneous
stimuli.
syc.h..
.,
87:
272-300.
Duncan,
J.,
Humphreys,
G.W.
In
press. Visual
search
and
stimulus
similarity.
Psychol.
Rey.
Early,
T.,
Posner,
M.I.,
Reiman,
E.,
Raichle,
M.E.
In
press.
Left
striato-pallidal
hyperactivity
in
schizophrenia.
Psychiat.
Develop.
Eriksen,
C.W.,
Hoffman,
J.E.
1972.
Temporal
and
spatial characteristics
of selective
encoding
from
visual displays.
Percept.
&
Psychophys.. 12:201-204.
Eriksen,
C.W. &
Yeh,
Y.
1985.
Allocation
of
attention
in
the
visual
field.
I.Exq-
Psychol:
Hum
Percept
&
Perf.. 11:583-597.
Farah,
M.J.
1988.
Is
visual
imagery
really visual? Overlooked evidence
from
neuropsychology.
P
95:307-317.
Fischer,
B.,
Breitmeyer,
B.
1987.
Mechanisms
of
visual
attention
revealed
by
saccadic
eye
movements.
Neuropsychol
25
IA:73-84.
Friedrich,
F.J.,
Walker,
J.,
Posner,
M.I.
1985.
Effects
of
parietal
lesions
on
visual
matching.
Cog.
Neuropsychol..
2:253-264.
Gazzaniga,