Cerebral

Cortex

February

doi

Advance

Access

publication

June

Large-Scale

Gamma-Band

Phase

Synchronization

and

Selective

Attention

Sam

M.

Alexa

B.

Keiichi

and

Lawrence

M.

Psychophysics

and

Cognitive

Neuroscience

Laboratory

Department

of

Psychology

University

of

British

Columbia

Vancouver

Canada

for

Dynamics

of

Emergent

Intelligence

RIKEN

Brain

Science

Institute

Saitama

Japan

and

Research

Centre

University

of

British

Columbia

Vancouver

Canada

Explaining

the

emergence

of

a

coherent

conscious

percept

and

an

intentional

agent

from

the

activity

of

distributed

neurons

is

key

to

understanding

how

the

brain

produces

higher

cognitive

processes

Gamma-band

synchronization

has

been

proposed

to

be

a

mechanism

for

the

functional

integration

of

neural

populations

that

together

form

a

transitory

large-scale

task

and/or

percept-specific

network

The

operation

of

this

mechanism

in

the

context

of

attention

orienting

entails

that

cortical

regions

representing

attended

locations

should

show

more

gamma-band

synchronization

with

other

cortical

areas

than

would

those

representing

unattended

locations

This

increased

synchronization

should

be

apparent

in

the

same

time

frame

as

that

of

the

deployment

of

attention

to

a

particular

location

In

order

to

observe

this

effect

we

made

electroencephalogram

recordings

while

subjects

attended

to

one

side

or

the

other

of

the

visual

field

-LRB-

which

we

confirmed

by

event-related

potential

analysis

-RRB-

and

calculated

phase-locking

statistics

between

the

signals

recorded

at

relevant

electrode

pairs

We

observed

increased

gamma-band

phase

synchronization

between

visual

cortex

contralateral

to

the

attended

location

and

other

widespread

cortical

areas

approximately

ms

after

the

directional

cue

was

presented

confirming

the

prediction

of

a

large-scale

gamma

synchronous

network

oriented

to

the

cued

location

Keywords

alpha

attention

EEG

gamma

neural

synchrony

Introduction

Performance

of

the

myriad

perceptual

and

cognitive

processes

of

which

the

brain

is

capable

requires

transient

functional

coupling

and

subsequent

decoupling

of

specific

task-relevant

neural

populations

Gamma-band

synchronization

is

a

plausible

mechanism

for

the

selection

and

integration

of

such

neuronal

groups

-LRB-

e.g.

Varela

et

al.

-RRB-

Direct

brain

recordings

show

that

increased

gamma-band

synchronization

within

a

cortical

area

occurs

most

strongly

between

columns

representing

information

that

is

being

integrated

for

example

between

columns

representing

features

of

a

common

object

-LRB-

Gray

and

Singer

Gray

et

al.

Engel

Kreiter

et

al.

-RRB-

Stimulus-specific

gamma

synchronization

has

been

observed

between

monkey

and

between

and

extrastriate

motion

areas

and

between

left

and

right

hemisphere

of

cats

-LRB-

Engel

Konig

and

Singer

Engel

Konig

et

al.

Frein

et

al.

-RRB-

The

summation

of

such

gamma

synchronous

activation

yields

increased

gamma-band

power

in

the

electroencephalogram

-LRB-

EEG

-RRB-

and

has

been

experimentally

linked

to

a

wide

range

of

cognitive

processes

including

attention

learning

and

memory

and

visual

and

auditory

perception

-LRB-

Ward

Kaiser

and

Lutzenberger

-RRB-

Human

EEG

recordings

also

reveal

increased

long-range

gamma-band

synchrony

between

task-relevant

brain

areas

The

Author

Published

by

Oxford

University

Press

All

rights

reserved

For

permissions

please

e-mail

journals.permissions@oxfordjournals.org

during

associative

learning

mental

rotation

conscious

recollection

visual

working

memory

and

coherent

perception

-LRB-

Tallon-Baudry

et

al.

Miltner

et

al.

Rodriguez

et

al.

Bhattacharya

et

al.

Burgess

and

Ali

Gruber

et

al.

-RRB-

Such

results

support

the

hypothesis

that

gammaband

synchronization

enables

the

selective

activation

of

a

functionally

coupled

ensemble

of

neuronal

groups

relevant

for

the

performance

of

a

particular

task

and

for

binding

the

features

of

an

object

into

a

unified

percept

-LRB-

Engel

and

Singer

Varela

et

al.

-RRB-

Of

more

specific

relevance

to

the

present

experimental

paradigm

the

deployment

of

covert

attention

in

humans

has

been

linked

to

changes

in

local

oscillatory

synchronization

in

the

alpha

band

Covert

deployment

of

visuospatial

attention

entails

that

attended

areas

in

the

visual

field

receive

enhanced

processing

whereas

ignored

areas

are

suppressed

-LRB-

e.g.

Posner

et

al.

-RRB-

Whereas

EEG

studies

have

traditionally

focused

on

the

enhanced

processing

of

attended

targets

relative

to

unattended

distractors

-LRB-

for

a

review

see

Gazzaniga

et

al.

-RRB-

recent

research

has

focused

on

the

anticipatory

biasing

of

the

cortex

after

attention

has

been

deployed

to

a

location

but

before

the

appearance

of

the

target

Attending

to

one

visual

hemifield

yields

a

sustained

increase

of

alpha-band

EEG

activation

over

the

ipsilateral

visual

cortex

a

process

thought

to

accomplish

the

suppression

of

distractors

-LRB-

Worden

et

al.

Sauseng

et

al.

Kelly

et

al.

-RRB-

Moreover

these

lateralized

changes

in

local

oscillatory

activity

have

been

shown

to

determine

the

speed

of

detection

for

subsequently

appearing

targets

-LRB-

Thut

et

al.

-RRB-

Cortical

gamma-band

activity

conversely

appears

to

be

relevant

for

the

enhanced

processing

of

attended

information

as

studies

using

implanted

electrodes

and

human

EEG

have

shown

that

local

gamma

synchrony

is

increased

by

selective

attention

-LRB-

Tiitinen

et

al.

Fries

et

al.

Gobbele

et

al.

-RRB-

Such

evidence

taken

together

with

the

data

cited

above

implicating

gamma-band

synchronization

in

feature

binding

and

transient

functional

connectivity

between

brain

areas

and

the

assumption

that

many

of

the

effects

of

attention

would

seem

to

require

transient

functional

coupling

between

select

populations

of

cortical

neurons

leads

to

the

hypothesis

that

large-scale

gamma-band

synchrony

might

play

an

important

role

in

selective

attention

As

mentioned

earlier

the

allocation

of

attention

to

one

location

results

in

certain

advantages

being

given

to

stimuli

appearing

at

that

location

relative

to

those

at

unattended

locations

Specifically

attended

stimuli

are

promoted

for

processing

in

cortical

regions

responsible

for

higher

cognition

and

are

biased

for

inclusion

in

consciousness

a

highly

integrated

yet

apparently

anatomically

distributed

state

-LRB-

Treisman

Tononi

-RRB-

Attention

also

produces

more

effective

feature

binding

both

within

and

across

sensory

modalities

For

example

attended

stimuli

avoid

illusory

conjunctions

and

receive

feature

binding

that

can

be

absent

for

unattended

stimuli

-LRB-

for

reviews

see

Treisman

Wright

and

Ward

-RRB-

Accordingly

cortical

areas

representing

attended

loci

must

be

biased

for

inclusion

in

a

large-scale

functional

network

to

support

the

enhanced

feature

binding

higher

processing

and

propensity

for

conscious

experience

that

stimuli

appearing

at

such

a

locus

of

attention

are

known

to

receive

We

hypothesized

that

longrange

gamma-band

synchronization

mediates

this

transient

functional

network

enabling

the

increased

communication

between

cortical

areas

representing

attended

loci

and

other

diverse

cortical

regions

and

creating

a

preparatory

network

for

the

enhanced

processing

of

attended

stimuli

To

test

this

hypothesis

we

recorded

EEG

while

subjects

were

engaged

in

a

covert

attention-orienting

task

Our

specific

a

priori

hypothesis

was

that

when

attention

was

deployed

endogenously

to

one

side

of

visual

space

electrodes

over

the

contralateral

visual

cortex

would

show

increased

gamma-band

phase

synchronization

with

other

widespread

cortical

areas

indexing

the

establishment

of

the

predicted

long-range

gamma

synchronous

attentional

network

We

also

predicted

that

this

would

occur

in

the

same

time

frame

as

that

uncovered

in

behavioral

studies

of

endogenous

orienting

that

is

beginning

around

ms

after

cue

onset

-LRB-

see

Wright

and

Ward

-RRB-

Moreover

we

expected

that

the

establishment

of

this

long-range

network

would

occur

in

coordination

with

reciprocal

changes

in

local

alpha-band

and

gamma-band

activation

-LRB-

see

Ward

-RRB-

Figure

Stimulus

display

and

its

time

course

-LRB-

not

drawn

to

scale

for

clarity

-RRB-

See

text

for

measurement

intervals

for

synchrony

and

ERP

analyses

Methods

Thirteen

healthy

adults

-LRB-

males

-RRB-

with

normal

or

corrected-to-normal

vision

participated

in

the

experiment

after

giving

written

informed

consent

-LRB-

approved

by

University

of

British

Columbia

Behavioral

Research

Ethics

Board

mean

age

years

standard

deviation

-LSB-

SD

-RSB-

years

-RRB-

Subjects

were

seated

with

eyes

approximately

cm

from

a

computer

monitor

and

were

instructed

to

maintain

fixation

on

a

plus

sign

in

the

center

of

the

screen

An

arrow

cue

appeared

at

the

center

of

the

screen

replacing

the

fixation

plus

to

instruct

subjects

to

covertly

attend

to

a

box

either

to

the

left

or

to

the

right

-LRB-

visual

angle

laterally

-RRB-

of

fixation

on

a

given

trial

-LRB-

see

Fig.

-RRB-

Arrow

cues

-LRB-

by

visual

angle

-RRB-

were

presented

for

ms

after

which

the

fixation

point

-LRB-

by

visual

angle

-RRB-

reappeared

Targets

were

presented

in

boxes

-LRB-

by

visual

angle

-RRB-

which

were

positioned

below

the

plane

of

fixation

-LRB-

Fig.

-RRB-

Either

a

or

an

-LRB-

probability

-RRB-

would

appear

in

one

of

the

boxes

-LRB-

probability

-RRB-

ms

after

the

cue

onset

-LRB-

rectangular

distribution

to

produce

random

jitter

both

to

reduce

the

overlap

of

event-related

potentials

-LRB-

ERPs

-RRB-

from

the

cue

on

those

to

the

target

and

to

reduce

the

effects

of

evoked

neural

sources

on

phase

synchrony

measures

-RRB-

Target

stimuli

were

presented

for

ms

and

subtended

a

visual

angle

of

by

Subjects

were

instructed

to

make

a

button-press

response

if

they

detected

a

but

not

if

they

detected

an

in

the

cued

location

and

to

make

no

response

if

either

stimulus

appeared

at

the

uncued

location

This

paradigm

was

adapted

from

that

of

an

earlier

study

-LRB-

Worden

et

al.

-RRB-

and

was

chosen

because

it

successfully

produced

lateralized

changes

in

ongoing

local

power

following

the

deployment

of

spatial

selective

attention

The

EEG

was

recorded

from

electrodes

positioned

at

standard

locations

plus

electrodes

at

nonstandard

sites

near

the

inion

The

electro-oculogram

-LRB-

EOG

-RRB-

was

recorded

bipolarly

with

electrodes

positioned

cm

from

the

outer

canthi

of

both

eyes

and

above

and

below

the

right

eye

Electrode

impedances

were

kept

below

kX

-LRB-

sufficient

because

of

amplifier

input

impedance

GX

-RRB-

EEG

and

EOG

were

amplified

with

a

gain

of

band-pass

filtered

between

and

Hz

digitized

at

Hz

and

stored

on

disk

for

analysis

Scalp

voltages

were

referenced

to

the

right

mastoid

Synchrony

Analysis

Four

subjects

were

excluded

for

the

synchrony

analysis

due

to

particularly

noisy

data

in

the

postcue

period

and/or

in

the

high

frequency

domain

-LRB-

both

of

which

are

irrelevant

for

the

ERP

analysis

mean

age

of

the

analyzed

subjects

years

SD

years

males

-RRB-

Epochs

for

the

synchrony

analysis

were

extracted

from

ms

before

the

cue

until

ms

after

its

onset

After

deleting

any

epochs

containing

ocular

or

nonocular

artifacts

-LRB-

identified

by

the

automatic

rejection

algorithm

in

EEGLAB

Delorme

and

Makeig

-RRB-

epochs

for

the

left

cue

and

epochs

for

the

right

cue

remained

for

all

subjects

combined

ranging

from

to

epochs

per

subject

per

cue

condition

The

data

in

the

retained

epochs

were

band-pass

filtered

digitally

at

Hz

intervals

between

and

Hz

-LSB-

passband

f

f

where

f

represents

the

filter

frequency

e.g.

at

Hz

the

passband

was

from

-LRB-

-RRB-

to

-LRB-

-RRB-

Hz

-RSB-

Then

using

algorithms

in

the

MATLAB

Signal

Processing

Toolbox

we

calculated

the

analytic

signal

i

t

t

f

t

if

t

A

t

e

of

the

filtered

waveform

for

each

epoch

f

-LRB-

t

-RRB-

to

obtain

the

instantaneous

phase

-LRB-

t

-RRB-

and

amplitude

A

-LRB-

t

-RRB-

at

each

sample

point

-LRB-

points

per

pffiffiffiffiffi

epoch

-RRB-

where

f

t

is

the

Hilbert

transform

of

f

-LRB-

t

-RRB-

and

i

-LRB-

Pikovski

et

al.

-RRB-

Instantaneous

amplitudes

from

this

analysis

represent

the

envelope

of

the

filtered

waveform

and

are

roughly

equivalent

to

Fourier

amplitudes

except

that

they

are

estimated

for

each

instant

in

time

rather

than

as

an

average

over

a

sliding

window

We

interpreted

these

amplitudes

as

reflecting

variations

in

local

neural

synchrony

in

the

various

frequency

bands

much

as

do

power

spectral

densities

-LRB-

Fourier

amplitude

squared

-RRB-

from

a

Fourier

analysis

We

measured

long-range

neural

phase

synchrony

by

calculating

phase-locking

values

-LRB-

PLVs

-RRB-

both

for

individual

data

and

for

the

Cerebral

Cortex

February

V

N

combined

data

PLVs

were

obtained

by

comparing

the

instantaneous

phases

of

the

signals

recorded

by

various

pairs

of

electrodes

for

example

electrodes

j

and

k

at

each

point

in

time

t

across

the

N

epochs

available

-LRB-

Lachaux

et

al.

-RRB-

PLVj

k

t

N

ei

j

t

k

t

N

PLV

is

a

real

value

between

-LRB-

random

phase

difference

no

phase

locking

-RRB-

and

-LRB-

constant

phase

difference

maximum

phase

locking

-RRB-

Because

of

distortions

involved

in

calculating

the

Hilbert

transform

at

the

edges

of

the

analyzed

epochs

-LRB-

e.g.

Freeman

-RRB-

we

do

not

display

the

first

or

the

last

ms

-LRB-

sample

points

-RRB-

of

the

synchrony

analyses

of

our

epochs

-LRB-

note

that

the

last

ms

also

would

be

contaminated

by

the

target

presentation

at

a

random

time

within

that

interval

-RRB-

Thus

we

report

amplitude

and

phase-locking

measures

only

for

reduced

epochs

from

ms

before

until

ms

after

cue

onset

To

remove

the

record

of

ongoing

synchrony

unrelated

to

the

task

we

standardized

PLVs

and

amplitudes

relative

to

the

precue

interval

from

ms

before

cue

onset

until

cue

onset

-LRB-

ms

-RRB-

This

was

done

by

subtracting

the

mean

PLV

for

the

baseline

interval

at

a

given

frequency

from

the

PLV

for

every

data

point

at

that

frequency

and

dividing

the

difference

by

the

SD

of

PLV

for

the

baseline

interval

at

that

frequency

The

resulting

index

PLVz

indicates

standardized

changes

from

the

average

baseline

PLV

at

a

given

frequency

in

the

direction

of

increased

synchronization

-LRB-

positive

values

-RRB-

or

decreased

synchronization

-LRB-

negative

values

-RRB-

The

same

standardization

was

applied

to

the

amplitude

values

To

reduce

the

effects

of

volume

conduction

-LRB-

see

Appendix

for

a

more

detailed

discussion

of

the

problem

of

volume

conduction

in

the

analysis

of

phase

locking

using

these

techniques

-RRB-

and

to

remove

spurious

synchronization

arising

from

using

a

right

mastoid

reference

electrode

the

same

calculations

were

performed

for

the

scalp

current

density

-LRB-

SCD

-RRB-

or

more

properly

the

scalp

divergence

of

the

current

density

a

reference-free

measure

that

sharpens

the

borders

of

synchronous

regions

and

reduces

spurious

synchronies

-LRB-

Lachaux

et

al.

-RRB-

Classically

SCD

scalp

conductivity

Laplacian

of

scalp

potential

where

the

Laplacian

is

the

local

second

spatial

derivative

Perrin

et

al.

-LRB-

-RRB-

showed

that

SCD

in

a

spherical

coordinate

system

could

be

approximated

for

any

point

on

the

scalp

surface

using

a

sphere

head

model

Legendre

polynomials

and

spline

interpolation

To

compute

SCD

we

used

a

MATLAB

script

supplied

by

Carsten

Allefeld

-LRB-

html

-RRB-

that

implements

the

algorithm

of

Perrin

et

al.

-LRB-

-RRB-

-LRB-

see

their

eqs

and

-RRB-

Allefeld

's

script

computes

a

spherical

Laplacian

operator

using

Legendre

polynomials

the

supplied

spherical

coordinates

of

a

set

of

electrodes

and

splines

of

order

In

a

separate

script

we

then

applied

the

Laplacian

operator

to

the

potentials

recorded

at

our

electrodes

to

compute

SCD

This

procedure

has

been

shown

to

be

superior

to

other

methods

used

previously

to

approximate

SCD

from

recorded

potentials

and

to

give

a

close

approximation

to

the

true

SCD

-LRB-

Perrin

et

al.

-RRB-

All

reported

results

pertain

to

the

PLVz

values

based

on

SCD

unless

otherwise

specified

although

analyses

of

scalp

potentials

and

SCDs

gave

highly

similar

results

For

this

reason

and

because

the

SCD

derived

from

the

scalp

potential

at

a

given

electrode

should

reflect

primarily

neural

sources

in

cortical

regions

close

to

that

electrode

-LRB-

see

Appendix

-RRB-

we

often

refer

to

synchrony

changes

between

the

cortical

regions

underlying

the

relevant

electrodes

interchangeably

with

the

recording

electrodes

themselves

In

addition

we

measured

long-range

synchrony

only

for

a

sparse

array

of

electrodes

distributed

uniformly

across

the

scalp

the

distance

between

the

closest

electrode

pairs

was

approximately

cm

At

this

distance

the

effects

of

volume

conduction

on

phase

synchrony

is

much

reduced

both

for

intracranial

electrodes

-LRB-

Lachaux

et

al.

-RRB-

and

for

scalp

electrodes

-LRB-

Nunez

et

al.

see

Appendix

-RRB-

This

array

was

chosen

before

any

analyses

were

conducted

and

was

used

in

previous

studies

as

well

-LRB-

e.g.

Doesburg

et

al.

-RRB-

Finally

to

characterize

the

statistical

reliability

of

changes

in

synchronization

and

desynchronization

in

the

time

courses

of

recorded

potentials

and

inferred

SCD

between

pairs

of

electrodes

relevant

sets

of

epochs

were

shuffled

times

for

each

frequency

and

data

point

combination

measuring

PLVz

in

the

same

way

for

each

shuffled

data

set

to

create

surrogate

distributions

of

PLVz

values

-LRB-

Lachaux

et

al.

-RRB-

Gamma-Band

Phase

Synchronization

and

Selective

Attention

This

procedure

produces

distributions

of

PLVz

that

very

closely

approximate

a

normal

distribution

We

considered

a

measured

PLVz

above

the

th

percentile

of

the

relevant

surrogate

distribution

to

be

a

significant

increase

in

synchronization

and

one

below

the

th

percentile

to

be

a

significant

decrease

in

synchronization

Only

changes

in

synchronization

that

met

or

exceeded

this

criterion

are

discussed

This

still

results

in

a

large

number

of

possible

tests

and

the

surrogate

method

by

itself

does

not

protect

against

the

accumulation

of

experimentwise

Type

I

error

from

making

many

such

tests

To

deal

with

this

problem

we

rely

upon

demonstrations

that

-RRB-

the

changes

we

observed

were

predicted

a

priori

in

the

regions

of

interest

-LRB-

ROIs

-RRB-

in

which

they

were

found

and

-RRB-

the

patterns

of

changes

we

observed

persist

across

several

nearby

frequencies

and

time

points

the

surrogate

distributions

of

which

are

derived

from

independent

shufflings

rendering

it

highly

unlikely

that

the

observed

patterns

resulted

from

a

random

set

of

false

positives

ERP

Analysis

Epochs

for

analysis

of

ERPs

were

extracted

from

ms

before

until

ms

after

target

onset

After

deleting

any

of

these

epochs

contaminated

by

ocular

or

nonocular

artifacts

-LRB-

in

this

case

using

the

automatic

rejection

algorithm

of

ERPSS

from

the

University

of

California

San

Diego

ERPLAB

-RRB-

ERPs

to

targets

were

computed

by

averaging

the

EEG

signal

across

artifact-free

epochs

for

each

subject

For

these

ERP

analyses

the

EEG

records

were

digitally

rereferenced

to

averaged

mastoids

and

after

averaging

digitally

low-pass

filtered

using

a

half-amplitude

Gaussian

filter

to

view

ERPs

Hz

Three

of

the

subjects

were

excluded

from

the

ERP

analysis

because

their

EEG

signals

contained

too

many

artifacts

in

particular

eye

movements

or

blinks

after

the

presentation

of

the

target

resulting

in

a

large

number

of

trials

being

rejected

from

their

data

Thus

the

subject

groups

used

in

the

ERP

analysis

differed

slightly

from

that

used

in

the

synchronization

analysis

Although

the

subgroup

used

for

ERP

analysis

is

the

optimum

one

for

that

analysis

ERPs

were

also

analyzed

using

data

only

from

the

subjects

included

in

the

PLV

analysis

in

order

to

ensure

that

any

observed

ERP

effects

were

also

present

in

that

data

set

Multiway

analyses

of

variance

-LRB-

ANOVAs

-RRB-

were

performed

on

averaged

ERPs

ERPs

at

electrodes

and

the

electrodes

of

interest

in

the

phase

synchronization

analysis

were

analyzed

as

were

electrodes

POz

and

which

are

electrodes

typically

of

interest

when

examining

ERPs

in

visual

attention

tasks

These

particular

electrodes

are

known

to

reflect

attentional

modulation

of

activity

over

parietal

and

occipital

cortices

reflected

by

shifts

of

attention

at

the

electrode

contralateral

to

visual

field

presentation

-LRB-

see

Results

for

a

more

extensive

rationale

-RRB-

Because

our

interest

in

the

ERP

analyses

was

solely

to

confirm

that

attention

had

been

directed

to

the

cued

location

by

the

arrow

cue

and

maintained

there

until

target

onset

our

analyses

focused

on

the

component

the

first

positive

component

within

a

window

of

ms

after

target

onset

and

the

component

or

first

negative

component

within

a

window

of

ms

after

target

onset

Results

Phase

Synchronization

Our

main

a

priori

prediction

was

confirmed

as

increased

gamma-band

-LRB-

Hz

-RRB-

phase

synchronization

was

observed

between

posterior

visual

cortical

areas

contralateral

to

the

cued

location

and

other

widespread

cortical

areas

occurring

from

about

ms

until

about

ms

after

the

cue

appeared

-LRB-

Fig.

-RRB-

The

most

prominent

increases

were

observed

between

electrode

and

electrodes

over

widespread

cortical

areas

and

electrode

and

electrodes

over

widespread

cortical

areas

following

right

and

left

cues

respectively

-LRB-

Fig.

B

-RRB-

Although

present

following

the

onset

of

either

directional

cue

the

effect

is

more

pronounced

and

more

prolonged

following

the

left

cue

We

interpret

this

burst

of

increased

lateralized

phase

synchronization

as

an

indicator

of

the

establishment

of

the

hypothesized

gamma

synchronous

attentional

network

This

effect

was

d

Doesburg

et

al.

Figure

Lateralization

of

large-scale

gamma-band

phase

synchronization

at

Hz

in

source

current

density

-LRB-

SCD

-RRB-

Black

lines

indicate

reliable

increases

in

synchronization

and

white

lines

indicate

reliable

decreases

in

synchronization

colors

represent

interpolated

instantaneous

amplitude

-LRB-

SCD

-RRB-

-LRB-

A

-RRB-

Long-range

synchronization

ms

after

cue

onset

for

all

electrode

pairs

that

include

either

or

-LRB-

B

-RRB-

Time

course

of

synchronization/desynchronization

for

all

electrode

pairs

throughout

the

analyzed

epoch

after

presentation

of

the

left

and

right

cues

respectively

-LRB-

C

-RRB-

Time

course

of

the

second

lateralized

gamma

burst

following

the

left

cue

for

all

pairs

that

include

or

-LRB-

D

-RRB-

Time

course

of

the

second

gamma

burst

following

the

right

cue

for

all

pairs

that

include

or

maximal

around

Hz

-LRB-

because

the

data

were

filtered

using

a

bandwidth

of

f

this

signal

contains

energy

from

nearby

frequencies

-RRB-

but

was

also

visible

at

other

frequencies

in

the

gamma

band

-LRB-

see

Supplementary

Material

A

-RRB-

A

second

burst

of

lateralized

large-scale

gamma-band

phase

synchronization

again

maximal

at

Hz

was

also

observed

approximately

ms

postcue

onset

-LRB-

Fig.

D

-RRB-

As

was

the

case

for

the

first

burst

of

increased

gamma-band

synchronization

this

lateralization

was

anchored

at

electrodes

and

following

the

right

and

left

cues

respectively

and

was

more

pronounced

and

more

prolonged

following

the

left

cue

No

such

bursts

of

long-range

synchronization

lateralized

as

a

function

of

cue

direction

were

present

in

other

frequency

bands

they

occurred

only

in

the

gamma

frequency

band

although

nonlateralized

increases

and

decreases

in

synchronization

did

occur

in

other

frequency

bands

around

the

time

of

the

first

gamma

burst

-LRB-

see

Supplementary

Material

A

-RRB-

No

reliable

patterns

of

coordinated

synchronization

or

desynchronization

in

other

frequency

bands

were

observed

in

conjunction

with

the

second

gamma

burst

Analysis

of

individual

subject

data

revealed

similar

although

less

striking

patterns

of

lateralized

gamma-band

synchronization

-LRB-

because

of

poorer

signal-to-noise

ratio

which

is

a

function

of

the

number

of

epochs

analyzed

-RRB-

For

some

subjects

reliable

effects

closely

resembled

those

in

the

group

data

whereas

for

some

others

the

pattern

took

the

form

of

decreases

in

synchronization

between

visual

cortical

areas

ipsilateral

to

the

cued

hemifield

and

widespread

electrodes

as

well

as

or

in

place

of

the

increases

contralateral

to

the

cued

hemifield

observed

in

the

main

effect

for

our

group

data

-LRB-

Supplementary

Material

B

-RRB-

In

addition

to

the

changes

in

long-range

gamma-band

synchrony

just

described

we

observed

a

reduction

in

the

local

-LRB-

standardized

-RRB-

amplitude

of

the

signal

in

the

alpha

frequency

band

-LRB-

Hz

-RRB-

occurring

from

about

to

ms

after

cue

onset

over

the

left

visual

cortex

and

from

cue

onset

until

about

ms

after

it

over

the

right

visual

cortex

-LRB-

Fig.

-RRB-

This

reduction

of

alpha-band

amplitude

coincided

with

an

increase

in

gamma-band

amplitude

-LRB-

Fig.

-RRB-

and

with

the

lateralized

gamma-band

synchronization

patterns

described

earlier

The

decrement

in

alpha

amplitude

was

surprisingly

larger

at

visual

electrodes

ipsilateral

to

the

cued

location

than

at

contralateral

electrodes

A

subsequent

reversal

was

then

observed

as

greater

alpha-band

amplitude

was

seen

at

electrodes

ipsilateral

to

the

cued

location

relative

to

that

at

contralateral

electrodes

This

latter

effect

endured

from

about

ms

until

about

ms

after

cue

onset

over

the

left

visual

cortex

and

from

about

ms

after

cue

onset

until

beyond

the

end

of

the

displayed

epoch

over

the

right

visual

cortex

-LRB-

Fig.

-RRB-

and

replicates

the

pattern

reported

by

Worden

et

al.

-LRB-

-RRB-

Although

also

visible

in

the

SCD

plotted

data

for

this

result

are

taken

from

the

scalp

potentials

because

they

pertain

only

to

local

EEG

amplitude

-LRB-

comparable

SCD

amplitude

data

can

be

seen

in

Supplementary

Material

A

-RRB-

The

possibility

should

be

considered

whether

the

bursts

of

lateralized

gamma-band

synchrony

we

observed

could

have

arisen

from

a

single

oscillating

source

whose

activity

could

have

been

volume

conducted

to

several

electrodes

for

example

a

strong

local

gamma-band

activation

located

in

visual

cortex

contralateral

to

the

cued

location

Such

a

scenario

however

would

entail

a

much

greater

gamma

amplitude

increase

over

contralateral

visual

cortex

than

over

ipsilateral

visual

cortex

This

was

not

observed

in

fact

gamma

amplitude

increased

more

over

ipsilateral

visual

cortex

than

over

contralateral

visual

cortex

-LRB-

see

Figs

and

and

Appendix

-RRB-

For

these

reasons

we

can

confidently

reject

the

notion

that

our

lateralized

longrange

phase

synchrony

results

arose

from

this

kind

of

volume

conduction

scenario

Other

possibilities

are

discussed

in

the

Appendix

An

increase

in

beta-band

phase

synchronization

also

was

observed

from

about

ms

until

about

ms

after

the

cue

onset

-LRB-

see

Supplementary

Material

A

-RRB-

This

increased

synchronization

was

strongly

anchored

at

the

right

occipitoparietal

and

left

frontal

electrodes

with

strong

connectivity

linking

these

regions

and

increased

phase

synchrony

between

these

Cerebral

Cortex

February

V

N

Figure

Standardized

amplitude

from

filtered

-LRB-

alpha

Hz

and

gamma

Hz

-RRB-

electrode

-LRB-

and

-RRB-

potentials

-LRB-

vertical

axes

-RRB-

as

a

function

of

time

after

cue

onset

-LRB-

at

ms

-RRB-

for

the

various

cue

conditions

electrodes

and

other

cortical

areas

Corresponding

local

amplitude

changes

were

also

evident

with

prominent

increases

in

left

frontal

right

occipitoparietal

electrodes

and

those

over

the

right

frontal

areas

The

topology

of

this

beta

oscillatory

network

emerged

following

both

the

left

and

the

right

cue

but

did

not

appear

to

be

affected

by

the

direction

of

attentional

deployment

Event-Related

Potentials

The

current

paradigm

was

chosen

due

to

its

success

in

a

previous

study

in

illuminating

changes

in

local

EEG

power

during

selective

visual

attention

-LRB-

Worden

et

al.

-RRB-

In

that

study

electrophysiological

measures

were

used

to

confirm

that

attention

had

been

effectively

deployed

as

no

behavioral

measures

are

available

in

this

paradigm

and

it

is

important

to

any

arguments

about

the

mechanism

of

attention

deployment

to

confirm

that

attention

was

indeed

deployed

as

specified

to

subjects

Worden

et

al.

-LRB-

-RRB-

did

confirm

appropriate

attention

deployment

in

their

study

although

they

based

their

conclusion

only

on

attentional

modulation

of

the

amplitude

They

failed

to

find

modulations

although

some

other

studies

with

similar

endogenous

orienting

paradigms

have

found

modulations

of

both

components

-LRB-

e.g.

Mangun

and

Hillyard

Sauseng

et

al.

-RRB-

We

also

confirmed

that

attention

indeed

was

shifted

to

the

cued

location

by

analyzing

ERPs

to

the

targets

Figure

presents

Gamma-Band

Phase

Synchronization

and

Selective

Attention

d

Figure

ERP

waveforms

to

targets

at

electrodes

POz

and

Waveforms

to

targets

presented

in

the

right

visual

field

are

at

the

top

of

the

figure

waveforms

to

targets

presented

in

the

left

visual

field

are

presented

at

the

bottom

of

the

figure

Note

that

amplitude

to

validly

cued

targets

is

largest

contralateral

to

target

presentation

the

results

of

our

analyses

-LRB-

see

also

Supplementary

Material

C

-RRB-

For

trials

where

the

stimulus

presented

was

a

target

we

performed

sets

of

ANOVAs

on

the

and

amplitudes

separately

Electrode

-LRB-

-RRB-

Stimulus

side

-LRB-

Left

Right

-RRB-

Validity

-LRB-

Valid

Invalid

-RRB-

and

Electrode

-LRB-

POz

-RRB-

Stimulus

side

-LRB-

Left

Right

-RRB-

Validity

-LRB-

Valid

Invalid

-RRB-

Analysis

of

the

component

revealed

a

significant

attention

modulation

replicating

the

results

of

Worden

et

al.

-LRB-

-RRB-

At

electrodes

and

a

significant

main

effect

of

validity

was

found

-LRB-

P

-RRB-

showing

that

amplitude

was

larger

on

trials

where

the

stimulus

appeared

in

a

validly

cued

location

The

interaction

of

Electrode

Side

was

also

significant

-LRB-

P

-RRB-

revealing

that

amplitude

was

greatest

when

the

stimulus

was

presented

contralateral

to

the

recording

electrode

The

interaction

between

Electrode

Side

and

Validity

was

also

significant

-LRB-

P

-RRB-

indicating

that

the

effect

of

attention

on

the

was

larger

on

the

side

contralateral

to

the

cued

location

Doesburg

et

al.

Analysis

of

amplitude

at

electrodes

POz

and

showed

the

same

pattern

with

a

significant

main

effect

of

Validity

-LRB-

P

-RRB-

Also

as

for

electrodes

and

an

interaction

between

Electrode

and

Side

was

found

-LRB-

P

-RRB-

with

larger

amplitude

to

targets

presented

contralateral

to

electrodes

and

and

larger

amplitude

at

electrode

POz

to

targets

presented

to

the

left

of

fixation

Finally

there

was

also

a

significant

interaction

between

Electrode

Side

and

Validity

-LRB-

P

-RRB-

Analysis

of

ERPs

using

only

data

from

the

subjects

included

in

the

synchrony

analysis

showed

the

same

patterns

of

results

confirming

that

results

from

the

main

ERP

analysis

generalize

to

the

subject

group

for

whom

the

synchrony

results

are

presented

-LRB-

see

Supplementary

Material

C

-RRB-

The

same

analyses

showed

no

attentional

modulation

of

amplitudes

again

as

found

by

Worden

et

al.

-LRB-

-RRB-

For

electrodes

and

there

was

no

main

effect

of

nor

significant

interactions

involving

Validity

There

was

an

interaction

between

Side

and

Electrode

with

larger

amplitude

for

targets

presented

contralateral

to

the

electrode

-LRB-

P

-RRB-

For

electrodes

POz

and

as

for

and

the

analysis

revealed

no

main

effect

nor

any

interactions

involving

Validity

There

was

however

an

interaction

between

Side

and

Electrode

-LRB-

P

-RRB-

with

larger

amplitude

contralateral

to

target

presentation

for

electrodes

and

and

larger

amplitude

to

targets

to

the

left

of

fixation

at

electrode

POz

Although

they

reveal

nothing

new

about

attention

orienting

in

this

paradigm

these

ERP

results

do

provide

convincing

evidence

that

attention

was

indeed

directed

to

the

cued

location

by

the

arrow

cue

and

maintained

there

until

target

onset

First

as

mentioned

earlier

previous

experiments

with

similar

endogenous

attention-orienting

paradigms

have

found

that

the

ERP

component

is

larger

when

targets

are

presented

in

an

attended

-LRB-

cued

-RRB-

location

than

when

presented

in

an

unattended

location

and

in

particular

that

the

ERP

modulation

is

closely

tied

to

faster

responding

to

the

target

at

the

cued

location

a

more

traditional

behavioral

measure

of

attention

orienting

-LRB-

e.g.

Mangun

and

Hillyard

-RRB-

Our

finding

of

a

significantly

larger

component

to

targets

presented

at

the

cued

location

is

a

strong

indicator

that

subjects

were

reliably

shifting

their

attention

to

that

location

when

directed

to

do

so

by

the

arrow

cue

The

fact

that

we

and

Worden

et

al.

-LRB-

-RRB-

found

no

significant

cue

effect

on

the

component

in

this

paradigm

does

not

contradict

this

interpretation

Modulations

of

and

components

are

known

to

be

dissociable

from

one

another

depending

upon

the

task

-LRB-

e.g.

Luck

et

al.

-RRB-

In

endogenous

cueing

tasks

involving

stimulus

discrimination

like

the

one

used

in

this

experiment

Luck

et

al.

-LRB-

-RRB-

found

that

whereas

the

was

significantly

larger

on

validly

cued

trials

this

effect

was

not

found

for

the

component

Further

Vogel

and

Luck

-LRB-

-RRB-

found

evidence

that

the

component

is

a

reflection

of

the

discrimination

of

visual

stimuli

as

our

task

was

a

visual

discrimination

task

it

is

reasonable

to

understand

the

modulation

of

the

component

to

be

a

reliable

indicator

of

the

subjects

successful

shift

of

attention

to

the

cued

location

Discussion

Cue-directed

deployment

of

attention

to

one

side

of

the

visual

field

confirmed

by

the

modulation

of

the

component

of

the

ERP

to

the

subsequent

target

coincides

with

an

increase

in

gamma-band

phase

synchronization

between

the

contralateral

visual

cortex

and

other

widespread

cortical

areas

Our

results

support

the

view

that

gamma-band

synchronization

is

the

mechanism

that

implements

-RRB-

the

selective

properties

of

attention

-LRB-

certain

neuronal

groups

are

biased

for

inclusion

into

the

network

and

others

are

not

-RRB-

-RRB-

its

integrative

properties

-LRB-

when

neurons

corresponding

to

attended

objects

features

are

included

in

a

long-range

network

they

are

more

integrated

with

other

perceptual

and

cognitive

representations

-RRB-

and

-RRB-

the

special

relationship

between

attention

and

conscious

executive

processes

-LRB-

inclusion

in

the

network

is

equivalent

to

inclusion

in

a

global

conscious

workspace

allowing

cognitive

and

behavioral

operations

on

this

information

that

are

informed

by

other

considerations

such

as

goal

and

context

e.g.

Dehaene

and

Naccache

-RRB-

Synchronously

oscillating

neurons

can

perform

such

integration

because

they

communicate

more

effectively

than

do

nonsynchronous

neurons

Bursts

of

action

potentials

from

a

sending

neuron

must

be

consistently

received

during

the

depolarized

phase

of

a

target

neuron

's

membrane

potential

fluctuation

in

order

for

those

action

potentials

to

be

efficacious

and

this

happens

when

the

sending

and

receiving

neurons

are

phase

locked

-LRB-

Fries

-RRB-

What

is

still

mysterious

is

how

and

why

synchronization

in

the

various

frequency

bands

plays

the

role

it

does

Our

results

on

the

relationship

between

local

and

long-range

synchronization

in

alpha

beta

and

gamma

bands

begin

to

address

this

question

Gamma-Band

Phase

Synchronization

The

selection

and

integration

of

information

into

a

large-scale

complex

that

extends

across

brain

areas

has

been

posited

to

be

consciousness

-LRB-

Tononi

-RRB-

We

propose

that

the

selection

of

certain

neuronal

groups

for

integration

into

a

large-scale

gamma

synchronous

network

accounts

for

how

selective

attention

enables

the

increased

integration

of

attended

information

relative

to

unattended

information

within

and

across

sensory

modalities

and

biases

attended

information

for

higher

processing

and

entry

into

consciousness

-LRB-

cf.

Lamme

Koch

and

Tsuchiya

-RRB-

In

this

view

the

emergence

of

a

dynamic

executive

consciousness

within

the

brain

may

result

from

a

large-scale

gamma-synchronous

network

of

task-relevant

neural

populations

This

implements

functional

integration

and

serves

to

activate

a

specific

network

from

a

large

repertoire

of

possible

networks

The

representational

contents

of

neural

groups

included

in

this

coherently

oscillating

network

define

the

content

of

consciousness

and

are

dynamically

assigned

according

to

task

demands

perceptual

input

and

motor

output

-LRB-

Varela

et

al.

-RRB-

Local

brain

recordings

have

demonstrated

that

synchronously

gamma

oscillatory

cortical

columns

code

figure-ground

segregation

and

the

binding

of

features

for

the

encoding

of

global

stimulus

properties

leading

to

the

proposal

that

gamma-band

synchrony

underlies

sensory

awareness

-LRB-

Gray

et

al.

Engel

Konig

and

Singer

Engel

and

Singer

-RRB-

Long-range

complexes

of

gamma

synchronous

brain

regions

correspond

to

the

emergence

of

a

coherent

conscious

percept

and

the

binding

of

local

features

into

a

global

visual

percept

-LRB-

Rodriguez

et

al.

Doesburg

et

al.

Rose

et

al.

-RRB-

Such

results

show

frequency

specificity

similar

to

the

results

reported

here

suggesting

a

common

neural

mechanism

of

large-scale

integration

Conscious

recollection

moreover

is

associated

with

greater

gamma-band

EEG

connectivity

than

is

familiarity

-LRB-

Burgess

and

Ali

-RRB-

Gamma

oscillations

are

generally

restricted

to

brain

states

associated

with

consciousness

-LRB-

waking

and

rapid

eye

movement

Cerebral

Cortex

February

V

N

sleep

-RRB-

and

are

more

spatially

segregated

than

low-frequency

oscillations

present

during

nonconscious

central

nervous

system

states

thereby

allowing

the

increased

specificity

of

information

selection

required

for

consciousness

-LRB-

Nunez

-RRB-

A

variety

of

previous

findings

support

the

notion

that

gammaband

synchrony

is

relevant

for

attention

and

that

it

is

a

mechanism

for

functional

integration

across

brain

areas

These

include

lateralization

of

induced

gamma-band

responses

to

somatosensory

stimulation

and

visual

stimuli

can

be

modulated

by

selective

attention

-LRB-

Gruber

et

al.

Gobbele

et

al.

-RRB-

the

auditory

transient

response

is

larger

for

attended

stimuli

than

it

is

for

those

that

are

ignored

-LRB-

Tiitinen

et

al.

-RRB-

intracranial

recordings

of

area

in

monkeys

show

greater

gamma-band

synchronization

between

neurons

activated

by

an

attended

stimulus

relative

to

those

activated

by

an

unattended

stimulus

-LRB-

Fries

et

al.

-RRB-

intracranial

EEG

recordings

in

humans

have

shown

that

successful

memory

formation

is

associated

with

greater

gamma-band

synchronization

between

the

rhinal

cortex

and

the

hippocampus

-LRB-

Fell

et

al.

-RRB-

increased

EEG

gamma-band

coherence

between

somatosensory

and

primary

visual

areas

occurs

when

subjects

learn

an

association

between

a

finger

shock

and

a

visual

stimulus

-LRB-

Miltner

et

al.

-RRB-

gamma-band

phase

synchronization

across

posterior

electrodes

is

greater

when

a

stimulus

is

identified

in

a

fragmented

pattern

relative

to

when

a

stimulus

is

not

identified

-LRB-

Gruber

et

al.

-RRB-

EEG

phase

synchronization

between

posterior

and

frontal

cortical

regions

is

increased

during

mental

rotation

-LRB-

Bhattacharya

et

al.

-RRB-

gamma-band

activity

is

increased

at

frontal

and

occipitotemporal

electrodes

during

the

delay

phase

of

a

short-term

memory

task

-LRB-

TallonBaudry

et

al.

-RRB-

and

perceptual

grouping

is

associated

with

increased

gamma-band

oscillations

in

the

high

gamma

band

-LRB-

Hz

-RRB-

at

central

occipital

locations

whereas

the

requirement

to

focus

attention

on

the

perceptual

groups

activates

additional

low

gamma-band

-LRB-

Hz

-RRB-

oscillations

in

parietal

locations

-LRB-

Vidal

et

al.

-RRB-

The

prominence

of

increased

long-range

gamma-band

synchronization

at

right

parietal

electrodes

in

our

data

strengthens

the

attentional

interpretation

of

the

effect

as

the

right

parietal

lobe

is

particularly

relevant

for

visual

attention

-LRB-

Egly

et

al.

-RRB-

and

this

area

shows

increased

gamma

activity

when

attentional

focusing

is

required

-LRB-

Vidal

et

al.

-RRB-

This

introduces

a

theoretical

bridge

between

gamma-band

phase

synchronization

and

current

knowledge

about

the

functional

neuroanatomy

of

attention

Moreover

coordinated

changes

in

gamma

and

alpha

synchronization

are

maximal

ms

after

the

onset

of

the

cue

at

the

time

where

previous

work

has

shown

that

behavioral

enhancement

as

a

function

of

attention

reaches

its

zenith

-LRB-

Wright

and

Ward

-RRB-

Prior

to

the

increase

in

gamma-band

phase

synchronization

a

period

of

desynchronization

is

also

observed

in

our

data

beginning

when

the

cue

is

presented

and

lasting

until

about

ms

after

cue

onset

-LRB-

Fig.

see

Supplemental

Material

A

for

detailed

time

course

-RRB-

This

may

reflect

phase

scattering

a

process

thought

to

disrupt

existing

gamma

synchronous

neural

assemblies

in

order

to

enable

the

emergence

of

new

transient

assemblies

Similar

patterns

have

been

found

preceding

transient

bursts

of

increased

gammaband

synchronization

in

coherent

perception

-LRB-

Rodriguez

et

al.

Doesburg

et

al.

-RRB-

Moreover

stimulus

processing

can

produce

either

local

synchronization

or

desynchronization

in

the

gamma

band

depending

on

task

relevance

-LRB-

Mazeheri

and

Picton

-RRB-

Our

analysis

of

individual

subjects

data

revealed

Gamma-Band

Phase

Synchronization

and

Selective

Attention

Doesburg

et

al.

some

instances

of

global

gamma-band

desynchronization

between

visual

cortex

ipsilateral

to

the

cued

hemifield

and

widespread

electrodes

-LRB-

Supplementary

Material

B

-RRB-

We

interpret

this

as

a

functional

decoupling

between

cortical

regions

representing

the

to-be-ignored

location

thus

indicating

a

suppression

of

unattended

information

Our

results

indicate

that

bursts

of

lateralized

gamma-band

phase

synchronization

are

transient

occurring

about

ms

after

cue

Although

this

is

within

the

predicted

time

frame

for

the

initiation

of

endogenous

orienting

-LRB-

e.g.

Wright

and

Ward

-RRB-

our

subjects

were

required

to

maintain

their

attention

at

the

cued

location

far

beyond

the

termination

of

this

gamma

burst

This

suggests

that

the

observed

synchronization

is

related

to

the

deployment

of

attention

to

a

location

but

is

not

required

for

the

maintenance

of

attention

at

that

location

Bursts

of

gamma-band

phase

synchronization

related

to

the

onset

of

a

coherent

percept

have

also

been

found

to

be

short

lived

relative

to

the

duration

of

the

percept

itself

-LRB-

Rodriguez

et

al.

Doesburg

et

al.

-RRB-

Large-scale

gamma-band

synchronization

must

therefore

be

regarded

as

a

mechanism

for

integrating

a

functional

network

rather

than

one

that

is

responsible

for

maintaining

that

integration

Our

analysis

revealed

a

second

burst

of

lateralized

long-range

gamma

synchrony

at

ms

after

cue

onset

This

finding

echoes

earlier

findings

from

coherent

perception

where

a

second

burst

of

long-distance

gamma-phase

synchrony

has

also

been

recorded

-LRB-

Rodriguez

et

al.

Doesburg

et

al.

-RRB-

The

temporal

relationship

between

the

first

and

second

burst

of

gamma

synchrony

in

this

as

well

as

in

previous

studies

is

consistent

with

a

theta

frequency

-LRB-

Hz

-RRB-

cycle

Phase

coupling

between

theta

and

gamma

activity

has

been

observed

across

brain

regions

during

cognitive

processing

in

studies

employing

scalp

or

intracranial

EEG

and

has

been

interpreted

as

a

mechanism

mediating

neural

communication

across

long

distances

-LRB-

Schack

et

al.

Canolty

et

al.

-RRB-

In

light

of

this

it

seems

likely

that

the

second

burst

of

lateralized

longrange

gamma

synchrony

reported

here

may

be

related

to

the

maintenance

or

refinement

of

the

attentional

network

established

by

the

first

burst

Alpha-Band

Amplitude

Reduction

Previously

it

has

been

shown

that

shifts

of

visuospatial

attention

to

locations

in

one

hemifield

yield

a

sustained

increase

in

alpha

activation

over

ipsilateral

visual

cortical

areas

beginning

around

ms

after

cue

onset

-LRB-

Worden

et

al.

Thut

et

al.

-RRB-

Our

study

replicated

this

result

We

also

replicated

an

earlier

reduction

of

alpha

activity

over

both

contralateral

and

ipsilateral

visual

areas

reported

by

Worden

et

al.

-LRB-

-RRB-

Our

results

however

also

indicated

that

this

early

reduction

was

much

more

pronounced

over

visual

cortex

ipsilateral

to

the

attended

location

One

possible

explanation

for

this

discrepancy

between

our

results

and

those

of

Worden

et

al.

-LRB-

-RRB-

is

the

several

differences

in

the

analysis

techniques

used

Here

we

report

local

activity

changes

in

instantaneous

amplitude

that

are

standardized

relative

to

the

mean

of

a

precue

baseline

whereas

studies

using

temporal

spectral

evolution

which

report

lateralization

only

for

the

later-occurring

alpha-band

evolution

plotted

the

nonstandardized

amplitude

of

the

filtered

rectified

and

smoothed

signal

as

a

function

of

time

-LRB-

Worden

et

al.

Thut

et

al.

-RRB-

A

striking

temporal

correspondence

is

evident

between

the

early

bilateral

but

unequal

decrease

of

local

alpha

amplitude

d

the

similar

bilateral

but

unequal

increase

of

local

gamma

amplitude

and

the

first

burst

of

lateralized

long-distance

gammaband

phase

synchronization

all

these

effects

were

maximal

ms

after

cue

onset

This

suggests

that

the

activities

of

oscillatory

mechanisms

in

multiple

frequency

bands

interact

across

local

and

long-distance

scales

to

enable

selective

visuospatial

attention

Specifically

we

propose

that

local

alpha-band

activity

reflects

suppression

of

a

cortical

area

local

gamma-band

activity

reflects

active

processing

in

a

cortical

area

and

longrange

gamma

synchronization

serves

to

establish

a

transient

network

promoting

the

transfer

of

information

appearing

at

attended

locations

from

the

relevant

modality-specific

cortical

areas

-LRB-

in

this

case

contralateral

occipital

and

posterior

temporal

cortices

-RRB-

to

other

cortical

regions

-LRB-

cf.

Ward

-RRB-

The

lateralization

effects

in

local

amplitude

discussed

earlier

however

suggest

that

the

relationship

between

neural

oscillations

and

attentional

processing

is

more

complex

given

that

gammaband

amplitude

is

slightly

lower

in

the

hemisphere

contralateral

to

the

attended

location

during

this

period

A

possible

explanation

for

this

is

that

when

cortical

tissue

is

engaged

in

a

longrange

gamma-band

synchronous

assembly

increased

columnar

selection

and

segregation

occur

locally

leading

to

relatively

lower

gamma-band

and

relatively

higher

alpha-band

amplitude

as

a

comparatively

restricted

set

of

columns

are

engaged

in

active

processing

In

support

of

this

notion

it

has

been

found

that

cortical

stimulation

at

Hz

produces

increasingly

focal

responses

-LRB-

intercolumnar

inhibition

-RRB-

whereas

Hz

stimulation

propagates

to

other

cortical

areas

-LRB-

Llinas

et

al.

-RRB-

If

long-distance

synchronization

between

neural

groups

underlies

transient

functional

integration

as

we

and

others

have

proposed

then

increased

long-distance

synchronization

should

be

exhibited

throughout

the

period

during

which

the

neural

populations

in

question

are

coupled

In

the

case

of

selective

attention

this

entails

synchrony

between

cortical

areas

representing

attended

information

and

other

brain

regions

throughout

the

period

of

attention

maintenance

In

support

of

this

notion

studies

have

found

evidence

for

long-duration

long-range

coupling

of

attention-related

brain

regions

in

an

attention-orienting

paradigm

First

in

a

cued

target-discrimination

paradigm

increased

high

alpha-band

phase

coupling

in

the

EEG

between

frontomedial

electrodes

and

parietal

electrodes

contralateral

to

the

attended

hemifield

was

found

to

occur

during

the

ms

just

preceding

target

onset

-LRB-

Sauseng

et

al.

-RRB-

Second

our

own

magnetoencephalographic

results

using

a

paradigm

identical

to

the

experiment

reported

here

showed

increased

long-distance

high

alpha-band

phase

synchronization

between

sensors

over

occipital

cortex

contralateral

to

the

cued

location

and

sensors

over

other

widespread

cortical

regions

beginning

ms

after

cue

onset

and

lasting

throughout

the

period

of

attentional

maintenance

-LRB-

Doesburg

and

Ward

forthcoming

-RRB-

Moreover

we

also

observed

an

initial

bilateral

longrange

desynchronization

in

the

alpha-band

peaking

around

ms

after

cue

onset

The

tight

correspondence

of

these

effects

with

the

amplitude

changes

in

the

alpha

band

described

here

suggests

that

an

alpha

oscillatory

mechanism

involving

local

desynchronization

and

long-range

synchronization

is

responsible

for

the

maintenance

of

selective

attention

successfully

report

perceiving

the

second

of

successive

targets

in

a

rapid-serial-visual-presentation

stream

compared

with

trials

on

which

perception

of

the

second

target

was

not

reported

synchronization

of

a

beta-band

oscillatory

network

was

observed

between

the

right

cingulum

right

posterior

parietal

lobe

and

left

frontal

areas

shortly

after

the

second

target

was

presented

-LRB-

Gross

et

al.

-RRB-

A

long-range

beta

oscillatory

network

bearing

a

similar

topography

and

time

course

was

also

present

in

our

data

-LRB-

see

Supplementary

Material

A

-RRB-

This

effect

was

maximal

at

about

Hz

did

not

vary

according

to

the

direction

of

attentional

deployment

and

reached

its

maximum

during

the

peak

of

the

lateralized

gamma-band

synchronization

This

suggests

that

this

beta

synchronous

network

is

of

general

relevance

for

attentional

deployment

and

that

this

mechanism

operates

in

tandem

with

gamma-band

oscillations

The

pattern

of

interactions

between

the

gamma-band

and

beta-band

networks

is

still

to

be

explored

On

the

basis

of

these

results

however

we

postulate

that

the

beta-band

network

is

a

general

mechanism

that

implements

attentional

preparation

or

readiness

whereas

the

gamma-band

network

selects

task-relevant

neural

populations

and

integrates

them

into

a

transient

functional

network

Supplementary

Material

Supplementary

materials

can

be

found

at

oxfordjournals.org

Notes

This

research

was

supported

by

a

Discovery

Grant

from

the

Natural

Sciences

and

Engineering

Research

Council

of

Canada

to

L.M.W.

We

thank

Stephanie

Thai

Vivian

Pan

and

Lauren

Emberson

for

help

in

collecting

the

data

We

thank

Carsten

Allefeld

for

supplying

the

MATLAB

algorithm

for

the

SCD

analysis

We

also

thank

Dr

Kentaro

Yamanaka

Graduate

School

of

Education

University

of

Tokyo

for

help

in

developing

the

phase

synchrony

analysis

program

Conflict

of

Interest

declared

Address

correspondence

to

Sam

M.

Doesburg

Department

of

Psychology

University

of

British

Columbia

West

Mall

Vancouver

BC

Email

sam@psych.ubc.ca

Appendix

In

the

context

of

EEG

and

MEG

recordings

of

brain

activity

volume

conduction

refers

to

the

propensity

for

electric

or

magnetic

fields

to

be

transmitted

from

an

electrical

source

through

the

tissues

of

the

brain

skull

and

scalp

to

sensors

distributed

over

a

wide

area

on

or

near

the

scalp

The

problem

has

been

considered

extensively

in

the

context

of

source

analysis

in

EEG

and

MEG

Here

the

well-characterized

inverse

problem

is

to

reconstruct

the

primary

current

distribution

within

the

brain

from

the

electric

or

magnetic

fields

measured

on

or

near

the

scalp

Extensive

modeling

and

sophisticated

algorithms

have

made

this

problem

less

of

an

issue

in

recent

times

In

the

context

of

the

analysis

of

neural

phase

synchrony

however

much

less

work

has

been

done

and

the

possibility

of

volume

conduction

creating

spurious

synchronies

remains

a

serious

consideration

The

most

extensive

research

relevant

to

this

problem

was

done

by

Lachaux

et

al.

-LRB-

-RRB-

They

defined

and

investigated

in

the

context

of

intracranial

EEG

recordings

the

measure

of

PLV

used

here

They

also

specifically

addressed

the

possibility

of

spurious

synchrony

indicated

by

this

measure

arising

from

volume

conduction

and

concluded

that

long-range

synchronies

were

unlikely

to

arise

because

of

this

effect

This

conclusion

was

based

on

both

direct

measurements

of

PLV

at

intracranial

electrodes

spaced

at

cm

intervals

over

which

Beta-Band

Attention

Network

Previous

magnetoencephalographic

results

from

an

attention

blink

paradigm

have

shown

that

when

subjects

were

able

to

Cerebral

Cortex

February

V

N

volume-conduction

induced

spurious

synchrony

did

not

extend

further

than

cm

in

normal

tissue

and

on

simulations

using

local

field

potential

recordings

from

a

subject

as

dipole

sources

and

forward

calculating

the

resulting

scalp

potential

using

a

spherical

head

model

In

the

simulation

they

calculated

PLV

for

scalp

potential

SCD

-LRB-

the

local

second

spatial

derivative

of

the

scalp

potential

-RRB-

and

electrocorticogram

-LRB-

ECoG

obtained

from

a

deblurring

technique

introduced

by

Le

and

Gevins

-RRB-

for

scalp

electrodes

at

various

positions

relative

to

the

radial

dipole

sources

which

were

located

in

separate

hemispheres

around

the

midline

Both

the

SCD

and

the

deblurred

ECoG

sharpened

synchronous

regions

in

the

simulations

and

reduced

spurious

synchronies

relative

to

those

calculated

for

the

scalp

potential

They

had

this

effect

because

both

reduce

the

overlap

of

the

volumes

recorded

by

different

scalp

electrodes

in

particular

eliminating

the

contributions

of

deep

sources

and

shrinking

the

surface

areas

of

the

scalp

affected

by

shallow

sources

In

addition

another

study

by

Nunez

et

al.

-LRB-

-RRB-

also

found

that

SCD

or

ECoG

reduced

the

effects

of

volume

conduction

on

coherence

between

scalp

electrodes

at

various

distances

-LRB-

which

includes

but

is

not

the

same

as

phase

synchrony

because

coherence

is

also

influenced

by

amplitude

correlation

-RRB-

with

spurious

coherence

dropping

to

near

zero

when

scalp

electrodes

were

separated

by

cm

or

more

The

studies

of

Lachaux

et

al.

-LRB-

-RRB-

were

based

on

instantaneous

phase

and

instantaneous

amplitude

obtained

from

convolving

a

Morlet

wavelet

of

appropriate

frequency

interval

with

the

EEG

signals

An

alternative

approach

and

the

one

we

use

here

is

to

obtain

these

quantities

from

the

analytic

signal

based

on

the

Hilbert

transform

for

the

filtered

EEG

signals

-LRB-

Tass

et

al.

-RRB-

Le

Van

Quyen

et

al.

-LRB-

-RRB-

directly

compared

the

methods

for

analysis

of

neural

synchrony

for

data

from

neuronal

models

intracranial

EEG

and

scalp

EEG

and

found

that

they

were

essentially

equivalent

We

have

also

analyzed

some

of

our

other

data

using

both

methods

but

we

found

the

areas

of

synchrony

to

be

more

sharply

delineated

with

the

Hilbert

transform

based

technique

so

we

used

that

technique

here

To

set

the

problem

of

volume

conduction

effects

on

neural

synchrony

measured

by

sensors

more

sharply

consider

the

simple

case

simulated

by

Lachaux

et

al.

-LRB-

-RRB-

We

have

radial

dipoles

oscillating

at

some

frequency

call

them

and

located

at

some

distance

from

one

another

recorded

by

electrodes

each

near

to

one

of

the

sources

The

dipoles

generate

signals

exp

i

xt

exp

i

xt

pffiffiffiffiffi

and

are

the

amplitudes

of

the

signals

and

are

where

i

the

respective

phase

angles

and

x

is

the

common

frequency

-LRB-

for

clarity

we

are

assuming

noiseless

signals

with

constant

phase

offset

however

the

results

apply

to

the

averages

of

noisy

signals

-RRB-

The

signals

actually

recorded

by

the

electrodes

are

affected

by

the

conductivity

of

the

brain

skull

and

scalp

-LRB-

here

assumed

to

be

one

constant

average

value

c

-RRB-

and

the

distance

of

electrode

j

from

source

k

-LRB-

djk

-RRB-

so

that

the

recordings

can

be

written

as

c

c

c

c

and

arctan

arctan

These

expressions

-LRB-

-RRB-

readily

generalize

to

any

number

of

sources

When

we

add

these

electrode

recordings

to

i

times

their

Hilbert

transforms

to

obtain

the

analytic

signal

-LRB-

see

Methods

-RRB-

we

obtain

exp

exp

where

and

Recall

that

PLVj

k

t

N

ei

j

t

k

t

N

so

that

given

the

above

development

-LRB-

i.e.

especially

eq

-RRB-

and

j

t

and

k

t

for

any

specific

time

t

t

f

This

means

that

raw

PLV

depends

on

the

relative

amplitudes

of

the

sources

as

well

as

the

constancy

of

their

relative

phases

across

trials

For

this

reason

we

use

the

standardized

PLVz

to

eliminate

the

volume

conduction

effects

of

sources

whose

amplitudes

do

not

change

from

those

in

the

baseline

period

-LRB-

see

Methods

-RRB-

For

PLVz

to

be

different

from

zero

one

-LRB-

or

possibly

both

-RRB-

of

things

must

happen

-RRB-

must

become

more

-LRB-

or

less

-RRB-

constant

across

trials

making

also

more

-LRB-

or

less

-RRB-

constant

across

trials

-LRB-

true

synchronization

or

desynchronization

-RRB-

or

-RRB-

the

amplitude

of

one

source

must

increase

-LRB-

or

decrease

-RRB-

reliably

across

trials

and

by

enough

that

both

and

now

contain

significantly

more

-LRB-

or

less

-RRB-

contribution

from

that

particular

source

thus

making

more

-LRB-

or

less

-RRB-

constant

across

trials

-LRB-

spurious

synchrony

caused

by

volume

conduction

-RRB-

The

latter

could

happen

either

because

a

source

that

is

already

active

becomes

more

-LRB-

or

less

-RRB-

active

reliably

across

trials

or

because

a

source

that

is

inactive

during

the

baseline

is

reliably

activated

by

the

task

during

part

of

the

analyzed

epoch

This

means

that

spurious

volume-conducted

synchrony

does

not

appear

in

the

absence

of

changes

in

local

amplitude

For

this

reason

we

emphasize

inspection

of

both

PLVz

and

local

amplitude

in

our

interpretation

of

synchrony

changes

In

particular

the

lateralized

changes

we

found

in

Hz

PLVz

anchored

at

and

occurring

at

approximately

ms

after

cue

onset

were

not

accompanied

by

corresponding

changes

in

local

amplitude

so

we

can

be

confident

that

these

changes

are

not

spurious

-LRB-

Figs

and

-RRB-

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