collaborators: sang-hun lee, seoul national university ...sang-hun lee, seoul national university...

Traveling Waves of Activity in Visual

Cortex During Binocular Rivalry

Collaborators:

Sang-Hun Lee, Seoul National University

Randolph Blake, Vanderbilt University

Perceptleft eye right eye

t

dominancein percept

Spatiotemporal dynamics during

binocular rivalry

Right eye

Left eye Ocular dominancecolumns

L

Binocularneurons

V1

R

R

L

V1 suppression hypothesis

• Early versus late.

• Eye versus pattern.

• Transitions vs sustained periods of

dominance.

• Role of attention.

• Local processing vs feedback from higher

visual areas.

Unresolved issues

Pattern rivalry

Left eye Right eye

Kovacs et al, PNAS (1996)

Binocular rivalry in monkey IT

Sheinberg & Logothetis, PNAS (1997)

Binocular rivalry in human IT

Tong et al, Neuron (1998)

Display

left eye right eye

Percept

Wilson, Blake & Lee (2001)

Latency

L / R / N

Perceptual traveling waves

Percept

Brain

Predicted and measured responses

Meas

ured f

MR

I r

esp

onse

(% c

han

ge im

age int

ens

ity)

Time (sec)0 3 6 9

1

2

0

Lee, Blake, & Heeger, Nature Neurosci (2005)

Predic

ted

neur

al a

ctiv

ity

Time

PerceptPeak fMRI response

Perceptual and neural traveling waves

Lee, Blake, & Heeger, Nature Neurosci (2005)

Latency (s)

# o

f tr

ials

1 3

Behavior

fMR

I r

esp

onse

lat

enc

y

(sec)

0 1 2 34.5

5.0

5.5

6.0

Distance (cm)

Behavioral latency

1-1.5 sec

1.5-2 sec

2-3 sec

6.5

Infer ~115 ms timing

difference over ~3.5 mm

distance.

Activity correlates with perceived latency

Lee, Blake, & Heeger, Nature Neurosci (2005)

t

FMRIresponse

time to peakpeak amplitude

Localcontrast

Neuralactivity

Estimating neural activity

Model of cortical activity

& hemodynamic impulse

Localcontrast

Rt

Rh

Rl

Neuralactivity

e-t/τ1 sin(2πf1t) - a e-t/τ

2 sin(2πf2t)Hemodynamic

impulse

PredictedfMRI response

9s

t

0

1

2

time (sec)

fMR

I r

esp

onse

(%

)

0 2 4 6 80

.5

1

time (sec)

0

.5

1

time (sec)

DN PN

SL

fixed parameters:

τ2=7.4, f

2=.12

a

f1

τ1

Rh/Rl

Rt

.1

.053

7.0

5.5

.5

SL

.1

.065

6.5

6.5

.75

PN

.08

.035

7.0

8

.5

DN

0 2 4 6 8

0 2 4 6 8

Model fits

Lee, Blake, & Heeger, Nature Neurosci (2005)

Estimated neural latencyN

eur

al lat

enc

y

Time

Lee, Blake, & Heeger, Nature Neurosci (2005)

0

0.5

1.0

1.5

2.0

2.5

0 1 2 3

Est

imat

ed n

eur

al lat

enc

y (s

ec)

Distance (cm)

DN

PN

SL

Observer

Ave speed = 2 cm/sec

Attention signals in V1

Gandhi, Heeger, & Boynton, PNAS (1999)

left eye right eye

Diverted attention

displayC

C2DA3B42D...Detect repetition

C

Time

0

.4

.8

-.4

-.8

0 3 6 9

0

.4

.8

-.4

-.8

fMR

I r

esp

onse

(% c

han

ge int

ens

ity)

0 3 6 9

Time (sec) Time (sec)

Rivalry (perceived) Diverted attention

Waves in V1 without

attention/perception

Diverting attention eliminates

waves in V2 & V3

0

10

20

30

-10

-20Dif

fere

nce in

tim

e t

o pe

ak (

%) V1 V2 V3

Rivalry tracked

Replay tracked

Rivalry diverted-attention

Replay diverted-attention

0 2 4 6 8

Time (sec)

fMR

I re

sponse (

%)

0 2 4 6 8

Time (sec)

fMR

I re

sponse (

%)

0 2 4 6 8

Time (sec)

fMR

I re

sponse (

%)

10

-20

-10

20

0

Diffe

rence in tim

e to p

eak (

%)

Rivalry-tracked inverted

No wave carrier

V1 V2 V3

.2

0

.4

.6

-.2

-.4

-.6

.2

0

.4

.6

-.2

-.4

-.6

.2

0

.4

.6

-.2

-.4

-.6

Rivalry-tracked inverted Trigger only

No wave carrier

Control experiments

Summary

- V1 activity correlated with spatio-temporal dynamics of

perceptual waves during binocular rivalry.

- The velocity of neural waves in V1 matched the latency

of perceptual waves.

- Neural waves in V1 were still present when attention

was diverted, but weaker in amplitude and faster in

velocity.

- V2 and V3 exhibited cortical waves of activity during

rivalry but the waves were eliminated when attention was

diverted.

Implications

- Neural wave propagation is intrinsic to V1.

- Attention is required for neural waves to be

consciously perceived, through interactions between V1

and later visual areas.

- Constrains models of binocular rivalry (rivalry

hierarchy: both early and late).

- Constrains models of processing and circuitry in V1

(waves are slow relative to action potential propagation

and synaptic transmission).