How

is th

e de

velo

pmen

t of c

ortic

al m

aps

in V

1 co

ordi

nate

dac

ross

cor

tical

lami

na?

Man

y ne

ural

mod

els p

ropo

se h

owm

aps

of o

rient

ation

(OR)

, ocu

lar d

omina

nce

(OD)

, dis

parit

y,et

c., s

elf-o

rgan

ize.

Thes

e m

odels

sho

w ho

w sp

onta

neou

sac

tivity

, be

fore

eye

ope

ning

, co

mbin

ed w

ith c

orre

latio

nlea

rnin

g, c

an g

ener

ate

map

str

uctur

es s

triki

ngly

simi

lar

toth

ose

foun

d in

viv

o. M

ost o

f the

se m

odel

s do

not

disc

uss

lamin

ar a

rchit

ectu

re o

r how

cell

s de

velo

p th

eir c

onne

ctio

nsac

ross

cor

tical

lay

ers.

This

is

an e

spec

ially

im

porta

ntpr

oblem

gi

ven

anato

mic

al ev

iden

ce th

at clu

sters

ofho

rizon

tal

conn

ectio

ns,

betw

een

iso-

orie

nted

regi

ons,

in

laye

r 2/3

form

bef

ore

bein

g in

nerv

ated

by la

yer 4

affe

rent

s.An

atom

ical e

viden

ce d

emon

stra

tes

that

tha

lamic

affe

rent

swa

it in

the

subp

late

for

week

s be

fore

inne

rvat

ing

laye

r 4.

Thes

e pr

oblem

s ar

e ad

dres

sed

with

in a

mod

el o

f how

the

corti

cal s

ubpla

te se

lf-or

gani

zes O

R an

d OD

map

s whi

ch th

enen

train

thos

e of

the o

ther

lam

ina.

Othe

r evi

denc

e sh

ows

that

subp

late

abla

tion

inter

feres

with

the

dev

elopm

ent o

f OD

colu

mns.

W

e de

mon

strat

e th

at th

e sa

me

type

s of

mec

hani

sms

whic

h ha

ve b

een

prop

osed

to d

evelo

p OR

and

OD m

aps i

n ea

rlier

mod

els o

f the

cor

tical

plat

e ca

n dr

ive th

eirde

velo

pmen

t in

the

subp

late.

The

mod

el de

mon

stra

tes

how

thes

e m

aps

may

the

n be

tran

sferr

ed to

laye

r 4 b

y a

know

ntra

nsien

t sub

plat

e-lay

er 4

circ

uit.

The

mod

el als

o su

gges

tsho

w de

velo

pmen

t with

in o

ther

lamin

a m

ay b

e sim

ilarly

entra

ined

afte

r ax

ons

from

the

sub

plat

e to

mar

gina

l zon

eco

ntac

t de

ndrit

es o

f th

e su

prag

ranu

lar a

nd i

nfra

gran

ular

corti

cal la

yers

.S

up

por

ted

by:

Su

ppo

rted

in p

art

by

AFO

SR

, D

AR

PA

, N

SF

,an

d O

NR

.

1. A

BSTR

ACT

Grin

vald

(http

://ww

w.we

izman

n.ac

.il/b

rain

/imag

es/cu

bes.h

tml)

2. A

DULT

ORG

ANIZ

ATIO

N OF

V1

Ocul

ar D

omin

ance

Col

umns

(ODC

s)Al

tern

atin

g st

ripes

of c

orte

x re

spon

d pr

efer

entia

llyto

visu

al in

puts

of e

ach

eye

R/L

in F

igur

e

Orien

tatio

n Co

lum

nsA

smoo

th p

atte

rn o

f cha

ngin

g or

ienta

tion

pref

eren

ceOr

gani

zed

in a

pinw

heel

like f

ashi

on

(

in

Fig

ure)

Horiz

onta

l pro

jectio

nsco

nnec

t are

as o

f sam

eoc

ular

dom

inan

ce

Bosk

ing

et al

., 199

7

Horiz

onta

l pro

jectio

nsco

nnec

t are

as s

imila

ror

ienta

tion

pref

eren

ce

Lowe

l et a

l., 19

92

3. L

ATER

AL C

ONNE

CTIO

NS IN

V1

Clus

ters

of l

ater

al p

roje

ctio

ns a

re fo

und

in th

esu

prag

ranu

lar an

d in

fragr

anul

ar la

yers

5. DE

VELO

PMEN

TAL

QUES

TION

S

How

do O

cula

r Dom

inan

ce &

Orie

ntat

ion

map

s for

m in

V1?

Ocul

ar d

omin

ance

col

umns

and

orie

ntat

ion

tuni

ngar

e fou

nd b

efor

e eye

ope

ning

in th

e cat

How

do co

rtica

l col

umns

form

?Co

nsis

tent

tuni

ng is

foun

d ac

ross

ver

tical

pene

tratio

ns in

V1

How

can

this

occu

r whe

n m

aps d

evelo

p be

fore

inte

rlam

inar

corti

cal c

onne

ctio

ns h

ave m

atur

ed?

How

are

orien

tatio

n co

lum

ns an

d clu

ster

s of

horiz

onta

l con

nect

ions

coo

rdin

ated

?Cr

ude c

lust

ers o

f hor

izont

al co

nnec

tions

are f

ound

in la

yer 2

/3 pr

ior t

o ar

rival

of af

fere

nts f

rom

laye

r 4

Thes

e clu

ster

s con

nect

iso-

orien

ted

colu

mns

inm

atur

e ani

mals

The

conn

ecte

d re

gion

s ar

e co

nsis

tent

bef

ore

and

afte

r int

erlam

inar

con

nect

ions

dev

elop

Mol

ecul

ar g

radi

ents

pro

vide

a c

rude

map

Ephe

rins,

Netri

ns, S

emap

horin

s, Sl

it, et

c.

Activ

ity re

fines

exi

stin

g m

aps

Activ

ity p

rovid

es co

rrelat

ions

bet

ween

relat

ed ce

lls

Mig

ratin

g N

euro

n

Ret

ina

Tec

tum

Nas

al

Tem

pora

lA

nter

ior

Po

ster

ior

A Na

sal-T

empo

ral

grad

ient o

f Eph

rece

ptor

sin

retin

al ga

nglio

n ce

llsin

tera

ct w

ith an

terio

r to

post

erio

r gra

dien

ts o

fre

pella

nt e

pher

in lig

and

in th

e Te

ctum

. The

resu

ltis

a cru

de re

tinot

opic

map

.

Norm

al De

velo

pmen

t ‡‡‡‡

Bino

cular

Dep

rivat

ion

‡‡‡‡

Mono

cular

Dep

rivat

ion

‡‡‡‡

Coo

k et

al,.

199

9

LGN

6. D

EVEL

OPM

ENTA

L M

ECHA

NISM

S TTX

7. C

ORTI

CAL

SUBP

LATE

Corti

cal s

ubpl

ate f

orm

s circ

uit w

ith L

GNLG

N af

fere

nts w

ait in

sub

plat

e fo

r wee

ks b

efor

e the

ysy

naps

e in

corti

cal p

late

(Gho

sh &

Sha

tz 19

94)

Ablat

ion

of su

bplat

e sto

ps m

ap fo

rmat

ion

Whe

n su

bplat

e is a

blat

ed, o

cular

dom

inan

ceco

lum

ns fa

il to

form

(Gho

sh &

Sha

tz 19

92)

Orien

tatio

n tu

ning

and

orien

tatio

n m

aps d

o no

tde

velo

p af

ter s

ubpl

ate

ablat

ion

(Kan

old

et al

., 200

1)

Subp

late

conn

ects

to L

ayer

4 (G

hosh

1995

)

Conn

ectio

ns ex

ist fr

om su

bplat

e to

Laye

r 4 w

hen

LGN

affe

rent

s beg

in to

gro

w in

to L

ayer

4

Subp

late

conn

ects

to L

ayer

2/3

Subp

late

conn

ects

to L

ayer

1 (A

llend

oerfe

r & S

hatz

1994

)

Laye

r 2/3

has d

endr

itic

arbo

rizat

ions

in L

ayer

1

Albu

s & W

olf 1

984

8. E

ARLY

TUN

ING

CHAR

ACTE

RIST

ICS

Early

vis

ual r

espo

nse

in L

ayer

s 4

and

6Fi

rst l

ight

evo

ked

resp

onse

s at

P8

(pos

tnat

al d

ay 8

)11

% o

f cell

s are

orie

ntat

iona

lly tu

ned;

58%

bias

edNu

mbe

r of t

uned

cel

ls in

crea

ses

afte

r eye

ope

ning

Late

vis

ual r

espo

nse

in la

yers

2/3

and

5Sl

uggi

sh re

spon

se to

light

unt

il W4 (

week

4)By

W3 m

ost c

ells s

how

orien

tatio

n tu

ning

OFF

field

bias

Corti

cal c

ells r

espo

nd to

neg

ative

cont

rast

stim

uli

76%

at P

8Eq

ualiz

es b

y W4

Rece

ptiv

e fie

ld s

ize d

ecre

ases

with

age

Refin

emen

t of i

nitia

l rec

eptiv

e fiel

d

“Cel

ls th

at fi

re to

geth

er w

ire to

geth

er”

Late

ral c

onne

ctio

ns ar

e bet

ween

cells

with

sim

ilar

tuni

ng ch

arac

teris

tics

Ocul

ar D

omin

ance

ODCs

pro

ject m

ore t

o ar

eas o

f sam

e dom

inan

ceth

an o

ther

dom

inan

ce

Blob

s and

Inte

rblo

bs p

rojec

t mor

e to

their

own

type

Orie

ntat

ion

Iso-o

rient

ed ar

eas p

rojec

t prim

arily

to ar

eas o

fsim

ilar o

rient

atio

n

Dive

rsity

~20-

30%

of p

rojec

tions

to d

iffer

ent “

mod

ules

”

Yosh

ioka

et al

., 199

6

Bosk

ing

et al

., 199

7

9. HO

RIZO

NTAL

CON

NECT

IONS

Retin

a

Orien

ted

Lear

ns g

enicu

loco

rtica

l map

Unor

iente

d

On C

ente

r / O

ff su

rroun

d

Lear

ns c

ortic

ogen

icular

map

Rand

om re

tinal

activ

itydr

ives n

etwo

rk b

efor

e eye

open

ing

Subp

late

LGN

10. M

ODEL

SUB

PLAT

E M

AP

Orien

tatio

n Ma

p Le

arne

d in

Sub

plat

e

Left

Mono

cular

Stri

pes

Affe

rent

s com

pete

for

terri

tory

Mono

cular

Lay

ers

Cons

erve

d # s

ynap

ses

Eyes

are u

ncor

relat

ed

Subp

late

LGN

Ocul

ar D

omin

ance

Map

Lea

rned

in S

ubpl

ate

Retin

aRi

ght

Subp

late

map

is ta

ught

to L

ayer

4

Patte

rned

vis

ual in

puts

driv

e se

greg

atio

n of

ON an

d OF

F su

bfiel

ds in

Lay

er 4

neu

rons

At s

timul

us e

dges

, ON

and

OFF

thal

amic

cel

ls a

resp

atia

lly o

ut o

f pha

se a

nd th

us a

nti-c

orre

late

d

Left

Righ

t

Retin

a

LGN

Subp

late

Laye

r 4

11. M

ODEL

LAY

ER 4

MAP

Ori

ente

d

Lea

rned

Lay

er 4

map

emul

ates

LG

N-S

ubpl

ate

map

Subp

late

act

ivity

gui

des

mig

ratio

n of

axo

ns a

ndpa

ttern

of s

ynap

toge

nsis

from

LG

N to

Lay

er 4

ON

and

OFF

laye

rsbe

com

e eq

ually

act

ive

whe

n ey

es o

pen

Whe

n ey

es o

pen,

rand

om r

etin

al a

ctiv

ityis

rep

lace

d by

pat

tern

edvi

sual

inpu

ts

12. M

ODEL

LAY

ER 2/

3 MAP

Subp

late

guid

es h

orizo

ntal

con

nect

ions

Retin

a

LGN

Subp

late

Left

Righ

t

Laye

r 2/3

Syna

pses

with

Sub

plat

ein

Lay

er 1

Clus

tere

d ho

rizon

tal

conn

ectio

ns

Subp

late

activ

ityin

stru

cts d

evelo

pmen

tof

Lay

er 2/

3 con

nect

ions

On C

ente

r / O

ff su

rroun

d

Rand

om re

tinal

activ

itydr

ives n

etwo

rk b

efor

eey

e ope

ning

13. M

ODEL

LGN

-TO-

SUBP

LATE

MAP

Orien

tatio

n Co

lum

ns

Ocul

ar D

omin

ance

Col

umns Oc

ular

Dom

inan

ce C

olum

nsde

velo

p in

sub

plat

e wi

thhe

lp o

f co

nser

vatio

n of

LGN

syna

pses

[plo

t of o

cular

ity in

dex]

Orien

ted

cells

self

orga

nize

in s

ubpl

ate

[Len

gth

show

s deg

ree o

for

ienta

tion

tuni

ng an

d an

gle

show

s pr

efer

ed o

rient

atio

n]

14. Q

UANT

IFIC

ATIO

N OF

SUB

PLAT

ETU

NING

Matri

ces o

f Weig

hts

Feed

forw

ard

patte

rn o

fco

nnec

tions

from

the L

GNRe

cept

ive fi

elds i

nitia

lized

aswe

ight

noi

se

Orien

ted

prof

iles d

evelo

p

Peak

Orie

ntat

ion

Netw

ork i

s pro

bed

with

stim

uli o

f diff

eren

t orie

ntat

ion

Peak

orie

ntat

ion

is pl

otte

d

Leng

th sh

ows o

rient

atio

nin

dex

Orien

tatio

n Tu

ning

Cur

ves

Orien

tatio

n tu

ning

curv

esca

lculat

ed fo

r eac

h ce

ll

Most

fit a

gau

ssian

pro

file

with

half

widt

hs ~

30˚ f

or tu

ned

cells

0.79

1.00

0.54

0.48

15. L

EARN

ED L

GN-T

O-4

MAP

Subp

late

Laye

r 4Oc

ular

Dom

inan

ce C

olum

ns

Orien

tatio

n Co

lum

ns

Maps

in th

e Su

bplat

e ar

e tau

ght t

o La

yer 4

AFFE

RENT

S FR

OM O

N LA

YERS

AFFE

RENT

S FR

OM O

FF L

AYER

S

16. O

N/OF

F IN

LAY

ER 4

ON a

nd O

FF s

egre

gatio

n wh

en e

yes

open

Spat

ially

offs

et O

N &

OFF

cells

fire

to s

ame

edge

Antic

orre

latio

n d

rives

segr

egat

ed re

cept

ive fi

elds

Sign

ifica

nt d

iver

sity

exi

sts

in a

rrang

emen

t of O

Nan

d OF

F su

bfiel

ds in

corti

cal r

ecep

tive f

ields

17. M

ODEL

SUB

PLAT

E AB

LATI

ON

Ocul

ar D

omin

ance

Col

umns

fail t

o de

velo

p

Orien

tatio

n Tu

ning

fails

to d

evelo

p

Som

e ce

lls h

ave

a si

gnifi

cant

tuni

ng in

dex

but i

nspe

ctio

n of

the c

urve

s sho

w no

tuni

ng

(Gho

sh &

Sha

tz 1

992)

(Kan

old

et al

., 200

1)

18. L

AYER

2/3 C

LUST

ERED

HORI

ZONT

AL C

ONNE

CTIO

NSSu

bplat

e Gu

ides

Hor

izont

al C

lust

ers

Clus

terin

g is

simila

r to

in vi

vo at

eye o

peni

ng

Recip

roca

l con

nect

ions

bet

ween

laye

r 2/3

cells

Dive

rsity

in sh

ape a

nd o

rient

atio

n of

clus

ters

Mode

l Res

ults

Data

from

Sin

cich

and

Blas

del 2

001

19. O

THER

MOD

ELS

Most

mod

els ar

e sin

gle l

ayer

edOt

her d

evelo

pmen

tal m

odels

hav

e not

dem

onst

rate

d ho

w ve

rtica

l col

umns

arise

Clus

terin

g in

Lay

er 2

/3 ra

rely

add

ress

edTh

e coo

rdin

ated

dev

elopm

ent o

f lay

er 2/

3 hor

izont

alco

nnec

tions

with

map

s of

orie

ntat

ion

and

ocul

ardo

min

ance

has

not

pre

viou

sly

been

mod

eled

The

subp

late

goe

s unn

otice

dOu

r mod

el is

the f

irst t

o us

e the

sub

plat

e to

expl

ainco

rtica

l dev

elopm

ent

LAMI

NART

Mod

el (G

ross

berg

and

Willi

amso

n 20

01)

Dem

onst

rate

s ho

w pa

ttern

ed v

isio

n ca

n re

fine

horiz

onta

l con

nect

ions

in L

ayer

2/3

Afte

r dev

elop

men

t the

se c

ircui

ts g

ener

ate

prop

ertie

s of a

dult

perc

eptu

al gr

oupi

ng

The

pres

ent m

odel

is c

onsi

sten

t with

thes

e re

sults

20. C

ONCL

USIO

NS

Subp

late

enab

les d

evelo

pmen

t of C

olum

nsLe

arns

Orie

ntat

ion

and

Ocul

ar D

omin

ance

Map

s

Teac

hes

OR a

nd O

DC to

Lay

er 4

Inst

ruct

s clu

ster

ing

of L

ayer

2/3 c

onne

ctio

ns

Rem

oval

of S

ubpl

ate

elim

inat

es m

ap fo

rmat

ion

Eye

open

ing

segr

egat

es O

N &

OFF

inpu

tsTh

e in

trodu

ctio

n of

pat

tern

ed v

isio

n pr

ovid

es a

spat

ial a

ntico

rrelat

ion

of O

N an

d OF

F ce

lls

Futu

re D

irect

ions

Deve

lop

inte

rlam

inar

conn

ectio

ns

Allo

w su

bplat

e to

die

Deve

lop

layer

2/3 m

aps

Inco

rpor

ate m

ore r

ealis

tic in

hibi

tory

circ

uit a

ndde

velo

p in

hibi

tory

con

nect

ions

Gene

raliz

es m

odel

to o

ther

corti

cal a

reas

, suc

h as

A1 an

d ex

trast

riate

are

as

21. R

EFER

ENCE

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10.

CO

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phen

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rg (s

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ogni

tive

& N

eura

l Sys

tem

s, B

osto

n U

nive

rsity

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ton,

MA

, USA

Crair

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