Journal
of
Comparative
and
Physiological
Psychology
1970,
Vol.
73, No.
2,
181-187
DEVELOPMENT
AND
SEGMENTATION
OF
VISUALLY
CONTROLLED MOVEMENT
BY
SELECTIVE
EXPOSURE
DURING
REARING
1
ALAN
HEIN,
2
RICHARD
HELD,
AND
ELLEN
C.
GOWER
Massachusetts
Institute
of
Technology
Three experiments
are
reported
which
clarify
the
role
of
movement-pro-
duced
changes
in
visual stimulation
for the
acquisition
of
visually con-
trolled behaviors.
The first
study
shows
that
exposure during passive
transport, which provides
an
asystematic
relation between self-produced
movements
and
visual
stimulation,
delays
the
acquisition
of
visual-motor
coordination when
a
kitten
is
subsequently
free
to
locomote
in
light.
The
second experiment
demonstrates
that
control
of
movement
by one
eye
develops
if
that
eye is
exposed during locomotion.
This
control does
not
transfer
to the
contralateral
eye
which
is
exposed
only
during
passive
transport.
In the final
experiment, view
of the
forelimbs
is
restricted
to one
eye. Visually guided reaching develops under
the
control
of
that
eye
but
does
not
transfer
to the eye
which
has not
viewed
the
limbs.
The
results
of
Experiments
2 and 3
provide evidence
that
the
system
for
visual
guidance
of
movement consists
of
components which
can be
acquired
inde-
pendently.
Movement
during exposure
to
patterned
light
has
been recognized
as
important
for
the
development
arid
maintenance
of
visually
guided behaviors
in
higher mam-
mals
by
Hebb (1949),
Hein
(1968), Held
(1961),
Riesen
(1958),
and
others.
One set
of
observations consistent with this prem-
ise
derives
from
experiments
in
which ani-
mals
are
deprived
of
patterned
light
stimulation. Rearing
in the
dark
or in
diffused
light produces substantial
deficits
in
visually controlled behavior (Ganz
&
Fitch, 1968; Riesen,
Kurke,
&
Mellinger,
1953;
Wiesel
&
Hubel,
1965a). Although
neural
dysfunction
has
been observed
in
these animals (Ganz, Fitch,
&
Satterberg,
1968; Wiesel
&
Hubel, 1965b),
there
is
evidence
to
suggest
that
visual-motor
deficits
are not due
solely
to
abnormalities
of
the
visual system (Ganz
&
Fitch,
1968;
Meyers
&
McCleary,
1964; Wiesel
&
Hubel, 1965a). Whatever damage
to the
1
This
research
was
supported
by
Grants
GB-
2728
and
GB-6712
from
the
National
Science
Foundation
and
Grant
NGL-22-009-308
from
the
National
Aeronautics
and
Space
Administration.
The
authors
are
grateful
to
Rhea Diamond
for her
help
in the
preparation
of
this manuscript.
2
Requests
for
reprints
should
be
sent
to
Alan
Hein, Department
of
Psychology, Massachusetts
Institute
of
Technology, Cambridge, Massachu-
setts
02139.
visual
system results
from
patterned light
deprivation, exposure
to
patterned light
does
not by
itself
assure normal develop-
ment
of
visually
controlled behavior.
Di-
rect evidence
is
provided
by
experiments
in
which neonates
are
either
free
to
loco-
mote
in an
intermittently illuminated
en-
vironment
or
provided with
patterned
light
stimulation
only when prevented
from
moving.
These animals
fail
to
develop
visually guided behaviors (Hein, Gower,
&
Diamond,
1970).
Hein
and
Held (1962) suggested
that
the
mechanism which underlies acquisition
of
visually
guided behaviors utilizes
the
correlation
between self-produced move-
ment
and
change
in
visual stimulation.
In
an
experimental examination
of
this
hy-
pothesis,
kittens
that
locomoted
in
pat-
terned
light were compared with kittens
passively transported within
the
same
environment
(Held
&
Hein, 1963). When
tested,
the
animals
that
had
locomoted
showed
visual placement
of
their
fore-
limbs
and
discrimination
of
deep
from
shallow
sides
of a
visual
cliff,
but
their
passively transported
littermates
did
not.
After
considering
a
number
of
alternative
explanations,
the
authors concluded
that
variation
in
visual
stimulation
concurrent
with
and
systematically dependent upon
181
182
A.
HEIN,
R.
HELD,
AND E. C.
GOWER
self-produced movement
is the
essential
condition
for
development
of
visually
guided
behaviors.
Since
that
time
certain
implications
of
this
hypothesis have been
experimentally
investigated
and
summa-
rized
in the
literature
(Hein, 1970; Held,
1968a).
In the
present
paper
the
authors
report three
of
these studies
in
detail
and
examine
more closely
the
contribution
of
motor-visual feedback
to the
development
of
visually coordinated behavior. Experi-
ment
1
examines
the
effects
of
prior expo-
sure during passive transport upon subse-
quent acquisition
of
visually controlled
behavior
during locomotion. Experiment
2
examines
the
effects
of
exposing
one eye
during locomotion
and the
other
eye
dur-
ing
passive
transport.
Experiment
3 de-
termines
if the
development
of
visually
guided reaching, which requires view
of
the
limbs,
can be
acquired independently
by
each eye.
EXPERIMENT
1
Although
deficient
in
visual placing
and
cliff
discrimination,
passively
transported
kittens
show pupillary
reflexes,
visual-
centering
responses,
tactual
responses,
and
other motor activities immediately
follow-
ing
exposure
in a
gondola (Held
&
Hein,
1963). When
the
transported animals
are
removed
from
the
gondola
and
permitted
free
locomotion
in
patterned light,
they
rapidly acquire visually controlled behav-
iors. These observations imply
that
pas-
sive transport neither induces general
de-
bility
of the
motor system
nor
results
in
deterioration
of
peripheral
parts
of the
visual
system.
Held
and
Hein
(1963) have
suggested
that
deficits
in the
passively
transported
animals
result
from
deprivation
of
the
motor-visual feedback essential
for
development
of
visually
controlled
behav-
iors. Alternately,
visually
controlled
be-
haviors
may
develop
during
passive
trans-
port
but at a
much slower
rate
than
during
locomotion.
However,
the finding
that
pro-
longed
transport
(126
hr.)
did not
result
in
acquisition
of
visually
triggered
extension
of
the
limbs
or
discrimination
on a
visual
cliff
argues against
this
alternative.
It
remains
possible
that
the
later
development
of
vis-
ual-motor coordination
is
either
facilitated
or
impeded
by
passive
transport.
The
pres-
ent
experiment examines
the
effect
of
prior
transport
on the
time
required
for
develop-
ment
of
visually controlled behaviors during
subsequent
locomotion.
Method
Exposure
apparatus.
The
carousel apparatus
de-
scribed
by
Held
and
Hein
(1963)
was
used
to
con-
trol movements
and
visual experience
of
young
kittens.
The
animals were held with neck yokes
and
halters
at
opposite ends
of a
lever pivoted
at
its
center.
The
lever
and
appropriate mechanical
linkages
transferred
the
movements
of the
loco-
moting kitten
to the
kitten transported
in a
gon-
dola. Symmetry
of the
visible surround provided
both
animals with
a
similar
view. Visual
stimula-
tion
was
systematically related
to
self-produced
movements
for the
locomoting animals.
For the
transported
animals,
the
relation between self-
produced
movements
and
visual stimulation
was
asystematic, having been perturbed
by
movements
of
the
gondola.
Subjects.
Immediately after birth,
19
kittens
were
placed with
their
mothers
and
littermates
in
large
cages
within
a
totally darkened room. There-
after
they remained
in the
dark until termination
of
the
experiment except during periods
of
expo-
sure
in the
carousel apparatus
and
during testing
of
visual-motor
capacities.
Procedure.
When
the
experimental
kittens
were
8 wk. of age
they
were
removed daily
from
the
darkroom
and
placed
in the
gondola
for 3 hr. of
exposure
in
patterned light.
A
kitten
of the
same
age
locomoted
at the
other
end of the
lever.
Its
movements were transformed
by the
apparatus
into movements
of the
gondola. This procedure
was
repeated
for 11
days, providing
33 hr. of
passive transport
in
light
for the
experimental ani-
mals—3
hr.
more
than
the
average
duration
of
locomotion
found
sufficient
for
development
of
visually guided behaviors
in the
previous study.
At
the end of
Hour
33, the
experimental
kittens
were
removed
from
the
gondola,
the
vibrissae were
cut,
and the
kittens tested
for
visual placing.
Al-
though
forelimb
extension could
be
elicited
by
vestibular
or
tactual stimulation, none
of the
passively
transported
animals
extended
their
limbs
on
approaching
a
broad
surface.
The
present
au-
thors
now
refer
to
this response
as
visually trig-
gered
extension.
As
previously emphasized (Held
&
Hein, 1963),
this
extension response provides
a
test
of
visual-motor capacity which does
not re-
quire
prior training
and
hence does
not
confound
exposure
with testing. Only
a
technique
that
meets
this requirement
can
reveal deficits which
may be
readily
overcome during training.
On
the day
following
testing,
the
animals were
returned
to the
apparatus
but
placed
at the op-
posite
end of the
lever
and
permitted
to
locomote
for
3 hr. A
metal
bar
equal
in
weight
to the
kitten
was
placed
in the
gondola. This exposure
was re-
peated daily until
the end of the
experiment.
After
DEVELOPMENT
OF
VISUALLY
CONTEOLLED
MOVEMENT
183
each
exposure
period,
the
animals
were
tested
for
visually triggered extension.
The first six
kittens
used
in
this
experiment were also observed during
eight descents
from
the
center platform
of a
visual
cliff
on the day the
extension response
was first
displayed.
Results
All
animals eventually acquired
the ex-
tension response.
The
average duration
of
locomotion
necessary
for
this
development
"was
41 hr. In the
original
study,
kittens
of
comparable
age
that
had no
prior exposure
in
light required
a
mean
of
30
hr. to ac-
quire
extension (Held
&
Hein,
1963). Fig-
ure
1
presents
the
distribution
of
durations
of
locomotion
to
acquire
the
extension
re-
sponse
for the
original group
of
locomoting
kittens
and for the
group passively
trans-
ported prior
to
locomotion.
A
Mann-
Whitney
U
test
used
to
assess
the
signifi-
cance
of the
difference
between
these
groups
yielded
p < .05
(two-tailed).
The six
kittens
tested
on the
visual
cliff
were able
to
discriminate
the
shallow
from
the
deep side.
All
descents were
to
the
shallow side
for
five
animals;
one
ani-
mal
descended once
to the
deep side
and
seven times
to the
shallow.
Discussion
The
present experiment reveals
that
prior passive transport delays acquisition
of
visually triggered extension
and
vis-
ual-cliff
discrimination during subsequent
locomotion.
If
passive transport simply
deprives
the
animal
of
feedback essential
for
development
of
coordinated visual-
motor behaviors,
no
delay would
be ex-
pected.
The
delay
of
acquisition during
subsequent
locomotion indicates
that
ex-
posure
with asystematic
feedback,
as
provided
by
transport
in the
gondola,
has
some
special disruptive
effect.
Another
piece
of
evidence consistent
with this interpretation
is the
observation
that
passively transported animals
do not
exhibit
visually triggered extension.
This
response
has
been shown
to
develop with
exposure
in
light,
in the
absence
of
view
of
the
limbs (Hein
&
Held, 1967), and,
in-
deed,
in the
absence
of any
motor-visual
feedback
(Hein
et
al.,
1970).
The
failure
of
kittens transported
in the
gondola
to
Mlocomotion
without
prior
exposure
(fromHeld&Hem,l°63)
•
passive
transport
prior
to
locomotion
3-25
26-28
29-31
32-34
35-37
3S
T
40
41-68
HOURS
OF
EXPOSURE
FIG.
1.
Number
of
hours
of
exposure during
locomotion
necessary
to
acquire extension
re-
sponse
in
groups with
and
without prior passive
transport.
show
the
extension response
can
therefore
be
interpreted
as a
specific
effect
of
expo-
sure with asystematic motor-visual
feed-
back.
EXPERIMENT
2
Held
and
Hein (1963) argued
that
neither disruption
of
performance
by
shock,
fright,
or
overactivation upon
re-
lease
from
the
deprived
state,
nor the
development
of
competing responses, could
account
for the
deficits
which
follow
pas-
sive transport. Such behaviors were
not
seen
during observation
of
their experi-
mental animals
at the end of the
exposure
period.
At
that
time
the
kittens
that
had
been
passively transported displayed
ap-
propriate pupillary
and
pursuit
reflexes
and
tactual-placing responses. This sug-
gests
that
the
deficits
of
passively
trans-
ported animals
do not
reflect
atrophy
of
the
visual system
or
debility
of the
motor
system. However,
it is
possible
that
these
animals
fail
to
perform visual-placing
re-
sponses
and
visual-cliff discriminations
due to
generalized inhibition
of
movement
in
response
to
visual stimuli. This possi-
bility
may be
excluded
by
showing
that
the
passively transported kitten
performs
visually
controlled movements under cer-
tain
conditions.
The
attempt
to
meet
this
requirement involves
the
exposure
of
each
eye
under
a
different
condition. Riesen
et
184
A.
HEIN,
R.
HELD,
AND E. C.
GOWER
TABLE
1
DESCENTS
FROM
VISUAL
CLIFF
FOLLOWING
ALTER-
NATING
MONOCULAR
EXPOSURE
DURING
LOCOMOTION
AND
PASSIVE
TRANSPORT
Subject
1
2
3
4
5
6
Total
during
locomotion
R
L
L
L
R
L
Cliff
descents
(shallow/deep)
Eye
exposed
during
locomotion
8/0
8/0
8/0
7/1
7/1
8/0
46/2
Eye
exposed
during
transport
5/3
2/6
4/4
6/2
5/3
5/3
27/21
al.
(1953)
and
Chow
and
Nissen (1955),
using
a
similar procedure,
found
deficits
in
interocular transfer
of
discriminations
learned
monocularly.
Their results sug-
gested
that
exposing
one eye
during loco-
motion
and the
other
during
passive
trans-
port
might produce
an
animal which showed
visually controlled responses when tested
with
one eye but not
when tested with
the
other.
Method
Subjects.
Immediately
after
birth,
six
kittens
were
placed
in the
dark with their mothers
and
littermates
and
remained
in
darkness except dur-
ing
periods
of
controlled exposure
in
light
and
testing.
Procedure. Beginning when
they
were
4 wk. of
age,
the
kittens
received
3 hr. of
exposure
daily.
When
a
kitten
was
removed from
the
dark,
an
opaque
vinyl
occluder
was fitted
over
the
solera
and
under
the lid of one
eye.
The
animals
were
run
in
pairs.
One
kitten
was
passively
transported
in a
gondola
at one end of
the
levered
arm
while
the
other
was
free
to
locomote
at the
other end.
After
1.5 hr. of
exposure
in
light,
the
occluder
was
transferred
to the
contralateral
eye and the
posi-
tions
of the two
animals exchanged.
This
exposure
was
continued
for 1.5
additional
hr.
Thus,
periods
when
visual
stimulation
of one eye
accompanied
self-produced movement
alternated
with periods
when
visual
stimulation
was
provided
to the
other
eye
during passive
transport.
The
kittens
were
tested
monocularly after each
1.5 hr. of
exposure
for
presence
of the
extension response. Scoring
was
done
by an
observer
who did not
know
the
exposure history
of the
animal.
On the day
that
the
kitten
first
showed triggered extension, using
either eye,
it was
tested
monocularly with each
eye for
discrimination
on the
visual
cliff.
Results
The
results
of
this
experiment
are
sum-
marized
in
Table
1.
When using
the eye
exposed
during locomotion,
all
kittens
eventually
showed
both
visually
triggered
extension
to a
broad horizontal surface
and a
preference
for the
shallow side
of the
visual
cliff.
When using
the eye
exposed
during
passive transport,
no
kitten
showed
the
extension response
and all
failed
to
discriminate between
the
shallow
and
deep
sides
of the
visual
cliff.
A
sign
test
of
the
difference
between number
of
descents
to
the
shallow side when using
the
actively
vs.
passively
exposed
eye is
significant
at
p
< .03
(one-tailed).
Discussion
When
using
the eye
exposed during loco-
motion,
the
kitten displays visually con-
trolled
behaviors. When using
the eye
ex-
posed
only during passive transport, these
responses
are
absent. Since
the
animal does
respond
appropriately
to
visual stimuli,
generalized
response inhibition cannot
ac-
count
for
deficits
resulting
from
passive
transport.
The
results
of
Experiments
1 and 2
when
taken together with
the
report
of
Hein
et
al.
(1970) indicate
that
each condition
of
exposure
may
support
the
development
of
certain capacities
and not
others. Animals
that
have been dark-reared show
no
visually controlled behavior except pupil-
lary
reflexes
and
visual-centralizing
re-
sponses.
.
Rearing
in
diffused
light
allows
the
triggered component
of the
visual-
placing
response
to
develop, while visually
guided
reaching
and
visually guided loco-
motion
do
not. Exposure
of an
immobilized
kitten
in a
normally illuminated environ-
ment
or
exposure
of a
freely
locomoting
kitten
in a
stroboscopically illuminated
environment
will
not
support development
of
visually guided behaviors, although
the
visually triggered extension response
is
acquired.
Visually guided behaviors
de-
velop
only when
the
exposure conditions
provide opportunity
for
self-produced
movement
systematically
associated
with
changes
in
visual stimulation. When
self-
produced
movements
are
asystematically
DEVELOPMENT
OF
VIStJAELY
1
GONTROLLEB
MOVEMENT
185
associated
with
changes
in
visual
stimula-
tion neither
visually
guided
behaviors
nor
the
visually triggered extension response
develop.
The
demonstration
that
the
development
of
visual-motor coordination
is
displayed
only when using
the eye
exposed during
locomotion
has a
further implication.
Control
of
behavior
by
each
eye is
iden-
tified
as an
independent component
of
visual-motor
coordination. Acquisition
of
each
component requires exposure
of
that
eye
with visual feedback
from
self-pro-
duced
movements.
This
finding
encouraged
the
search
for
other independent compo-
nents
of
visual-motor coordination.
EXPERIMENT
3
"
Hein
and
Held
(1967)
have
shown
that
visually controlled placing
of the
forelimbs
has
both triggered
and
guided components.
Only
the
triggered component developed
when
kittens
locomoting
in
light
were pre-
vented
.from
viewing
their
limbs. These
animals displayed
the
extension response
to a
broad surface
but
could
not
guide
their
limbs
to the
position
of a
small
target
in
visual space.
Failure
to
develop visually
guided reaching
was not
accompanied
by
deficits
in the use of the
limbs
for
visually
guided locomotion.
The
kittens
moved
about
efficiently;
they
avoided
obstacles
and
were
indistinguishable
from
normal animals
as
they
jumped
on and off
various objects.
It was
concluded
that
use
of
the
limbs
in
visually guided locomotion
and
visually guided reaching
by
those
same
limbs constitute
two
independent
components
of
visual-motor coordination.
The
present experiment determined
whether control
of
visually guided reaching
might
be
acquired independently
by
each
eye.
This
possibility
was
examined
by
per-
mitting view
of the
limbs
by one eye but
not
the
other.
Method
Subjects.
Of the 12
kittens
which
served
as
sub-
jects
for
this
experiment,
10
were
dark-reared
until
they
were
5-12
wk. of age and
then exposed
in
light
for
6 hr. a
day.
The
remaining
two
kittens
were
reared
from
birth
in a
room illuminated
for
24
hr.
a
day.
Procedure.
The
animals
that
had
been
dark-
reared were
permitted
to
locomote freely
in
light
for 6 hr. a day
while wearing lightweight
plastic
collars.
For 3 hr.
they
wore
opaque
col-
lars which prevented view
of the
limbs
and
torso
following
the
procedure described
by
Hein
and
Held
(1967).
For the
remaining
3 hr.
they
wore
clear collars
of the
same size
and
weight which
permitted
view
of the
limbs.
Three
different
ex-
posure conditions were used.
In
Condition
A, five
kittens
had one eye
occluded while
the
opaque
collar
was
worn,
and
other
eye
occluded while
the
clear collar
was
worn.
In
Condition
B,
five
kittens
had
both
eyes
open while
the
opaque
collar
was
worn,
and one eye
occluded while
the
clear collar
was
worn. Except
for
these exposure
periods,
all
animals
of
Conditions
A and B
were
kept without collars
in
total
darkness.
In
Condi-
tion
C, two
kittens
were
fitted at
birth
with
opaque
collars large enough
to
prevent view
of
the
limbs without
interfering
with either
lo-
comotion
or
suckling. These animals locomoted
freely
in
light
for 24 hr. a
day.
As the
kittens
grew,
successively
larger collars
were
provided
so
that
view
of the
limbs remained unavailable.
When
the
animals
were
30
days old,
the
opaque
collars
were replaced
by
clear collars
for 3 hr.
each
day, during
which
time
one eye was oc-
cluded.
The
dark-reared
kittens
were
exposed under
Condition
A or
Condition
B for 5, 6, or 7
days
before
being tested
for
visually guided reaching.
The two
kittens
of
Condition
C
were exposed
with monocular view
of the
limbs
for 17 and 21
days,
respectively,
before
testing.
The
animals
were
tested
monocularly,
first
with
one eye and
then with
the
other.
The
apparatus used
for
measuring visually
guided
reaching
is a
board with spaced cutouts
toward which
the
animal
is
lowered (described
by
Hein
&
Held,
1967).
The
discontinuous edge
is
formed
by
prongs 20.0
cm.
long
and 2.5 cm.
wide
separated
by 7.5 cm. A
test
consisted
of 12
trials,
6
with each forelimb. When
the
animal extended
a
limb, contact
of one or
more claws with
the
top of a
prong
was
scored
as a
hit.
Testing
and
scoring
were done
by
observers
who did not
know
the
exposure
history
of the
animal.
Results
The
results
of
Experiment
3 are
pre-
sented
in
Table
2. The
three
conditions
do
not
appear
to
differ
in
their
effects
upon
development
of
guided reaching. When
using
the eye
which
had
previously viewed
the
limbs,
all
kittens
showed
visually
guided
reaching. When using
the eye
which
had
not
previously
viewed
the
limbs,
the
percentage
of
hits
was not
significantly
different
from
chance.
A
sign
test
of the
difference
in
percentage
of
hits
is
signifi-
cant
at p <
.001
(one-tailed).