Download Response Characteristics of Single Cells in the Monkey Superior

Response
Characteristics
Superior
Colliculus
Cooling
of Visual
PETER
H. SCHILLER,
iWassachusetts
Institute
of Single
Following
for
publication
Ablation
or
Cortex
MICHAEL
of
Technology,
STRYKER,
Cambridge,
ELECTROPHYSIOLOGICAL
STUDIES
have shown
that the characteristics
of single cells in the
superior
colliculus
depend
to a considerable extent on cortical
input.
In the cat,
the majority
of studies reveal a dramatic
loss of binocularity
and direction
selectivity
in superficial
collicular
units
following
ablation
of the visual cortex (1, 18, 25). In
the ground
squirrel,
removal
of the visual
cortex renders
most cells in the intermediate and deep layers of the superior
colliculus
unresponsive
to visual stimuli
(14);
this also appears
to apply to the cat (22).
Work
on the rabbit,
however,
indicates
that in this species, ablation
of visual cortex produces
no discernible
effects on collicular
function
(10).
The present study has been undertaken
to investigate
the contribution
of visual
cortex to collicular
function
in the rhesus
monkey
(Macaca
mulatta),
a species whose
visual svstem is believed to be rather similar
to that of man. Neuroanatomical
work has
indicated
that in the monkey, as in the cat,
retina and visual cortex project densely on
the superior
colliculus
(8). In the monkey,
a foveate animal,
an interesting
specialization has been reported:
anterograde-degeneration
and autoradiographic
studies indicate that the anterior
part of the colliculus,
representing
the central
5” of the visual
field, receives extremely
sparse or no terminations
from the retina and, conversely,
heavy projections
from visual cortex (5, 9,
26)
Single-unit
studies of the superior
colliculus of the intact monkey have disclosed
that, as in the cat, most cells have binocular
Received
Cells in the Monkey
April
13, 1973.
MAX
CYNADER,
ltlassachusetts
AND
NANCY
BERMAN
02139
receptive
fields. In contrast to the cat, however, in which
about
70%
of the cells
studied
are selective for direction
of stimulus movement
(1, 13, 23), in the monkey
only a small percentage
of cells has been
found to have this attribute
(2, 4, 20). In
both species cells firing in relation
to eye
movement
have been reported
in the lower
layers of the colliculus
(20, 24, 27). In the
monkey
these cells discharge
prior
to saccades and show specificity
in terms of the
size and direction
of rapid eye movement.
Some of these units have dual properties;
not only do they fire prior
to certain
saccades, but they also have visual receptive
fields. Electrical
stimulation
in this region
of the alert animal
elicits
conjugate
saccades at very low current
levels (19, 21).
On the basis of our earlier
work, we have
suggested that the superior
colliculus
contributes
to the monkey’s
ability
to foveate
visual targets by saccadic eye movements
(20)
To determine
what the contribution
of
the visual cortex is to the function
of the
superior
colliculus
in the monkey,
we obtained
extracellular
single-unit
recordings
from the superior
colliculus
after the cortex
had either been ablated or reversiblv
cooled.
METHODS
The work reported here is based on extracellular recording
from the superior colliculus of
monkeys prepared by three different techniques:
1) anesthetized, paralyzed monkeys with unilateral ablation of visual cortex; 2) anesthetized,
paralyzed monkeys in whom part of visual cortex was reversibly cooled; and 3) alert monkeys
with one eye surgically immobilized,
in whom
visual cortex was unilaterally
removed.
182
SCHILLER,
Anesthetized
animals
with
removal
of visual cortex
STRYKER,
unilatcd
Eight
monkeys
were
studied.
Visual
cortex
was removed
by suction
under
aseptic
conditions
using
Nembutal
anesthesia
223, 122, 111,
56 29, 6, 5, and 5 days prior
to recording
from
thL superior
colliculus.
The lesion
on the dorsal
surface
extended
to the posterior
margin
of the
lunate
sulcus.
The
lesion
was extended
to include the medial
and lateral
convolutions
of the
calcarine
fissure.
For recording,
animals
were first anesthetized
with
Pentothal.
After
tracheotomy
and application of contact
lenses
(see also below),
animals
were
placed
in a stereotaxic
frame.
Two
trephine
holes
were
cut in the skull
above
the
superior
colliculus
to permit
stereotaxic
lowering
of microelectrodes
into
each
colliculus.
During
the experiment
animals
were
paralyzed
by infusion
of Flaxedil
(40 mg/hr)
diluted
with
5% dextrose
in lactated
Ringer
solution
and
were
respirated
with
a mixture
of N,O
and
0, (2). End-tidal
CO, was monitored
and maintained
at 4.0%.
The
methods
for unit
recording,
receptivefield
plotting,
and stimulation
were
similar
to
those previously
reported
(2). Platinum-iridium
electrodes
were used; single
cells were identified
by conventional
criteria
(14). A slide projector
mounted
on a tripod
was used to find the location of the receptive
fields on a tangent
screen
facing
the animal.
For
the quantitative
study
of unit
responses
to light
an optic
bench
was
used, which
through
a lens system,
a shutter,
and a mirror
galvanometer
could
project
stimuli to various
parts of the visual
field. Waveform
generators
were
used to drive
the shutter
and
mirror
galvanometer
(20).
In two animals
our aim was to determine
the
location
of receptive
fields
in the visual
field
with
special
emphasis
on the central
5O. Receptive-field
locations
relative
to the center
of the
fovea
are difficult
to determine
with
sufficient
accuracy
relying
solely
on repeated
plotting
of
the
fovea
with
a reversible
opthalmoscope.
Therefore,
two additional
procedures
to monitor
residual
eye movement
were
employed:
a) recordings
from
a reference
unit
and
b) a
laser optical
lever.
For the reference
unit
the
procedure
was to lower
two
microelectrodes,
one into
each colliculus.
While
exploring
one
colliculus
with repeated
penetrations,
the microelectrode
in the other
colliculus
was kept in one
place,
and the receptive-field
location
of the
reference
unit
or multiple-unit
activity
was
checked
repeatedly
for each eye. Reference
units
were
generally
chosen
in the anterior
part
of
of the colliculus
where
receptive
fields
for single cells
as well
as for multiple-unit
activity
CYNADER,
AND
BERMAN
were small
(< 1”). Thus,
movement
of the rcference
unit’s
receptive
field
on the
tangent
screen was a measure
of residual
eye movement
accurate
to within
t.25”.
This method
was compared
with
the optical-lever
method
and our
repeated
plotting
of the fovea with
a reversible
opthalmoscope.
For the optical-lever
technique
a laser beam
(Edmund
Scientific)
was reflected
from
two
small mirrors
attached
to the contact
lens with
epoxy
glue. The
contact
lens was glued
to the
cornea1
stroma
with
tissue
cement
(histoacryln-blau,
B. Braun,
Melsungen,
W.
Germany)
which
was applied
in a very
thin layer
around
the edge of the lens (3). In order
to expose
the
stroma,
the cornea1
epithelium
was removed
under
anesthesia
by gentle
scraping
with
a scalpel blade
2 min
after
application
of tincture
of iodine
(2%)
to the eye. The
glue
attached
the contact
lens firmly
to the stroma
and provided
a clear
optic
medium
which
did
not
cloud
with
time.
This
method
has been
used
successfully
in other
applications
with
the lens
remaining
attached
and clear for several
months
(3) .
After
the animal
was placed
in the stereotaxic
frame,
the laser beam
was directed
onto
that
portion
of the contact
lens
which
contained
the
two
mirrors,
reflecting
two
small
spots
of light
onto
the tangent
screen.
The
plotting
of each receptive
field was accompanied
by a check
on the reflected
laser-beam
positions,
thus
permitting
an assessment
of eye
movements,
including
rotation.
In some
of the animals,
small
lesions
were
placed
in the superior
colliculus
to mark
microelectrode
positions.
Subsequently
sections
were
stained
with
Nissl
or reduced
silver
stains
(Nauta
and Fink-Heimer
methods).
In animals
with long survival
times, retrograde
cell changes
in the lateral
geniculate
nucleus
were
studied
to determine
how complete
the cortical
ablation
was.
Anesthetized
animals
with
cooling
of visual cortex
reversible
In three
monkeys
a region
of cortical
area
17 was reversibly
cooled
during
recordings
in
the superior
colliculus.
The
recording
method
for the cooling
experiments
was identical
to
those described
above.
Cooling
and rewarming
was accomplished
by use of a “Peltier’‘-type
thermoelectric
cooling
probe
(Cambion
Inc.,
Cambridge,
Mass.);
a silver
plate
for thermal
conduction
was attached
to the probe.
A ZOmm-diameter
circular
extension
of this
plate,
which
fit into a trephine
hole in the skull, was
shaped
to conform
to the contour
of the brain.
Dura
was not removed.
In the center
of the
CORTICOTECTAL
circular plate was a 2-mm-diameter
hole through
which one could insert probes for recording
and temperature
measurement.
This
plate
cooled a region of visual cortex representing
a
4-8O area of the visual field.
Because of the relatively small area cooled,
it was necessary to align the recording and cooling sites topographically.
To do this, in two
of the monkeys we first recorded single cells
in visual cortex by inserting
a microelectrode
through
the center hole of the silver plate,
and we plotted on the tangent screen the location of their receptive fields. Penetrations
were
then made in the-superior
colliculus until units
were obtained with receptive fields no further
than 2--3O from the cortical receptive
fields.
This assured us that the colliculus
electrode
was within
the region
receiving
projections
from the area under the cooling probe. Residual eye movements
were checked using the
optical-lever
technique in one animal and the
method of repeated plotting
of the fovea with
a reversible opthalmoscope
in the other two.
Cooling was commenced by passing current
through the thermoelectric
device using a battery. The amount of current passed was monitored by an ammeter and controlled by variable
resistors which were operated
manually.
A
thermistor temperature
probe in a 24G needle
(Yellow Springs Instruments),
placed either on
the dura or slightly below the surface of the
cortex, was used to measure brain temperature.
In one animal bipolar
EEG was recorded by
attaching two wire electrodes to the thermistor.
Cooling to between 10 and 22 C was accompanied by a flattening
of the EEG signal.
After cooling, cortex could be warmed
to
body temperature
by passing current in the
reverse direction.
The whole procedure
was
quite rapid; a cycle going from 36 to 15 C and
back to 36 C took about 5 min. Unless cooled
to very low temperatures,
cortex would recover
rapidly,
as determined
by cortical EEG and
the responses of units in the superior colliculus.
On return to 36 C, or a few minutes thereafter,
the cooled area appeared to be fully functional.
In one animal we recorded from both colliculi
while cooling one visual cortex.
Alert
mon kevs
The methods used for alert recording
were
similar to those already described (20). One eye
of the monkey was immobilized
by transection
of the third, fourth, and sixth cranial nerves.
Eye-movement
electrodes
were
implanted
around the moving eye. During experimental
sessions the animal’s head was restrained.
Recordings in the superior
colliculus
permitted
study of receptive-field
characteristics
through
PATHWAY
the immo bilized
eye and the st udy of eyemovement related activity via the moving eye.
During these experiments
the major emphasis
was placed on the study of eye-movement cells
in the deeper layers of the superior colliculus.
Two animals were studied.
RESULTS
Recording
in superior
colliculus
of
paralyzed
and anesthetized
animals
with unilateral
visual cortex ablation
One hundred
thirty-six
visually
responsive units were studied
in six animals.
Of
these, 30 were in the superior
colliculus
contralateral
to visual cortex ablation
and
106 in the ipsilateral
colliculus.
In two
additional
monkeys,
receptive-field
plots of
single or multiple
units at 75 sites were
made to study in detail
the topographic
representation
of the retina on the collicu-
LAYERS.
Receptive-field-properties. The following
aspects of receptivesize of
field orga nization
were
studied
organ izaactiva ting region, center-surround
tion, spatial summation,
and the temporal
response
characteristics
of units to onset
and offset of a stimulus.
Unilateral
ablation
of visual cortex had no discernible
effect
on the receptive-field
properties
of units
in the colliculus
contralateral
to the ablation.
Ipsilateral
to the ablation
the response
characteristics
of single
cells in
stratum griseum
superficiale
and the upper
region
of stratum
opticum
were affected
onlv to a small extent.
Figure 1 shows the responses to a flashing
spot of two units in the same monkey,
one
studied
in the colliculus
contralateral
and
the other ipsilateral
to cortical
ablation.
These histograms
show that as the size of
the stimulus
is increased,
first there is spatial summation
followed
by progressive
surround
inhibition.
The
responses
are
typical of normal
collicular
units, showing
a transient
burst to both onset and offset
of the stimulus.
The small differences
in
the temporal
distribution
of the responses
in the two sets of histograms
are within
the
range of variation
among normal
units.
While
the majority
of units studied
in
the superficial
colliculus
ipsilateral
to visual cortex
ablation
had
receptive-field
SUPERFICIAL
184
SCHILLER,
STRYKER,
CYNADER,
AND
INTACT
BERMAN
SIDE
80-
ON
OFF
1.6 sot
ABLATED
SIDE
80-
60-
20-
ON
OFF
response
histograms
obtained
from a superior
colliculus
unit contralateral
to the side of
visual cortex
ablation.
Stimulus
duration,
1 set repeated
every
2 sec. Bin width,
20 msec; 30 repeated
stimulus
presentations
per histogram.
Ordinate:
total number
of discharges
per bin. Onset and offset of
stimulus
occurs at the left edge of the letter 0. B: response histograms
obtained
from a superior
colliculus
unit on the side ipsilateral
to the visual
cortex
ablation.
Twenty
repeated
stimulus
presentations
per
histogram.
Other
parameters
as in A.
FIG.
1.
~4.’
properties
indistinguishable
from
those
found
in intact
animals,
some showed
subtle
differences
in their
receptive-field
organization
in that they no longer
gave
uniform
on-off bursts throughout
the receptive field. After the ablation
such visual
receptive
fields appeared
“patchier”:
some
regions
produced
strong off-responses
with
small or no on-bursts;
the reverse was true
for other regions.
When
a stimulus
producing
the most vigorous
response
was
placed in the center of the field this on-off
imbalance
was frequently
evident.
Such
receptive
fields did not, however,
show onoff center-surround
organization
of the sort
commonlv
seen in the retina. We have not
seen such patchy
receptive
fields in the
colliculus
of normal
animals.
Response
histograms
obtained
from
at
least 20 presentations
of an optimal
size
circular
spot centered
in the receptive
field
allowed
us to classify the units we studied
into
five categories:
those in which
the
number
of discharges
elicited
by the onset
and offset of the stimulus were equal within
50% (category
3); those in which
the onand off-responses
differed
by more
than
50(;?, (categories
2 and 4); and those where
only an on- or off-response
was obtained
(categories
1 and 5). Figure
2 compares
these distributions
for units
in superior
colliculi
with normal
and ablated overlying
visual cortices. Data from the intact side of
unilaterally
ablated
visual cortex
animals
were pooled with those from intact animals
studied
previous
to this report under identical conditions
(2). The
shift toward
a
greater on-off imbalance,
which
is evident
primarily
in the increase of the size of the
off-burst,
is statistically
significant
at the
CORTICOTECTAL
INTACT
SIDE
ABLATED
PATHWAY
SIDE
185
INTACT
SIDE
ABLATED
SIDE
IOO-
-
123
80
I-w
zI)
2
60
:
z
2
a
lz
W
0
60-
l-
40-
W
n
40
a
W
CL
lh
20-
19
16
I
I
2
3
ON-
OFF
RESPONSE
4
I_
.OO1 level (two-tailed
Kolmogorov-Smirnoff
test). The units which
showed
this effect
did not seem to have a clear-cut
distribution either in terms of the location
of the
receptive
fields or in terms of the depth
of recording.
Animals
studied
with different survival
times after visual cortex ablation did not show any notable
differences.
The
effects for all the variables
studied
appeared
to be similar
among
the six
monkeys.
Ocular
dominance.
A similarly
subtle
effect of visual cortex ablation
was observed
for ocular
dominance.
The
majority
of
units studied
both ipsilateral
and contralateral
to the ablation
were binocular
(94
and 99.5?& respectively).
A slight shift in
the ocular dominance
distribution
was observed on the ablated
side. This is shown
in Fig. 3, where data from the normal
side
were obtained
in part from previous experiments (2). The increase
in the spread in
ocular dominance,
though
small, is significant at the ,001 level (two-tailed
Kolmogorov-Smirnoff
test).
Fovea1 refwesentation.
Anatomical
studies have indicated
that retinal
projections
to the anterior
part of the superior
colliculus, which
represents
the central
5” of vision, are absent or very sparse in the mon-
2
3
5
6
7
OCULAR
5
FIG. 2.
Distribution
of units in the superior
colliculus on the side of an intact
and ablated
visual
cortex,
based on the total number
of discharges
to
the onset and to the offset of a disc of light in the
center of the receptive
field using 20 or more repeated
stimulus
presentations
per unit.
Abscissa:
1, on-response
only; 2, on-response
greater
than offresponse by more than 507&; 3, on- and off-responses
equal within
SO%, 4, off-response
greater
than onresponse
by more
than SOq’,; 5, off-response
only.
Number
of units shown above each bar.
4
I
DOMINANCE
3. Ocular
dominance
distributions
for units
in superior
colliculi
with
overlying
visual
cortex
intact or ablated.
Abscissa:
1, response from contralateral
eye only; 2, strong
contralateral
preference;
3, weak contralateral
preference;
4, equal responses
from
both eyes; 5, weak ipsilateral
preference;
6,
strong
ipsilateral
preference;
7, response
from ipsilateral eye only. Number
of units shown above each
bar.
FIG.
key (5, 9, 26). In two additional
animals
an
attempt
was made, therefore,
to determine
whether
cells in this area depend
solely on
the geniculostriate
pathway
for their visual
input.
If this were the case, cells in fovea1
colliculus
should be largely unresponsive
to
visual stimulation
following
ablation
of visual cortex.
Repeated
plotting
of the fovea with a
reversible
opthalmoscope,
even before and
after plotting
each receptive
field, is difficult to make sufficiently
reliable
for the
absolute determination
of receptive-field
locations with respect to the fovea. However,
the optical-lever
and reference-unit
techprovided
a reliable
niques
(see METHODS)
measure
of residual
eye movement,
thus
allowing
an accurate
determination
of receptive-field
locations
relative
to one another.
Since in the intact
monkev
there
appears to be no significant
overlap
in the
visual
hemifields
represented
in the two
colliculi
(2, 19, 20), the line separating
the
receptive-field
centers of units recorded
in
onecolliculus
from those of units recorded
in the other should
represent
the vertical
meridian.
Recordings
were made in both colliculi
of two animals
following
unilateral
ablation of visual cortex. In one animal, studied
223 days after the cortical
lesion, receptive
fields of 27 units
on the side ipsilateral
186
SCHILLER,
STRYKER,
to the lesion
and 21 units
contralateral
were plotted.
In the other animal,
studied
56 days after the cortical
lesion, 17 receptive fields were plotted
on the ipsilateral
side and 10 on the contralateral
side.
Figure
4 shows the receptive-field
plots
from these two animals,
corrected
for drifts
in eye position
as determined
by the opticallever and reference-units
methods.
Vertical
and horizontal
lines are drawn
through
the opthalmoscope
plots of the fovea. The
vertical
meridian
determined
in this way,
which
assumes negligible
torsional
deviation, agrees well with that determined
from
receptive-field
locations.
This
plot shows
that after ablation
of visual cortex, units
representing
the central
5” of the visual
field are still numerous
in the colliculus.
These
animals
were studied
a relatively
long time after visual cortex ablation.
How-
INTACT
SIDE
CYNADER,
AND
BERMAN
ever, the central 5” was clearly represented
in all eight of the monkeys
studied
after
visual cortex ablation.
Furthermore,
every
penetration
in this area yielded units with
brisk visual responses
confined
to normalsized receptive
fields. Therefore
this area
appears to receive essentially
normal
visual
input
even after removal
of visual cortex.
As will be seen, similar
results were also
obtained
with cooling.
DEEP
LAYERS.
The most dramatic
effect of
visual cortex ablation
became evident
only
below the superficial
layers of the superior
colliculus.
At some point
in the stratum
opticum,
it became impossible
to activate
units by visual stimulation.
The multipleunit response, which is so characteristic
in
much of the superior
colliculus
of the intact
animal,
disappeared.
Single units were still
ABLATED
SIDE
FIG. 4.
Receptive-field
locations
of ‘75 units
in the superior
colliculi
of two monkeys
with unilateral
visual cortex
ablation.
Receptive
fields drawn
with heavy lines are from units
obtained
contralateral
to
the side of the lesion;
receptive
fields drawn
with
thin lines are from
collicular
units ipsilateral
to the
side of the lesion. Discontinuous
lines represent
fields from one monkey;
continuous
lines are fields obtained
from
the other.
CORTICOTECTAL
found, and they fired spontaneously,
but
we could not drive them using any sort of
visual stimuli
we could invent. Stratum
opticum then is a transitional
zone in this
respect. Visual responses are still evident
in the dorsal region but not in the ventral.
In order to verify the depth at which
units could no longer be driven by visual
stimuli,
small electrolytic
lesions
were
placed at this point in two animals, studied
5 and 29 days after cortical ablation. Lesions were also placed in the colliculus
contralateral
to the ablation at the site
where responses to light could no longer be
elicited. An example of two such lesions is
shown in Fig. 5. Visual cortex was removed
over the superior
colliculus on the right
side. It can be seen that visual responses
were obtained quite deep on the intact
side; on the ablated side visual responses
could not be obtained below the upper part
of stratum opticum.
In addition to localizing the recording
sites by anatomical
methods, we also inspected the perfused brains of animals to
determine the extent of cortical ablation. It
appeared that virtually
all of area 17 was
removed in these animals with minimal
sparing in some cases in the deep concavity
of the calcarine fissure in the region which
falls anterior to a line in the coronal plane
FIG.
placed
above
187
PATHWAY
bisecting the lunate sulcus. Most of areas
18 and 19 were also ablated.
In two animals with long survival times,
retrograde cell changes were studied in the
lateral geniculate nucleus, sections of which
were stained by the Nissl method. The
nucleus showed nearly complete degeneration sparing only a small number of cells.
Most of the spared cells were in the medial
and lateral parts of the ventral region of
the geniculate.
One of the animals from which we recorded was sacrificed 6 days following
cortex ablation. Anterograde
degeneration was
studied by staining sections through
the
superior
colliculus
with the Fink-Heimer
method. This showed a dense degeneration
pattern similar to that reported by Kuypers
(8) and Wilson and Toyne (26), which was
heaviest in stratum opticum. Stratum griscum superficiale, by comparison,
showed
much lighter terminal degeneration.
Recording
paralyzed
reversible
in superior colliculus of
and anesthetized animals with
cooling of visual cortex
In three monkeys a total of 64 superior
colliculus cells were studied under conditions of cooling visual cortex. After locating units in that region of the superior
colliculus which represented the same area
5. Photomicrograph
of a section
through
the superior
colliculi
showing
the site of two
at the point
where visual responses
could no longer be elicited.
Left side is intact.
Visual
the superior
colliculus
on the right
was ablated
5 days prior
to the experiment.
lesions
cortex
188
SCHILLER,
STRYKER,
CYNADER,
of the visual field as the region
of cortex
which
was to be cooled,
units
were repeatedly
stimulated
with an optimal
stimulus display
while
cortex
was reversibly
cooled. Of these units 72% were within
5”
of the center
of the fovea. The
results
obtained
under
these conditions
complement those obtained
with cortical ablation.
The
superficial
layers were largely
unaffected by cooling, while in the deeper layers
units
stopped
responding
to light
when
cortex was cooled.
Figure
6 shows two units having
their
receptive
fields in the same area of the
visual
field. The
first unit
was obtained
near the surface of the colliculus,
220 p
below the first audible
signs of penetrating
this structure
with the microelectrode.
Cooliqg had no discernible
effect on the responses
of this unit.
The
second
cell,
encountered
400 p below
the surface,
stopped responding
to visual stimuli
when
cortex was cooled, and returned
to normal
responsivity
after cortex was warmed
again.
Only 1 of the 14 superficial
units studied
showed
a clear change during
cooling
to
the onset and offset of a flashing
spot in
the center of the field. This cell showed a
50%
decrement
in the number
of on-
ON
OFF
FIG. 7. Response
histograms
obtained
from a single
rewarming
of visual cortex.
Each histogram
represents
of the receptive
field. Onset and offset of the stimulus
AND
BERMAN
1
I
500mrec
s--j--+-
COOLED
-it-it-
CElKiG
ON
OFF
‘II
l
.
STIMULUS
FIG. 6. Response
characteristics
the superior
colliculus
before,
cooling
of visual
cortex.
A: unit
surface
of the colliculus.
The
sents shutter
voltage.
Stimulus:
tered in receptive
field. B: unit
surface
of the colliculus.
Lower
galvanometer
voltage.
Stimulus:
of two units
in
during,
and after
220 p below
the
lower
trace repreflashing
spot cen400 p below
the
trace
is mirror
sweeping
spot.
discharges
when cortex was cooled as compared with
the responses
obtained
before
and after cooling.
Of the 50 deeper units studied,
45 had
receptive
fields located in that area of the
visual field which was represented
by visual
cortex under
the cooling
probe.
The visually elicited responses of all of these units
were effectively
disrupted
during
cooling.
A more detailed
picture
of such a unit is
shown in Fig. 7. This cell was located 1 mm
I second
cell in the superior
colliculus
during
cooling
and
20 repeated
presentations
of .75O disc in the center
occur at the left edge of the letter 0.
CORTICOTECTAL
below the surface. This figure shows a series
of response
histograms
taken in periodic
samples during
cooling
and warming.
The
response
to both onset and offset of the
stimulus
declined
as cortex became cooler
until the unit was completely
unresponsive.
Responses
stopped
when
the temperature
of the cortex, as measured
by a thermistor
2 mm below
the surface
of the brain,
reached 17” and was held there. After cortex was warmed
this unit became slightly
hyperresponsive.
This was observed in some
units but not in others.
Two observations
indicate
that the effect
of cooling
on colliculus
units was exerted
through
local suppression
of the region
of
under
the
cortical
area 17 immediately
cooling
probe. First, the superficial
layers
of the colliculus,
which were closer to the
cortical area cooled, were largely unaffected
by cooling. This was true even at the end of
the one experiment
in which we accidently
cooled the cortex to 3 C causing irreversible
damage;
the superficial
unit recorded
did
not change
its characteristics,
while
the
visual response
of the deeper units disappeared
permanently.
Second,
the level of
cooling
required
to eliminate
the visual
response
of deeper
units
increased
with
increasing
distance
of the unit’s receptive
field from the area of the visual field represented
near the center
of the cooling
probe. Receptive
fields represented
near the
center of the cooling
probe
were readily
suppressed by cooling;
receptive
fields more
to be unaffected
than 7’ away appeared
by cooling
at the levels we employed.
One of the questions
these findings raise
is whether
or not a clear functional
distinction can be made between
the properties
of cells which
are and which
are not influenced by cooling.
While
the aim of this
study was not to answer this question
in
detail,
some qualitative
differences
were
noted. In general,
cells unaffected
by cooling had receptive-field
properties
previously
found to be associated with superficial
cells,
while those influenced
by cooling had properties associated with deep cells. Thus, the
superficial
cells, immune
to cooling,
tended
to produce
smaller
signals with
the same
electrode,
were more
difficult
to isolate,
had smaller receptive
fields, and responded
quite consistently
to repeated
stimulation.
PATHWAY
189
Bv con trast, the deeper
cells, whose responses were modified
by cooling,
were
easier to isolate, had larger receptive
fields,
and showed response variability
to repeated
stimulation.
The basic property
of giving
both on- and off-responses
was maintained
in both groups, as was the lack of specificity
for stimulus
shape or orientation.
In order
to determine
whether
or not
cooling
of visual cortex affects the contralateral
superior
colliculus,
in one monkey
two penetrations
were made in the right
colliculus
while
the cooling
plate was on
the left visual cortex. Five units were studied, three of which
had their
receptive
fields 3” from the center of the fovea on
the side contralateral
to the effective cooling area. None of these units was affected
by cooling.
Recording
in superior
colliculus
alert
animals
with unilateral
ablation
of visual
cortex
of
SUPERFICIAL
LAYERS.
Thirty-eight
visually
responsive
units were studied in the superficial layers of the superior
colliculus
of
two alert monkeys
on the side ipsilateral
to cortical
removal.
The
receptive-field
properties
of units, as studied
through
the
immobilized
eye of these animals,
were
similar
to those found in the acutely prepared monkeys.
Thus, the majority
of the
units in the alert animal also had properties
indistinguishable
from those seen in intact
monkeys
(2, 20). Ten
units
were found
which had an abnormal
patchiness
in their
receptive-field
organization,
giving unequal
on- and off-bursts
to a stimulus
flashed in
the center of the receptive
field. An example
of a unit discharging
more vigorously to off than to on is shown in Fig. 8.
The maintained
activity
of units in the
alert animals
was typically
higher
than in
the acute animals.
DEEP
LAYERS.
After the electrode
advanced
in the colliculus
ipsilateral
to the cortical
lesion
past some point
in the stratum
opticum,
many
units
were
encountered
which could not be driven reliably
by any
visual stimuli
we employed.
A few of these
units showed occasional
high-frequency
discharges
when
the monkev
was looking
around,
but they did not seem to have vi-
190
SCHILLER,
STRYKER,
CYNADER,
AND
BERMAN
60-
2
OFF
ON
FIG. 8. Response
histogram
obtained
from
a single
unit in the superficial
alert monkey.
Thirty
repeated
presentations
of a .750 spot in the center of the
offset of stimulus
occur at the left edge of the letter
0.
sual receptive
fields although
they did show
less activity in the dark. Others maintained
a variable
activity
but did not appear
to
be influenced
by eye movements
in light
or in darkness
or by any form of visual
stimulation.
Slightly
deeper, eye-movement
cells similar to those described
previously
were encountered
(20). Thirty-four
eye-movement
cells were studied;
of these twenty-seven
were ipsilateral
and seven contralateral
to
the side of visual cortex ablation.
On the
side contralateral
to the lesion thev were
indistinguishable
from eye-movement
cells
seen in intact
animals.
On the ipsilateral
side the activity of such cells prior to eye
movement
also appeared
normal.
This is
shown in Fig. 9. Stimulation
through
the
microelectrode
produced
saccades at similar current
levels to those required
to
elicit eye movements
in intact animals (2 l),
and these elicited
saccades duplicated
the
I
superior
receptive
set
colliculus
of an
field. Onset and
characteristics
of the spontaneous
saccades
specifically
associated
with unit discharge.
The motor fields of eye-movement
units
(20, 21, 27) on the ablated
side were also
normal,
as shown in Fig. 10.
Following
the cortical
lesion,
however,
one clear difference
in the eye-movement
units was found:
they lacked visual receptive fields. In the intact
animal,
we have
previously
distinguished
two types of eyemovement
cells: the more superficially
located ones, which have practically
no spontaneous activity, a high percentage
of which
have visual receptive
fields; and the deeper
high
maintained
units,
with
relatively
activity,
which
do not appear
to have
visual receptive
fields (21). Of the 27 eyemovement
units recorded
ipsilateral
to the
cortical
lesion, 21 were of the first, more
superficial
type with low spontaneous
activity, the majority
of which could be expected in the normal
animal
to have visual
RECORDING
AND
STIMULATION,
ABLATED
RECORDING
AND
STIMULATION,
INTACT
SIDE
SIDE
I
500msec
FIG. 9. Recording
and stimulation
in the deeper layers of the superior
colliculus.
Responses
of two eyemovement
cells from the same animal
are shown,
one ipsilateral
and the other
contralateral
to the side
of visual cortex
ablation.
The first two columns
show saccade-associated
unit activity.
The third
column
shows saccades elicited
by stimulation
through
the microelectrode
immediately
following
recording:
70msec train of 5 pa, .5-msec pulses at 300 Hz.
CORTICOTECTAL
FIG.
10.
Motor
field of an eye-movement
unit in
the superior
colliculus
of an alert monkey
ipsilateral
to the side of the lesion. This plot depicts
the size
and direction
of saccades associated
with
unit firing. Open
circles
show saccades
without
accompanying
unit discharge;
filled circles represent
saccades which were preceded
by unit activity.
receptive
fields. Only 1 of these 21 units
had a visual receptive
field.
These findings
suggest that the ablation
of visual cortex results in the virtual
elimination
of visual input to the deeper layers
of the superior
colliculus,
including
the
eye-movement
cells.
DISCUSSION
The results of this study show that ablation or cooling of visual cortex disrupts
the
transmission
of visual information
to the
deeper
layers of the superior
colliculus.
The major findings
in the colliculus
lacking visual cortex input
are three:
1) the
entire
visual
half-field
is represented
on
the surface of the colliculus,
despite
anatomical
claims
of the absence of retinal
to the perifoveal
representaprojections
tion; 2) visual responsiveness
disappears
in
units located
below
the superficial
layers
of the colliculus;
and ?) eye-movement
units
in the deeper layers of the colliculus
still
discharge
before particular
eye movements,
but they no longer
have visual receptive
fields.
These results lend themselves to an interesting comparison
with three other species
studied in this manner:
the cat, the ground
squirrel,
and the rabbit.
In the rabbit,
vi-
PATHWAY
sual cortex does not appear to play a role
in determining
the receptive-field
properties of collicular
cells (10). In the cat, collicular
receptive
fields are similar
to those
of the monkey
in many respects; most cells
in the intact
animal
are binocular,
show
little or no shape specificity,
and respond
transiently
to both onset and offset of a
visual
stimulus.
The major
difference
is
that in the cat the majority
of the units
(7073 are direction
selective (1, 23). After
cortical
cooling
or ablation,
they are no
longer directional
or binocular
(1, 18, 25).
0 ther aspects of receptive-field
organization in the superficial
layers are largely
unaffected.
A recent
study by Stein and
Arigbede
(22) indicates
that in the deeper
layers, as in the monkey,
cooling
of visual
cortex renders
single cells unresponsive
to
visual
stimuli.
Studies
on the ground
squirrel
yield a
rather
different
result
(14). This
animal
has an all-cone
retina
with
crossed optic
nerves. The superior
colliculus
has units in
the upper layers which are direction
selective and show little shape specificity.
The
deeper
layers are reported
to have a predominance
of hypercomplex
cells. Ablation
or cooling
of visual cortex does not affect
the superficial
cells; direction
selectivity
is
still present, presumably
obtained
from the
direction-selective
retinal
ganglion
cells.
The
deeper
layers, however,
are affected
dramatically;
cells can no longer be driven
by visual
stimuli,
although
they retain
spontaneous
activity.
The attribute
of directionality
in the cat
is cortically
mediated,
while in the ground
squirrel,
as in many other rodents,
it is
already present in the retina.
Binocularity
in the cat superior
colliculus
appears to be
mediated
by visual
cortex,
while
in the
monkey
it seems to have emerged
without
much reliance
on connections
from visual
cortex. These findings are in harmony
with
the anatomy
of this system. In the cat the
retinal
projection
to the superior
colliculus
is primarily
contralateral,
while in the monkey the eye projects
equally to both colliculi. In the deeper layers, disruption
of the
corticotectal
input
from visual cortex has
similar
effects in the cat, ground
squirrel,
and monkey.
Of the animals
studied,
the
rabbit
appears to be the only exception.
192
SCHILLER,
STRYKER,
The comparison
among different
species
must largely
be restricted
to the sensory
since
aspect of the superior
colliculus,
those properties
which are related to motor
output
have not been extensively
studied.
Single-unit
activity
related
to eye movement
has been found
in both
cat and
monkey
(20, 21, 24, 27), but it is only in
the latter species that a clear relationship
has been shown
to exist between
the sensory and motor maps of this structure
(19,
21, 27). The fact that the eye-movement
responses
of cells in the deeper
layers of
the monkey
superior
colliculus
are still
present
after ablation
of visual
cortex is
consistent
with the observation
that some
of these cells respond before eye movement
in the dark and with calorically
induced
vestibular
nystagmus
(21). Since the response characteristics
of these cells depend
only in part on visual
input,
they must
receive
extensive
projections
from other,
nonvisual
structures
involved
in the control
of eye movement.
When our results are compared
with the
recent anatomical
studies on the nature of
cortical
and retinal
input
to the superior
colliculus,
an
apparent
contradiction
emerges.
The
anatomical
studies
have
shown that in the monkev
the retina does
not project
to the anterior
portion
of the
colliculus
or does so only very sparsely
(5, 9, 26). By contrast,
fibers from visual
cortex
project
to the entire
colliculus,
showing
especially
dense termination
in
the anterior
region.
Our results do not fit
these findings;
after ablation
of visual cortex, units having
receptive
fields in the
fovea1 area are still
plentiful
and have
properties
similar
to units with receptive
fields further
out in the visual field.
Several possibilities
may be considered
in dealing
with this contradiction.
One is
that our recordings
are in error. We doubt
this, for care was taken in our work not
only to verify the fovea1 area and to monitor residual
eye movements,
but also to
obtain
a sufficient
sample in our mapping
procedures
so that a large portion
of the
visual
field
was covered
with
receptive
fields, counteracting
the possible
effect of
any error in plotting
the fovea.
A second possibility,
anatomical
reorganization
following
the cortical
ablation,
seems also unlikely
to account for our find-
CYNADER,
AND
BERMAN
ing collicular
receptive
fields representing
the central retina, since cooling
the cortex
left the superficial
cells within
the central
5” of the visual field unaffected.
A further
possibility
is that the anatomical methods
have not to date been sufficiently sensitive
to detect retinal
terminals
in the anterior
part of the colliculus
representing
central vision, or that the survival times used have been wrong
for this
area. Whether
or not this is so remains
to
be seen.
A final possibility
is that the fovea1 area
in the colliculus
is innervated
not directly
from the retina but from a structure
other
than visual cortex; it is this other structure,
perhaps
the lateral
geniculate
nucleus,
which
receives the visual input
and then
relays it to the colliculus.
While
this alternative
cannot be ruled out, it does not
seem very likely to us. Were it so, our recordings
should
probably
have reflected
some inherent
differences
in the central
and more peripheral
representations
of the
visual field in the colliculus.
We have not
seen this. The onlv clear difference
between
central
and peripheral
representations
is
receptive-field
size. Furthermore,
any candidate
for such a structure
should
itself
have a binocular
projection
from the retina, since the fovea1 representation
is no
less binocular
following
the cortical
lesion
than are the more peripheral
representations in the colliculus.
Most of the known
sites of retinal
terminations
in the monkev
other
than the lateral
geniculate
nucleus
and the superior
colliculus
are chiefly contralateral
(5).
Although
the cooling c and ablation
methods in these studies demonstrate
the dependence
of collicular
function
on visual
cortex,
they provide
only margina .l cues
about the exact nature
of the cortical
information
which
reaches the colliculi.
In
the monkey
one may consider
several possibilities.
One is that the visual receptivefield properties
of deeper
collicular
cells
are determined
by visual
cortex.
This
would
seem to necessitate
a great deal of
convergence
from the cortex so that several
cells with preferences
for different
orientations would
impinge
on a single collicular
cell; in this way the lack of orientation
specificity
could come about. Recent work
suggests that in the cat there is indeed
a
CORTICOTECTAL
great deal of corticocollicular
convergence
(11, 12). The
equivalence
of on-off responses and binocularity
would
also be
produced
by cortical
convergence,
since in
the monkev most cortical cells do not seem
to produce
equivalent
on-off responses
to
flashes and only 50y0 of them are binocular
one could
assume
(6, 7, 17). Conversely,
that there
is a population
of binocular
cortical cells which have properties
similar
to those observed in the colliculus.
A recent
(17) suggests that in the
study by Poggio
monkey area 17 there may be a higher
proportion
of nonoriented
cells than has previously been reported.
Recent work on the cat has attempted
to
identify,
by antidromic
activation,
those
cortical
cells that send their axons to the
colliculus.
These experiments
have shown
that most such cells fall into the category
of complex
neurons
(15, 16) which
have
orientation
and direction
specificity.
Unfortunately
none of these considerations can answer how the superficial
cells
in the colliculus
might
influence
the cells
in the deeper layers under
normal
conditions.
Perhaps
one should
consider
the
possibility
that cortex modulates
the flow
of visual information
from the superficial
down to the deeper layers. Such a hypothesis might
not necessitate
a multiple
convergence notion,
since in this case the properties of the deeper cells may be assumed
to be derived from the superficial
cells.
PATHWAY
part of the stratum
and in the dorsal
opticum
are largely unaffected
by ablation
of visual cortex. Some cells do not, however,
respond
to visual stimuli
throughout
their
receptive
fields as uniformly
as do collicular
cells in the intact
animal.
Most cells are
still binocular
but the ocular
dominance
distribution
is slightly
broader.
3. In the deeper layers of the superior
colliculus
visual
responses
can no longer
be elicited from single cells after visual cortex ablation.
with
these findings,
4. In agreement
cooling
of visual
cortex
has little
or no
effect on the cells in the superficial
layers
of the superior
colliculus
but disrupts
visual responses below this region.
5. The central 5” of the visual field continues to be represented
on the surface of
the colliculus
following
either ablation
or
cooling
of visual cortex, despite anatomical
evidence for the virtual
absence of a fovea1
retinotectal
projection.
6. Eye-movement
cells in the deeper layers of the superior
colliculus
of the alert
monkey
are still present
after ablation
of
visual cortex but they no longer have visual
receptive
fields.
7. The results suggest that visual cortex
plays a prominent
role in controlling
the
flow of information
to the deeper layers of
the
superior
colliculus
of the
rhesus
monkey.
,\CKNOWLEDGMENTS
SUMMARY
1. This study investigated
the influence
of corticotectal
connections
by studying
the
response characteristics
of single cells in the
superior
colliculus
of the monkey
during
cooling or after ablation
of visual cortex.
2. The receptive-field
properties
of single cells in the stratum griseum
superficiale
We thank
Ms. Susan Volman
and Ms. Cynthia
Richmond
for their
assistance.
This research
was in part supported
by National
Institutes
of Health
Grants
EY00676
and EY00’756,
a Sloan Foundation
Grant,
and Public
Health
Services Training
Grant GM01064.
Present
address of M. CY nader:
Dept. of Psvchology, Dalhousie
Universi tYy Halifax,
Nova
Scotia.
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