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 Previous Article
The Journal of Neuroscience, December 1, 1998, 18(23):10219-10229
An Anatomical Substrate for the Spatiotemporal Transformation
A. K.
Moschovakis2,
T.
Kitama1,
Y.
Dalezios2,
J.
Petit1,
A. M.
Brandi1, and
A. A.
Grantyn1
1 Laboratoire de Physiologie de la Perception et de
l'Action, Centre National de la Recherche Scientifique-College de
France, 75005 Paris, France and 2 Division of Computational
Neurosciences, Institute of Applied and Computational Mathematics,
Foundation for Research and Technology-Hellas, and Department
of Basic Sciences, Faculty of Medicine, University of Crete, GR-7110
Iraklion, Greece
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ABSTRACT |
The purpose of the present experiments was to test the hypothesis
that the metrics of saccades caused by the activation of distinct
collicular sites depend on the strength of their projections onto the
burst generators. This study of morphofunctional correlations was
limited to the horizontal components of saccades. We evoked saccades by
stimulation of the deeper layers of the superior colliculus (SC) in
alert, head-fixed cats. We used standard stimulus trains of 350 msec
duration, 200 Hz pulse rate, and intensity set at two times saccade
threshold in all experiments. Evoked saccades were analyzed
quantitatively to determine the amplitude of the horizontal component
of their "characteristic vectors". This parameter is independent of
eye position and was used as the physiological, saccade-related metric
of the stimulation sites. Anatomical connections arising from these
sites were visualized after anterograde transport of biocytin injected
through a micropipette adjoining the stimulation electrode. The
stimulation and injection sites were, therefore, practically identical.
We counted boutons deployed in regions of the paramedian pontine
reticular formation reported to contain long-lead and medium-lead burst
neurons of the horizontal burst generator. Regression analysis of the
normalized bouton counts revealed a significant positive correlation
with the size of the horizontal component of the characteristic
vectors. This data supports a frequent modelling assumption that the
spatiotemporal transformation in the saccadic system relies on the
graded strength of anatomical projections of distinct SC sites onto the
burst generators.
Key words:
saccades; superior colliculus; burst generator; oculomotor system; orienting behavior; biocytin
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INTRODUCTION |
The neural system that controls
saccades is one of the best understood complex systems in the mammalian
brain. Its principal cell classes have been described in terms of
movement-related discharge patterns, topography, and connections (for
review, see Moschovakis et al., 1996 ). As with other motor systems, it
is characterized by transformations of signals as they pass from higher
order supranuclear structures to motoneurons. One such transformation
is called "spatiotemporal" because it links portions of the
saccadic system that use a space code to those that use a temporal code
to specify the same movement parameters. The saccadic burst generators
are typical of structures that use a temporal code to specify movement
amplitude. The size of the horizontal component of saccades is encoded
by long-lead (LLB) and medium-lead (MLB) burst neurons of the
paramedian pontine reticular formation (PPRF). Other LLB and MLB
neurons located in the rostral mesencephalon encode the size of the
vertical component of saccades. The saccadic burst generators receive
their main input from the superior colliculus (SC). This structure uses
a place code to specify the amplitude and direction of saccades in that
it contains cells that emit high frequency bursts before saccades of
particular direction and amplitude (Wurtz and Goldberg, 1972; Sparks
and Mays, 1980). Cells of the rostral SC discharge optimally for
saccades having small horizontal components, whereas cells of the
caudal SC prefer saccades with large horizontal components.
Early models of the spatiotemporal transformation assumed that the
spatial concentration of cells projecting to the vertical and
horizontal burst generators of the saccadic system varies systematically within the collicular map (McIlwain, 1982). In their
pioneering effort to test this hypothesis, Edwards and Henkel (1978)
described a rostrocaudal gradient of the number of tectal neurons
projecting to the region of the abducens nucleus. According to this
study, such tectoreticular cells become increasingly more numerous at
successively more caudal levels of the feline SC (Edwards and Henkel,
1978). Compared to a rostral SC site, the excitation of a caudal SC
site should then engage a larger number of SC neurons projecting to the
horizontal saccade generator in the PPRF, and such a gradient would
account for the spatiotemporal transformation in the horizontal plane.
However, several studies failed to confirm the observations of Edwards
and Henkel (Kawamura and Hashikawa, 1978; Stanton and Greene, 1981;
Olivier et al., 1991). Alternatively, the spatiotemporal transformation
could be based on the number of terminals that tectal efferent fibers
deploy within the confines of regions housing the horizontal burst
generator (Keller, 1980; Scudder, 1988; Moschovakis, 1994). To test
this hypothesis, we combined a quantitative study of the anatomical
projections to the PPRF, as revealed by circumscribed tracer injections
into the SC, with a quantitative study of the metrics of saccades
evoked by the electrical stimulation of the injection sites.
Parts of this paper have been presented in abstract form (Grantyn et
al., 1997).
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MATERIALS AND METHODS |
Experiments were performed on six adult cats weighing 3-4 kg.
They were surgically prepared under pentobarbital anesthesia (30 mg/kg,
i.p.) and sterile conditions. A search coil consisting of three loops
of teflon-insulated stainless steel wire was wound under the insertions
of the extraocular muscles. Stainless steel bolts were cemented onto
the occipital and temporal bones for painless head fixation. After
craniotomy, the dura mater was excised, and a cylindrical plastic
chamber was placed over the cortical surface and cemented to the bone.
The position of the chamber was determined stereotaxically so that
vertically or obliquely oriented electrodes would have access to the
superior colliculus. To prevent postoperative infections animals
received intramuscular injections of a long-acting antibiotic
(Extencilline). Four to seven days of postoperative recovery were
allowed before starting the experiments. The animals were placed in a
body-restraining cloth bag in front of a featureless screen, in a dimly
illuminated room. Their heads were fixed to a stereotaxic frame by
means of the implanted bolts. Drowsiness was prevented by alerting
stimuli (noises, spots of light, morsels of food) presented at
irregular intervals. To record the instantaneous horizontal and
vertical position of the animals' eyes, their heads were centered
within two magnetic fields with orthogonal directions and phase. The current induced in the eye coil was demodulated to obtain the vertical
and horizontal components of instantaneous eye position with a
resolution of 0.1°. Eye position was sampled at a rate of 500 Hz with
a microcomputer running Spike2 software (Cambridge Electronics Design)
and stored on disk for off-line analysis.
A double barrel micropipette assembly was lowered in the brain and
advanced to the SC. The assembly was constructed by fixing together a
graduated microsampling pipette [1-5 µl, 1.0 mm outer diameter
(o.d.); Corning, Corning, NY; catalog #7099U] and a glass tube
(1.5 mm o.d.) containing a tungsten wire. The tubes were heated inside
the spiral of a vertical puller, twisted, and pulled to produce a
double electrode with long taper. The glass was then broken off to
obtain an injection channel with a diameter of 10-20 µm. The excess
length of the tungsten wire was reduced by electrolysis to a sharp tip
of 80-100 µm in length, and the base of the tip was aligned with the
orifice of the injection channel. The major diameter of the double
pipette at the tip was ~80 µm. Recording multiunit activity through
the tungsten electrode allowed the detection of the collicular surface
and a crude judgment of the directional tuning of visually responsive
cells in the superficial tectal layers. When visual activity became
weak, the tungsten electrode was switched from recording to stimulation
to evoke saccades and to determine the depth of minimal threshold. We
defined the threshold as the current intensity needed to evoke a
saccade in about half of the trials. Electrical stimuli were delivered in trains of 70 cathodal pulses, 0.4 msec in duration, and at an
interval of 5 msec. These parameters were chosen from the literature (Guitton et al., 1980; Paré et al., 1994; Grantyn et al., 1996) to ensure that the amplitude of saccades evoked from each site would be
maximal. Individual pulses were recorded as events with a time
resolution of 10 µsec and stored on disk for later analysis.
Because the amplitude of saccades electrically evoked from the SC has
been shown to increase somewhat with stimulus intensity (Straschill and
Rieger, 1973; Stein et al., 1976; Grantyn et al., 1996), we defined
their size at current intensities equal to 2 × T (20-50 µA).
The metrics of evoked saccades are also known to depend on the position
of the eyes at the time of saccade onset (Straschill and Rieger, 1973;
McIlwain, 1986, 1990; Grantyn et al., 1996). Therefore, even with the
use of standard stimuli of equal relative intensities, the
site-specific saccade metrics cannot be obtained by a simple averaging
across a number of evoked saccades. To eliminate the effect of eye
position, we used the method proposed by McIlwain (1986, 1988), which
is based on the evaluation of the linear regression of horizontal
(vertical) saccadic components,  H (V), versus the initial
horizontal (H1) or vertical (V1)
eye position. These expressions are of the form:
Figure 1 provides an example from
one of the animals of the present study (NB3). The slopes,
aH and aV, of these regression lines
provide a measure of the position sensitivity of saccades. The
constants  H (13.5°) and V (5.6°)
indicate the amount of eye displacement (horizontal and vertical) that
would be obtained had the eyes started from primary position
(H1 = 0 and V1 = 0). The vector that
corresponds to these values (13.5, 5.6°) is defined as the
"characteristic" vector of the saccades evoked from the collicular
microzone that was electrically activated in animal NB3.
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Figure 1.
Plots of horizontal (H) and vertical (V)
size of saccades (ordinate) elicited in response to the
electrical stimulation (2 × T, 70 pulses) of the superior
colliculus versus initial horizontal (H1) and
vertical (V1) eye position
(abscissa). Solid lines are the linear
regression lines through the data (open circles,
vertical; solid circles, horizontal) and obey the
expressions displayed. The "characteristic vector" can be read off
the points at which the linear regression lines intersect the
vertical dashed line through zero initial eye
position.
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After collecting a sample of eye movement data, 0.8 µl of biocytin
(N-biotinyl-L-lysine; Sigma, St. Louis, MO; 5%
solution in 100 mM Tris buffer, pH 7.4) was pressure
injected in the SC through the second graduated barrel of the
micropipette assembly. The injection of the solution was made slowly,
over at least 30 min, and the array was left in place for another 15 min before it was slowly retracted. Animals were allowed to survive for
60 hr after the biocytin injections. They were then deeply anesthetized with pentobarbital (60 mg/kg, i.p.), heparinized (5000 U, i.v.) through
the femoral vein, and perfused transcardially with 1 l of
PBS, pH 7.4, followed by 2 l of 4% paraformaldehyde
dissolved in 100 mM phosphate buffer. The brain was
removed, blocked in the plane of the electrode tracks, and stored in a
20% solution of sucrose in phosphate buffer. After equilibration, 75 µm serial frontal sections were cut on a freezing microtome and
reacted according to a modified version of the procedure used by
Horikawa and Armstrong (1988). Briefly, sections were rinsed four times (20 min each) in a solution of PBS containing 0.1% Triton X-100. Then,
they were incubated overnight at room temperature in a 1:200 solution
of avidin-biotin-peroxidase complex (ABC kit; Vector Laboratories,
Burlingame, CA) in PBS containing 0.1% Triton X-100. They were then
rinsed three times (10 min each) in 0.05 M Tris buffer, pH
7.4. The presence of bound HRP was revealed using a modified version of
the heavy metal intensification of the DAB (3'-3'-diaminobenzidine)
reaction product (Adams, 1981). Briefly, sections were preincubated for
5-10 min in a 0.2% solution of nickel ammonium sulfate in Tris
buffer, and then placed in a solution of Tris buffer containing 0.05%
(w/v) DAB and 0.2% (w/v) nickel ammonium sulfate for 10 min.
H2O2 was added to this solution to a final
concentration of 0.006% (v/v), and the sections were incubated for an
additional 5-20 min at room temperature. Reacted sections were rinsed
three times in Tris buffer (10 min each), mounted on
chromalum-gelatin-coated slides, and left overnight to dry. They were
then cleared, lightly counterstained, dehydrated in a graded series of
alcohols, and coverslipped.
The evaluation of morphological data was done with the help of a Zeiss
Axioskope equipped with a drawing tube facing a monitor screen. The
optical encoders of the microscope stage were connected to a Compaq 486 computer running reconstruction software (Neurolucida; MicroBrightField, Colchester, VT). The tracing of outer contours of the
sections and of the outlines of selected nuclei was done using a 2.5×
objective. The positions of retrogradely labeled cells and projection
axons were entered at a higher magnification (200×). Subsequently,
entire sections were systematically scanned to detect and plot the
location of boutons. The scanning was done with a 40× objective. A
60× oil immersion objective was used to identify weakly stained
boutons. The superimposition of sections and bouton counts within
specified regions of the sections were obtained with the Neurolucida software.
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RESULTS |
Figure
2A-F
illustrates the position of the stimulation-injection sites
with respect to the outlines of the SC in the horizontal plane. The
stimulated sites are distributed over a considerable portion of the
mediolateral and anteroposterior extent of the SC. Their positions can
be placed on the coordinates of the standard motor map of the feline SC
(McIlwain, 1986) after replotting them on the normalized outlines of
the SC (Fig. 2G) as described before (Grantyn et al., 1996).
As shown in Figure 2G, the anatomical locations of the
stimulation-injection sites correspond to saccade vectors with
horizontal components ranging between 0 and 20°, and vertical
components ranging between -16 (down) and +5° (up). The
characteristic vectors of saccades evoked with standard stimulus parameters (see Materials and Methods) are shown in Figure
2H. Their horizontal components ranged from 2.1 to
13.5°, and their vertical components from -13.7 to +9.2°. A
comparison of Figure 2, G and H, indicates only a
rough correspondence between vectors effectively induced by electrical
stimulation and those predicted from the anatomical locations of the
stimulation sites. Such discrepancies can be partly attributed to
uncertainties inherent in matching individual outlines of the SC to any
standard map of the structure. Also, the SC may be anatomically
heterogeneous because of local, small scale variations in the
proportion of neurons representing different saccade vectors (Grantyn
et al., 1996). Accordingly, we decided to study the strength of
projections from labeled SC sites not in relation to the anatomically
predicted, but in relation to the experimentally determined, horizontal
components of saccades.
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Figure 2.
A-F, Horizontal
plots of the outlines of the superior colliculi to illustrate the
locations of stimulation and injection sites (large
crosses) in different animals. Dots show the
distributions of biocytin-labeled cells inside the SC. #
Cells, Number of labeled cells recovered in the SC; #
Fibers, number of labeled fibers counted at their entry in the
pons; C, caudal; L, lateral;
M, medial; R, rostral. G,
Stimulation-injection sites in different animals superimposed on a
retinotopic map of the SC (McIlwain, 1986) embedded within the
normalized outlines of each animal's SC. Orientation
arrows apply to A-G.
H, Two-dimensional plot of the characteristic vectors
(abscissa, vertical; ordinate,
horizontal) of saccades evoked from corresponding
collicular sites.
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Photomicrographs in Figure 3,
A and B, illustrate the spread of the tracer in
experiments NB3 and NB4, respectively. Figure 4 illustrates the tracer spread around
all injection sites reconstructed from serial sections. They represent
the maximum extension of the passive diffusion as determined at the
level of the injection center and within ± 0.5 mm rostral and
caudal to it. The subjectively defined intensity of local tissue
labeling is shown by different shading. Completely opaque zones
adjacent to the tracks were judged to be "strongly" labeled.
"Moderate" label corresponded to zones of considerable diffuse
staining that, however, allowed recognition of neuropil details. The
largest, "weakly" labeled zones were delimited based on the
presence of detectable diffuse staining in between the fibers and cells
containing the tracer injected. Within the intermediate gray layer
(SGI) the diameters of weakly labeled zones measured 0.8-1.3 mm. This
provides a rough estimate of the passive tracer diffusion and of the
limits of SC regions in which neuronal uptake of biocytin could
occur.
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Figure 3.
Photomicrographic illustration of the injection
sites in NB3 (A) and NB4
(B) and terminal arborizations in the PPRF of NB3
(C). Scale bars: A,
B, 1.25 mm; C, 50 µm.
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Figure 4.
Camera lucida reconstructions of the
stimulation-injection sites in the superior colliculus in the frontal
plane. Different degrees of shading correspond to areas of intense
(black), moderate (hatched), and weak
(stippled) tracer deposition. Drawings show maximal
extent of these areas, as seen in several (5-8) 75-µm-thick sections
centered on the electrode tracks. Note that in cases NB12 and NB14 the
ventrolateral extensions of the weakly stained regions correspond to
labeled fibers coursing in the intermediate white layer. These
extensions were not included in the measurements of the size of
diffusely labeled zones. MG, Medial geniculate;
NTO, nucleus of the optic tract; NPP,
posterior pretectal area; SGI, stratum griseum
intermedium; SGP, stratum griseum profundum;
SO, stratum opticum; PAG, periaqueductal
gray matter.
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In all experiments, the tips of the stimulation-injection arrays were
located in the SGI. Their positions were distributed between the upper
third (NB4, NB13) and the lower border (NB12, NB14) of the SGI (Fig.
4), despite the fact that we used the minimal saccade threshold to
guide electrode positioning. However, the zones of passive tracer
diffusion occupied the whole depth of the SGI, except for NB4 in which
the lowermost edge of the layer was spared. The involvement of the
optic layer (SO) was minimal in experiments NB12 and NB14. In the
remaining experiments, tracer diffusion involved the SO throughout its
depth. Involvement of the deep gray layer (SGP) was negligible in NB2
and NB12 and absent in the remaining four cases (Fig. 4).
Biocytin injections led to extensive labeling of cells and fibers
inside the SC. Labeled cells were found in the SGI, to a lesser extent
in the superficial gray layer and the SO, and occasionally in the SGP.
Their number varied considerably between experiments, from 91 (NB12) to
427 (NB4). The clouds of labeled cells around the tracks are shown in
Figure 2 (A-F), projected on the
horizontal plane. In some cases the center of the clouds more or less
coincided with the electrode tracks, but often they did not. The
majority of labeled cells were found within ~1 mm from the injection
sites. However, many remote cells were recovered as well, at distances varying between 1.4 (NB4) and 3.9 mm (NB2). Whereas cells neighboring the tracks may have taken up the tracer directly, through their somata
or dendrites, distant cells must have been labeled retrogradely through
axons damaged or interrupted by the passage of the electrode arrays. In
accordance with this, we observed numerous intratectal fibers coursing
in longitudinal, tangential, and oblique directions at all levels of
the SC and predominantly in the SO and the SGI (Fig.
5). Because of retrograde labeling, the
number and topography of cells recovered in the SC does not provide a
reliable estimate of the efficacy of local biocytin uptake or of the
number and position of labeled cells projecting to the burst
generators. Accordingly, we did not pursue a more detailed analysis of
the retrogradely labeled cells we recovered.
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Figure 5.
Distribution of labeled axons in the SC after
medial (A, NB3) or lateral (B, NB4)
injections of biocytin. Superpositions of camera lucida tracings from
five adjacent frontal sections at the level of the center of injection
sites. Only axonal segments visible at low magnification (40×) have
been included. Thick arrows delimit the zone occupied by
radial axons passing through the deep gray layer before joining the
tectobulbospinal tract. Concentric contours correspond, from inward to
outward, to dense, moderate, and weak diffuse staining around the
injection tracks (compare with Fig. 4). Numbers
(2-7) indicate layers of the SC
(superficial gray, optic, intermediate gray, intermediate white, deep
gray, and deep white, respectively). Aq, Aqueduct;
CG, central gray.
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Two streams of labeled projection fibers could be clearly recognized in
the vicinity of tracer deposits (Fig. 5). The first one consisted of
radially oriented fibers that converged on the dorsolateral border of
the central gray, where they entered the deep white layer and coursed
toward the dorsal tegmental decussation. Inside the SC, their
continuity with stained cells in the vicinity of the injection sites
was often obvious without serial reconstructions. As measured in
frontal sections, the size of the zones occupied by radial fibers
traversing the intermediate white layer and the SGP varied from 1.0 to
1.6 mm. These zones were somewhat larger than the extent of passive
tracer diffusion estimated from the diffuse staining of tissue (Fig.
5). This provides a second estimate of the size of collicular regions
containing labeled cells of origin of the crossed tectoreticulospinal
tract. The second stream was composed of tangential fibers coursing
laterally through the intermediate white layer and, to a lesser extent,
the deep gray layer. After leaving the SC at its ventrolateral border,
the second stream of fibers followed the trajectory of the ipsilateral
tectopontine tract through paralemniscal tegmental regions.
The PPRF is supplied by the first, crossed contingent of tectal
efferent fibers. Their number was counted at their entry in the pons,
1.0-1.3 mm posterior to the trochlear nucleus, to evaluate the
efficacy of biocytin uptake and transport specifically by fibers of
this contingent. The brainstem level at which fibers were counted is
illustrated in the low-power drawings of Figure 6. All predorsal bundle (PDB) fibers
containing biocytin reaction product have been included, disregarding
variations of staining intensity. Two examples of their distribution in
the PDB are shown in Figure 6, A1 and
B1, together with some more intensely stained
collaterals visible in the same sections. In four experiments (NB3,
NB4, NB12, and NB2), the number of stained PDB fibers did not differ
excessively (107, 162, 169, and 170, respectively). As expected, this
number was not related to the number of labeled cells in the SC. For
example, the smallest (107) and the largest (170) number of axons we
observed in these four experiments corresponded to 374 and 354 tectal
cells, respectively. In two other experiments, we observed strong
departures from this range. We found only 48 axons in experiment NB13.
There were no signs of reduced tracer diffusion or uptake in this
animal, as judged from the size of the tracer deposit and the number of
stained collicular cells. The slightly more superficial location of the injection center in NB13 (Fig. 4) cannot explain the small number of
fibers we found in the pons of this animal, because a much larger
number of fibers (162) was found after a comparable injection (NB4,
Fig. 4). Also, as in other experiments, fibers traversing the pons in
NB13 could be followed to the bulbospinal junction. This makes unlikely
an abnormally rapid fading of label with distance from the SC in NB13.
Case NB14 had 454 labeled axons, thus offering the opposite extreme. In
this case, the tracer deposit spread to the intermediate white layer.
However, this cannot be the reason for the excessive number of PDB
fibers we found in this animal. The injection sites of NB2 and NB12
also included the intermediate white layer, but we only found 170 and
169 labeled PDB axons in these experiments. Obviously, the use of the
same protocol in all experiments did not eliminate all variability in
labeling the PDB pathway. Therefore, bouton counts in the PPRF had to
be normalized (see below).
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Figure 6.
Camera lucida drawings of labeled predorsal bundle
fibers at their entry in the pons. A, B,
Topography of sections used to obtain the number of axons for the
normalization of bouton counts in experiments NB3 and NB4,
respectively. The sections are 1125 µm (A) and
1275 µm (B) posterior to the caudal pole of the
trochlear nucleus. A1,
B1, Higher power drawings of the predorsal
bundle region delimited by dashed lines in
A and B, respectively. Short solid
segments, Labeled descending axons. Dotted
lines, Axon collaterals visible at a magnification of 100×.
Axon counts are 107 (A1) and 162 (B1). Aq, Aqueduct;
BC, brachium conjuctivum; CG, central
gray; CI, inferior colliculus; DR, dorsal
nucleus of the raphe; MLF, medial longitudinal
fasciculus; NCF, nucleus cuneiformis;
NCS, nucleus centralis superior; NL,
nuclei of the lateral lemniscus; NRPo, nucleus
reticularis pontis oralis; NRT, nucleus reticularis
tegmenti pontis; PDB, predorsal bundle;
PN, pontine nuclei; VT, ventral tegmental
nucleus (of Gudden).
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The bouton plots of Figure 7 give
overviews of terminations emanating from the two descending pathways in
four of the animals we used. Each one of the overlays illustrates all
the boutons we encountered in five consecutive sections through
the rostral border of the nucleus reticularis pontis caudalis
(NRPc; Brodal, 1957; Taber, 1961). They demonstrate three main groups
of terminations: (1) in the nucleus reticularis tegmenti pontis (NRT)
contralaterally, (2) in the NRPc, mainly contralaterally, and (3) in a
crescent-shaped region of termination in the lateral and ventral parts
of the ipsilateral reticular formation. The quantitative evaluation of pontine terminations was done on 10-15 consecutive sections from each
animal. To ensure that all series of sections represented homotopic
regions of the pons, the most caudal section of each of them was
aligned with the caudal pole of the NRT. Because of a small difference
in brainstem sizes, the center of the segments we evaluated ranged
between 1.7 and 2.0 mm rostral to the abducens nucleus. All boutons
were plotted and counted in the contralateral and ipsilateral halves of
the sections. Next, separate counts were made in the region of the
horizontal saccade generator. This region was defined as a rectangle
extending dorsoventrally between 0 and 3 mm below the surface of the
fourth ventricle and mediolaterally between the midline and 1.6 mm
lateral to it (Fig. 7).
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Figure 7.
Composite plots (5 sections each) of
biocytin-labeled boutons in coronal sections through the PPRF of NB3
(A), NB12 (B), NB2
(C), and NB4 (D).
Dashed lines indicate the areas selected for bouton
counts. Thin solid lines delimit the reticular core and
other pontine nuclei. Vp, Principal sensory nucleus of
the trigeminal nerve; VIIIs, superior vestibular
nucleus; BC, brachium conjuctivum; NRT,
nucleus reticularis tegmenti pontis; NTB, nucleus of the
trapezoid body; PVG, periventricular gray;
TB, trapezoid body.
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We chose these dimensions and positioned the rectangle in such a way as
to obtain the best compromise between the reported locations of
horizontal excitatory medium- and long-lead burst neurons in the cat.
In summary, Sasaki and Shimazu (1981), who were the only ones to verify
the connection of functionally identified saccadic burst neurons with
the abducens nucleus (AbdN), describe them as occupying a region
extending from 0.5 to 2.0 mm anterior to the AbdN, 0.8 to 1.6 mm from
the midline, and 0.5 to 2.5 mm in depth. The region defined by Kaneko
et al. (1981) extends further in the rostrocaudal (up to 3.5 mm in
front of the AbdN) and dorsoventral (up to 3-4 mm deep) directions and
its lateral border is 1.4 mm from the midline. The region defined by
Curthoys et al. (1981) is intermediate between the previous two in
terms of rostrocaudal and dorsoventral extent, but in this case, the
vast majority of burst neurons were found in strictly paramedian sites,
within 0.6 mm from the midline. Therefore, the rectangle we selected for bouton counts includes portions of the burst neuron regions described by all three groups. As shown in Figure 7, the rectangle also
contains parts of the NRT. Boutons found in this nucleus were
subtracted from the total count to obtain the number of boutons in the
PPRF proper.
It is instructive to describe in some detail the two extreme cases in
our sample (NB4 and NB3); these differ a lot both in terms of the size
of the horizontal component of the characteristic vectors of evoked
saccades (Fig. 2) and in terms of the strength of their projections to
the PPRF. Of the 276 ± 36 boutons (mean ± SD) that were
seen in each one of the midpontine sections of NB3, 150 ± 64 were
deployed in the contralateral PPRF (range, 55-255), 7 ± 2 in the
ipsilateral PPRF, and 33 ± 6 in the contralateral NRT, whereas
the remaining participated in the crescent-shaped region of termination
in the lateral part of the ipsilateral reticular formation. Many of the
boutons that were recovered in the ipsilateral reticular formation were
deployed by fibers that originated in the contralateral predorsal
bundle and recrossed the midline. Recrossing of fibers descending in
the lateral tectopontine tract has also been occasionally observed.
Further caudally, a considerable number of boutons were found in the
nucleus reticularis gigantocellularis, bilaterally, and the abducens
nucleus, contralaterally. Much smaller bouton numbers were observed in
each one of the pontine sections of NB4. They were 13 ± 9 (range,
2-30) in the contralateral PPRF, 16 ± 4 in the ipsilateral PPRF,
and 5 ± 2 in the contralateral NRT. This difference was not
caused by a weaker labeling of the predorsal bundle component. On the
contrary, 162 labeled axons were counted in NB4 as they entered the
pontine tegmentum ~1.2 mm behind the trochlear nucleus, and only 107 in NB3. At the level of sections used for bouton counts, 2.5 mm further
caudally, the number of labeled predorsal bundle fibers in NB4 was
decreased by only 8%, whereas a loss of 52% was observed in NB3. The
rapid loss of predorsal bundle axons in NB3 appeared to correlate with an intense collateralization, whereas rostral pontine collaterals were
quite rare in NB4. Thus, the bouton density of NB3 and NB4 was
antipodal to the number of projecting axons but fit well the different
sizes of the horizontal components of saccades evoked from collicular
regions that give rise to these projections.
To examine quantitatively whether this relationship applied to all
animals in our sample, and to compensate for differences between
animals in terms of the number of stained axons we saw in the pons (see
above), we normalized the number of boutons in the PPRF. To this end,
we divided the number of boutons counted in each section through the
PPRF of each animal by the number of fibers entering the pons and then
multiplied by 100 to obtain the number of boutons per 100 fibers per
section. Figure 8 is a scatter plot of
the normalized bouton counts in the PPRF of all sections from all
animals studied. These have been arranged in order of the size of the
horizontal components of the "characteristic" vectors evoked in the
same animals. As shown, there is a concomitant trend for the normalized
number of boutons found in the contralateral PPRF to increase from
7.84 ± 5.7 (mean ± SD) per 100 fibers per section in NB4 to
140.3 ± 59.5 (mean ± SD) in NB3. The average normalized
number of PPRF boutons are plotted against the size of the horizontal
component of the "characteristic" vector of the saccades evoked
from the same collicular microzone in the inset of Figure 8. The linear
regression line through this data passes close to the origin, and its
slope is equal to ~10 contralateral PPRF boutons per degree of
horizontal eye displacement per 100 fibers per section. The high
correlation coefficient (r = 0.92) indicates that about
85% of the variance of the dependent variable (number of boutons
deployed in the contralateral PPRF) can be accounted for by the
independent variable (size of the horizontal component of the
"characteristic" vector of saccades). ANOVA indicated that this
relationship is highly statistically significant
(p < 0.0001).
View larger version (18K):
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Figure 8.
Scatter plot of the number of boutons per 100 fibers (ordinate) deployed in the PPRF. Dashed vertical
lines separate sections that belong to different animals.
Small open circles indicate the number of boutons
observed in adjacent individual 75 µm sections, whereas large
solid circles indicate the average for the animal indicated.
The inset is a plot of the average number of boutons
deployed in the PPRF per 100 fibers per section (B;
ordinate) from each one of the injection sites versus the size of the
horizontal component of the characteristic vector of the saccades
evoked from the same site (H; abscissa). Error
bars indicate the SEM. The solid line is the linear
regression line through the data and obeys the equation
displayed.
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|
It might be argued that instead of horizontal saccade size, the
normalized number of PPRF boutons is correlated with a different saccade metric such as radial size or direction. To test these hypotheses, we plotted the normalized bouton counts against the radial
size and the direction of the characteristic vector of evoked saccades.
The linear regression lines through data plotted in this manner were
more or less flat and did not reach statistical significance (radial
size: slope = 2.32 boutons per section per 100 fibers per degree,
r = 0.25, p > 0.1; direction:
slope = 0.75 boutons per section per 100 fibers per degree,
r = 0.48, p > 0.1). We also examined
the relationship between the normalized bouton counts in the PPRF and
the anatomical coordinates of the injection sites in the SC. The latter
were defined in two ways: (1) in terms of their relative distance from
the rostral pole of the SC [measured from the caudal edge of the
posterior commissure as proposed by Kanaseki and Sprague (1974) and
Edwards (1977)], and (2) in terms of the size of the horizontal
components of the saccade vectors that should be evoked from them
according to McIlwain's (1986) sensorimotor map of the SC after its
superposition on standardized outlines of the SC reconstructed from
individual experiments. No significant correlations were obtained with
either of these two purely anatomical parameters (relative distance
from rostral pole: r = 0.05, p > 0.1;
size predicted from standard map: r = 0.35, p > 0.1).
| |
DISCUSSION |
In this study we tested the hypothesis that the strength of
anatomical projections from different regions of the SC to the PPRF
covaries with the size of the horizontal components of saccades encoded
by these regions. The anatomical strength of connections could depend
on the density of functionally similar efferent neurons and/or the
number of terminals they deploy in relevant target areas. The former
was favored by Edwards and Henkel (1978) but, as pointed out in the
introductory remarks, further supportive evidence has not been
forthcoming. Here, we investigated the second of the two factors, the
number of terminals deployed by tectal axons in the PPRF.
To our knowledge, differences between paramedian pontine projections of
discrete SC regions were evaluated in only one previous study that used
an anterograde degeneration technique (Kawamura et al., 1974). Within
the resolution limit of their method, the authors concluded that there
are no quantitative differences between different parts of the SC in
terms of the density of their projections. Subsequent studies of
collicular efferent projections used the anterograde autoradiographic
tracing technique in cats (Edwards and Henkel, 1978; Huerta and
Harting, 1982; Cowie and Holstege, 1992) and monkeys (Harting, 1977).
Relationships between the location of injection sites and the density
of terminations were not examined in these studies.
The biocytin injections we used spanned a substantial fraction of the
rostrocaudal extent of the SC. In all experiments, the tips of
injection pipettes were located in the SGI so that variation in the
depth of labeled regions was small compared with the extent of the
dendritic fields (600-1600 µm) of the cells of origin of the
predorsal bundle (Moschovakis and Karabelas, 1985). From the duration
of the pulses we used and previous data on current-distance relationships (for review, see Tehovnik, 1996), we estimate that activated cell bodies or axons are located within 0.4-0.55 mm from the
electrode tip for current intensities equal to 20 µA and within
0.55-0.85 mm for current intensities equal to 50 µA. These estimates
match well the distances of tracer diffusion (0.5-0.7 mm) as well as
the size of the zones occupied by radially oriented labeled axons
traversing the SGI to join the tectobulbospinal tract. Therefore, it is
safe to conclude that the cells that were directly labeled with
biocytin correspond reasonably well to the cells that were directly
excited by current.
On the other hand, the number of labeled PDB axons varied almost by
10-fold despite the fact that the volume of tracer injected and the
histochemical processing of the tissue were the same in all
experiments. Accordingly, we had to normalize bouton counts by
calculating the number of boutons in the PPRF per 100 labeled fibers.
Our study demonstrates that the normalized number of boutons deployed
in the PPRF by different collicular microzones increases at a rate of
~10 per section per 100 fibers per degree of horizontal size of the
characteristic vector encoded by the same zones. It is important to
note that this correlation applies to the characteristic vectors of
saccades actually evoked from the labeled sites and not to the
anatomical coordinates of the injection sites as they relate to
standard motor maps. This is consistent with the fact that evoked
saccade vectors cannot be predicted with sufficient precision from the
coordinates of the stimulation sites on a standard motor map matched to
the outlines of the SC. For example, horizontal components of saccades
evoked from the isoazimuth region of 5-10° of the cat range between
6 and 13° (McIlwain, 1990). The situation is similar in the monkey.
Stimulation points along the 10° isoamplitude curve of this species
give rise to saccades that range from 4.5-14° (Robinson, 1972).
Other parameters that might be related to the strength of pontine SC
projections include saccade direction and radial size. Neither proved
statistically significant. We conclude that bouton counts in the PPRF
increase in proportion to only one specific parameter, the horizontal
amplitude of the characteristic vector encoded by the activated
population of tectal efferent neurons.
The PPRF contains long-lead and medium-lead burst neurons discharging
in relation to horizontal saccades and is, thus, thought to encompass
the "horizontal saccadic burst generator" (for review, see Hepp et
al., 1989; Moschovakis et al., 1996). In the cat, the locations of MLBs
and LLBs have been mapped in three studies (Curthoys et al., 1981;
Kaneko et al., 1981; Sasaki and Shimazu, 1981) that are not in perfect
agreement. As pointed out in the Results section, we chose for bouton
counts a PPRF region that contains LLBs and MLBs according to all three
studies. The region selected is in the rostral part of the nucleus
reticularis pontis caudalis and corresponds to an area that receives a
dense tectal projection as revealed by anterograde degeneration and
autoradiographic tracing (Kawamura et al., 1974; Harting, 1977; Huerta
and Harting, 1982; Cowie and Holstege, 1992). Terminations in the same
area have also been demonstrated by intracellular staining of
"visuomotor" tectal projection neurons (Olivier et al., 1993) and
tectal long-lead burst neurons (TLLBs; Scudder et al., 1996). These
anatomical projections do engage the saccadic burst generator, as shown
by the monosynaptic excitatory responses of primate LLBs (Raybourn and
Keller, 1977) and feline MLBs (Hikosaka and Kawakami, 1977; Chimoto et
al., 1996) to SC stimulation.
The region of the feline saccadic burst generator in the PPRF also
contains reticulospinal neurons that generate phasic or phasic-decremental discharges coupled to horizontal saccades and head
movements (Grantyn and Berthoz, 1987; Isa and Naito, 1995). Several
studies suggest that the gaze-related activity of reticulospinal neurons is derived from tectoreticulospinal neurons (TRSNs) that make
collateral connections with the PPRF (Grantyn and Berthoz, 1985;
Olivier et al., 1993). In agreement with this, TRSN burst activity is
related to both saccades and head acceleration in head-free cats (Munoz
et al., 1991). Therefore, the terminations of TRSNs in the PPRF could
contact reticulospinal neurons controlling head movements and eye-head
synergies in addition to cells of the saccadic burst generator (LLBs
and MLBs). Distinguishing between boutons that contact one or the other
class of premotor neurons does not seem necessary because eye and head
movements in the cat are strongly coupled during combined gaze shifts
(Guitton et al., 1984).
Focal injections of biocytin in the SC would also label PDB axons whose
activity is unrelated to saccades, and more generally to orienting
movements (Grantyn and Berthoz, 1985; Moschovakis et al., 1988; Istvan
et al., 1994). Similarly, the medial pontine reticular formation,
including the region we have studied, contains many cells whose
activity is not overtly related to gaze shifts (Siegel, 1979; Siegel
and Tomaszcewski, 1983; Isa and Naito, 1995; Kitama et al., 1995). By
definition, cells unrelated to orienting behavior are not particular as
to the direction and the amplitude of orienting movements. Their
presence, both in the population of labeled SC neurons and among their
target cells in the PPRF, should not, therefore, influence the observed
saccade-related gradient of bouton counts.
To implement the spatiotemporal transformation, several models of the
saccadic system have assumed a differential weighing of synaptic
connections so that TLLBs that discharge before larger saccades exert a
stronger excitatory influence on LLBs and MLBs than TLLBs that
discharge before smaller saccades (for review, see Moschovakis and
Highstein, 1994; Moschovakis et al., 1996). To illustrate how stronger
connections could be transformed to MLB bursts of longer duration, let
us consider the information flow through eye displacement models of the
burst generator (Jürgens et al., 1981; Scudder, 1988;
Moschovakis, 1994). Computer simulations of these models produce LLB
bursts that can be thought of as low-pass filtered versions of the
bursts emitted by collicular neurons (TLLBs). The resettable integrator
cells supposedly receive excitatory input from LLBs (Moschovakis, 1994)
or MLBs (Scudder, 1988) and suppress the discharge of LLBs. When their
augmenting discharge surpasses the discharge of LLBs, the latter stop
discharging. This moment is delayed if the TLLB excitatory drive on
LLBs is made stronger, for example, when the activated TLLBs are the
ones discharging for bigger saccades and deploying stronger
projections. Such a hypothetical circuit suffices to ensure the
proportionality of three variables: (1) the strength of projections of
topographically delimited populations of active TLLBs, (2) the duration
of MLB bursts, and (3) the duration of saccades. However, its correct performance depends on arbitrary choices of feedback and feedforward connection strengths and integrator time constant. The present study is
the first to demonstrate that one of its assumptions, namely the
differential weighing of SC projections to the saccadic burst
generator, is realistic from the point of view of anatomy. The
verisimilitude of other features remains to be experimentally determined.
| |
FOOTNOTES |
Received June 25, 1998; revised Sept. 16, 1998; accepted Sept. 22, 1998.
This work was supported by Human Capital and Mobility Grant
ERBCHRXCT-940559. We gratefully acknowledge the comments of Dr. G. Delides and of an anonymous referee, the help of M. Pagomenou and
G. G. Gregoriou with the analysis of the histological material, M. Chat and M. A. Thomas with the histochemistry, and S. Exinger with
the photomicrographs.
Reprint requests should be addressed to Dr. Alexej Grantyn, Laboratoire
de Physiologie de la Perception et de l'Action, College de
France-Centre National de la Recherche Scientifique, 11 Place Marcelin
Berthelot, 75005 Paris, France.
| |
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February 1, 2005;
93(2):
697 - 712.
[Abstract]
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R. Soetedjo, C. R. S. Kaneko, and A. F. Fuchs
Evidence Against a Moving Hill in the Superior Colliculus During Saccadic Eye Movements in the Monkey
J Neurophysiol,
June 1, 2002;
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[Abstract]
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E. L. Keller, R. M. McPeek, and T. Salz
Evidence Against Direct Connections to PPRF EBNs From SC in the Monkey
J Neurophysiol,
September 1, 2000;
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[Abstract]
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N. J. Gandhi and E. L. Keller
Comparison of Saccades Perturbed by Stimulation of the Rostral Superior Colliculus, the Caudal Superior Colliculus, and the Omnipause Neuron Region
J Neurophysiol,
December 1, 1999;
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[Abstract]
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N. J. Gandhi and E. L. Keller
Activity of the Brain Stem Omnipause Neurons During Saccades Perturbed by Stimulation of the Primate Superior Colliculus
J Neurophysiol,
December 1, 1999;
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[Abstract]
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Y. Izawa, Y. Sugiuchi, and Y. Shinoda
Neural Organization From the Superior Colliculus to Motoneurons in the Horizontal Oculomotor System of the Cat
J Neurophysiol,
June 1, 1999;
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Abstract
Introduction
