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Ipsilaterally projecting rubrospinal neurons in adult and developing opossums.

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THE ANATOMICAL RECORD 231538-547 (1991)
lpsilaterally Projecting Rubrospinal Neurons in Adult and
Developing Opossums
XIAO MING XU AND G.F. MARTIN
Department of Cell Biology, Neurobiology, and Anatomy, The Ohio State University
College of Medicine, Colurnbus, Ohio
ABSTRACT’ We have combined injections of Fast Blue with lesions of the
rubrospinal tract rostra1 and contralateral to them to determine if an ipsilateral
rubrospinal projection exists in adult or developing opossums and, if so, to characterize the neurons giving rise to it. Although the results indicate that some
rubral neurons project ipsilaterally, they are very few in number. Using quantitative and image analysis techniques, we have shown that 0.6% of the rubral
neurons that project to the lumbar cord in adult opossums do so ipsilaterally and
that such neurons are comparable in location and size to those that project contralaterally. Similar results were obtained in developing opossums. Our results are
discussed in light of rubrospinal development and ongoing experiments related to
rubrospinal plasticity.
The rubrospinal tract is generally considered to be
crossed (see reviews by Kuypers, 1982; Walberg, 19821,
but an ipsilateral component has been suggested for
the hedgehog (Michaloudi et al., 1988) and documented
for the rat (Shieh et al., 1983) and cat (Holstege and
Kuypers, 1982; Holstege, 1987). One of the objectives of
the present study was to establish whether an ipsilatera1 rubrospinal projection is present in the North
American opposum, Didelphis virginiana, and, if so, to
determine the location, number, and size of the neurons contributing to it. Previous studies suggested that
such a projection exists (Martin and Dom, 1970; Martin
et al., 1974; Cabana and Martin, 19861, but the results
were inconclusive. To the best of our knowledge, ipsilaterally projecting rubrospinal neurons have not been
characterized for any species.
We have shown previously that the opposum’s rubrospinal tract develops postnatally (Cabana and Martin, 1986, Martin et al., 1986, 1988) rather than prenatally as in rats (Leong et al., 1984; Shieh et al., 1983)
and cats (Bregman and Goldberger, 1982, 19831, making it possible to manipulate it without intrauterine
surgery. In the experiments reported here, we took advantage of that fact to identify rubrospinal neurons
that project ipsilaterally during selected stages of development. We paid particular attention to the critical
period for rubrospinal plasticity, i.e., the period during
which rubral axons can grow around a lesion of their
spinal pathway (Martin and Xu, 1988; Xu and Martin
19891, because an earlier study suggested that a welldeveloped, ipsilateral pathway may exist during that
stage of development (Cabana and Martin, 1986). If so,
it would be relevant to the interpretation of ongoing
experiments designed to determine whether rubrospinal plasticity results from regeneration of cut axons or
new growth. Although our results suggest that an ipsilateral rubrospinal tract exists in both adult and developing opossums, the neurons that contribute to it
are few in number. Using quantitative and image analysis techniques, we have shown that only 0.6% of the
0 1991 WILEY-LISS, INC.
rubral neurons that project to the lumbar cord in adult
opossums do so ipsilaterally and that such neurons cannot be distinguished from those that project contralaterally by their location or size. Similar results were
obtained in developing opossums.
METHODS
Four adult female opossums were anesthetized with
sodium pentobarbitol (40 mg/kg) for sterile surgery.
The eighth or ninth segment of the thoracic cord was
exposed first so that the rubrospinal tract could be
transected on the right side. The first or second segment of the lumbar cord was then exposed for a 10 p1
injection of 3%Fast Blue (FBI on the left side. Since the
rubrospinal tract was cut on the right, the side contralateral to the injection, we assumed that any neurons labeled in the left red nucleus projected ipsilaterally. Few, if any, rubral axons cross the midline at
spinal levels (Martin and Dom, 1970; Martin et al.,
1974; Cabana and Martin, 1986).
After the injection, the soft tissues were sutured together in layers and the animals were returned to the
vivarium under a veterinarian’s care, Seven days later
they were given an overdose of the anesthetic and perfused transcardially with saline followed by a 0.1 M
cirtate buffer-10% formaldehyde solution. The spinal
cord and brain were dissected out and immersed in the
same buffer with 30% sucrose for approximately 24
hours at 4°C.The brain was scored with a shallow cut
on the side of the lesion so that laterality of the tissue
sections could be determined after mounting. Frozen
sections through the lesion, the injection, and the
brainstem were cut in the corona1 plane at 40 pm. The
Received October 26, 1991; accepted February 9, 1991.
Address reprint requests to Dr. George F. Martin, Dept. of Cell
Biology, Neurobiology, and Anatomy, The Ohio State University College of Medicine, 333 West 10th Ave., Columbus, OH 43210-1218.
IPSILATERALLY PROJECTING RUBROSPINAL NEURONS
sections were mounted immediately and coverslipped
with Entellan (Merck) for viewing with a Leitz (Orthoplan) flurorescence microscope using the A cube of the
Ploem illumination system (excitation wavelength =
340-380 nm).
The positions of labeled neurons ipsilateral and contralateral to the injection were plotted and counted
from every fifth section through the red nucleus using
a n X-Y plotter attached to the microscope stage by position transducers. All labeled neurons were recorded,
including those not sectioned through the nucleus, and
selected fields were photographed. In each case, labeled
neurons contralateral to the injection were drawn from
two sections each through the rostral, middle, and caudal thirds of the red nucleus (about one out of 10 sections) using a drawing tube attached to the microscope.
Since labeled neurons were sparse ipsilateral to the
injection, all of them were drawn from every section.
The areas of labeled neurons were determined with the
aid of a n interactive computer-assisted image analysis
system (Magiscan, NikoniJoyce Loebl). Drawings of
the labeled neurons were fed into a black-and-white
television camera (Doge-MtI series 68, Newvicon), then
through a real-time video processor (Nippon Avionics,
Model Image Sigma), and finally into a computer
(Magiscan 2A, Joyce-Loebl) for digitization and analysis. The outline of each cell was filled in by the computer, which was instructed to separate dark areas (labeled cells) from light areas (noncells). Calibration was
done so that the area of labeled cells was measured in
pm2. Statistical analysis was accomplished by using
the Results program supplied by Joyce-Loebl. The output from the computer provided histograms showing
the size and frequency distribution of labeled neurons
on each side.
Using a comparable approach, one animal was subjected to a lesion of the right rubrospinal tract a t the
third segment of the cervical cord and a n injection of
FB on the left at the sixth cervical segment. Survival
time, perfusion, tissue processing, and evaluation were
accomplished a s described above.
For the developmental studies, pouch-young opossums were employed at estimated postnatal day
(EPD)20 (N = 41, 40 (N = 31, and 54 (N = 2). The
developing animals were obtained from females captured in the wild so their snout-rump length (SRL) was
measured by stretching them on a ruler to estimate age
from the growth curve of Cutts e t al. (1978). The
mother was anesthetized by a 1.2 ml intramuscular
injection of Ketamine (100 mg/ml) followed by inhalation of Metofane and then placed on her back. During
anesthesia the pouch sphincter relaxed, exposing the
litter. The pouch-young, still attached to the nipples,
were anesthetized individually by hypothermia or Metofane inhalation for lesions of the rubrospinal tract on
the right side of the thoracic cord and FB injections into
the left side of the lumbar cord as described for the
adult animal. The incisions were closed and the operated animals returned with their mother to the vivarium. Seven days later, the pouch-young were removed,
sacrificed by a n overdose of the anesthetic, and perfused through the heart with the same fixative used for
the adult animal. The spinal cord and brain were removed, scored, sectioned, mounted, and examined as
described above. In these cases, labeled neurons were
539
plotted and counted in one out of every three sections.
Labeled neurons were not drawn and measured because the fluorescence fades too rapidly in young animals.
RESULTS
Studies on Adult Animals
Figure 1provides photomicrographic documentation
of the results obtained from one of the adult animals
subjected to hemisection of the thoracic cord on the
right and a lumbar injection of FB on the left. The
photomicrographs were taken from one out of every 10
sections through the red nucleus from its rostral (top)
to caudal (bottom) ends. On the side contralateral to
the injection (right column, Fig. l ) , labeled neurons
were numerous throughout the length of the nucleus.
In rostral sections, most of them were found ventrally
(Fig. lB,D), whereas more caudally (Fig. lF,H,J,L),
they were more evenly dispersed dorsoventrally. In
caudal sections, there was a tendency for labeled neurons to be most numerous laterally. On the side ipsilateral to the injection, only one labeled neuron can be
observed (arrow, Fig. 1C). Figure 2 contains a plot of
the labeling present in one out of five sections from the
same case and a histogram of the quantitative results.
In the four cases studies, a n average of 431.2 neurons
was counted in one out of five sections on the side contralateral to the injection, whereas only 2.7 were
counted ipsilaterally. The paired t test showed that the
difference between the two groups was statistically significant (P < 0.01).
The histograms in Figure 3 show the frequency of
labeled neurons according to size in the rostral (top),
middle (middle), and caudal (bottom) thirds of the red
nucleus contralateral and ipsilateral to the injection.
Because of their sparsity, all of the labeled neurons
were counted and measured ipsilateral to the injection,
whereas only those in two sections from each third of
the nucleus (about one out of 10 sections) were evaluated on the contralateral side. The results suggest that
neurons projecting ipsilaterally do not constitute a separate subset based on size.
The locations of all labeled neurons ipsilateral to the
injection in the four lumbar cases are plotted on the
right in Figure 3. The top drawing depicts the locations
of such neurons in the rostral 1/3 of the red nucleus,
and i t can be seen that most of them were located ventrally. Those in the middle and caudal thirds of the
nucleus were found dorsally and ventrally. In general,
the ipsilaterally projecting neurons were found in areas that also project contralaterally.
Figure 4 illustrates the rubral neurons labeled contralateral and ipsilateral to the injection in the case
subjected to a lesion of the rubrospinal tract on the
right a t the third cervical segment and a n injection of
FB on the left three segments caudal to the lesion. On
the side contralateral to the injection, labeled neurons
were numerous throughout the length of the red nucleus (right column, Fig. 4). Rostrally, more of them
were labeled in the dorsal part of the nucleus than after
lumbar injections (compare Figs. 1D and 4D) and, caudally, neurons were labeled dorsomedially where they
were not labeled after lumbar injections (compare Figs.
1J and 4J).On the side ipsilateral to the injection (left
column Fig. 41, only three neurons were labeled (ar-
540
X.M. XU A N D G.F. MARTIN
Fig. 1, Fluorescence photomicrographs of labeled neurons in one
out of every 10 sections from the rostra1 (top) to caudal (bottom) poles
of the red nucleus contralateral (right column) and ipsilateral (left
column) to the injection in a n adult opossum subjected to a lesion of
the right rubrospinal tract a t the eighth thoracic segment and a lumbar injection of Fast Blue on the left. The arrow in C points to a
neuron labeled ipsilateral to the injection.
IPSILATERALLY PROJECTING RUBROSPINAL NEURONS
54 1
Fig. 2. Plot showing the locations of labeled neurons in one out of five sections through the red nucleus
from the case documented in Figure 1. The arrow indicates the only neuron labeled ipsilateral to the
injection in these sections. The histogram gives the average number of neurons labeled contralateral and
ipsilateral to the injection in the four adult cases subjected to lumbar injections
rows, Fig. 4A,C,G). Counts of labeled neurons on the
two sides show that 472 were present contralaterally,
whereas only 8 were present ipsilaterally. The photomicrographs in Figure 5 show that the neurons labeled
ipsilateral to the injection (Fig. 5C) were comparable in
size, shape, and labeling intensity t o those labeled contralaterally (Fig. 5B,D). The same was true for the neurons labeled after lumbar injections.
Studies on Developing Animals
At the ages studies (PD20, 40 and 541, the results
were comparable to those obtained in the adult animals, Figure 6 illustrates the labeling produced in one
of the cases operated a t PD20, which is during the critical period for rubrospinal plasticity. Labeling in the
red nucleus contralateral to the injection was extensive
and present in all of the areas labeled in adult animals
(right column, Fig. 6). As in the adult animal, that on
the ipsilateral side was sparse (arrows, Fig. 6A, K).
Figure 7 shows a plot of the labeling obtained in one
out of three sections from the same case. In the four
cases studies, the average number of labeled neurons
contralateral to the injection (one out of three sections)
was 227.8, whereas on the ipsilateral side it was 3.0.
The paired t test showed that the difference between
the two groups was statistically significant (P< 0.01).
DISCUSSION
In degeneration studies, there was often evidence for
axonal degeneration in the opposum’srubrospinal tract
ipsilateral as well as contralateral to lesions of the red
nucleus (Martin and Dom, 1970; Martin et al., 1974).
Such degeneration could not be taken as definitive evidence for an ipsilateral rubrospinal tract, however,
since the lesions may have damaged rubral axons from
the contralateral side. Although the orthograde transport of wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP) also provided evidence for
an ipsilateral projection (Cabana and Martin, 19861,
the injections may have produced “injury label” of ax-
542
X.M. X U AND G.F. MARTIN
Area of Labeled Neurons
n
Plot of Ipsi. Proi. Neurons
Latera i
Medial
Rostra1
Area ( p m ' )
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Fig. 3. Histograms showing the frequency of labeled neurons in
different size ranges from the rostral (top), middle (middle), and caudal (lower) thirds of the red nucleus ipsilateral and contralateral to
lumbar injections. The labeled neurons contralateral to the injection
were measured from only two sections in each third of the nucleus
(about one out of each 10 sections), whereas all of the neurons labeled
on the ipsilateral side were measured. The positions of the labeled
neurons in the rostral, middle, and caudal thirds of the red nucleus
ipsilateral to the injections are plotted on the right from all the lumbar cases.
ons from the contralateral red nucleus. The results of
the present study clearly document the existence of
ipsilaterally projecting rubrospinal neurons, however,
and show that they are comparable in location and size
to those that project contralaterally. The existence of
such neurons can be inferred in the hedgehog (Michaloudi et al., 1988) and their presence has been documented in the rat (Shieh et al., 1983) and cat (Hol-
IPSILATERALLY PROJECTING RUBROSPINAL NEURONS
Fig. 4. Fluorescence photomicrographs of labeled neurons in one out
of every 10 sections from the rostra1 (top) to the caudal (bottom) end
of the red nucleus contralateral (right column) and ipsilateral (left
column) to the injection in a case subjected to a lesion of the right
543
rubrospinal tract a t the third cervical segment and an injection of
Fast Blue into the sixth cervical segment on the left. The arrows in A,
C, and G point to neurons labeled ipsilateral to the injection.
544
X.M. XU AND G.F. MARTIN
Fig. 5.High power fluorescence photomicrographs of sections through the red nucleus contralateral (B,
D) and ipsilateral (A, C) to the injection from the case referred to in Figure 4.
stege and Kuypers, 1982; Holstege, 1987). The present
study is the first, however, to characterize them as to
location and size.
In a previous orthograde transport study, we observed substantial labeling in the area of the rubrospinal tract ipsilateral as well as contralateral to injections of WGA-HRP into the red nucleus of developing
opossums (Fig. 2, Cabana and Martin, 1986). With increasing age, the ipsilateral labeling became less obvious (Cabana and Martin, 1986), suggesting that the
ipsilateral pathway decreased in size due to axonal degeneration andlor retraction. Evidence for loss of ipsilateral projections in the development of the predominantly crossed corticospinal (Cabana and Martin, 1985;
Theriault and Tatton, 1989) and retinocollicular projections (Jeffrey and Perry, 1982; Martin et al., 1983;
Insausti et al., 1984; Jacobs et al., 1984) has been reported previously, so it was reasonable t o assume that
the same phenomenon might occur in rubrospinal development. The present results indicate that rubral
neurons that project ipsilaterally are almost as sparse
during development as in the adult animal, however,
arguing against the existence of a large ipsilateral
pathway that diminishes with age. It is likely that the
ipsilateral labeling observed in our previous study resulted from incorporation of the marker by axons from
the contralateral red nucleus and/or spread of the injection into the dorsolateral pons (Martin et al., 1979).
During development, rubrospinal axons have to
choose whether they will cross a t the ventral tegmental
decussation or remain ipsilateral. Although our results
speak only to the development of laterality in the lumbar cord, they suggest that rubrospinal axons make the
correct choice and that laterality is established early in
development. Laterality of reticulospinal and vestibulospinal projections is already established in the 11-day
chicken embryo (Glover and Petursdottir, 1988), but
that of the rubrospinal tract has not been reported.
Retina1 axons also make a choice at the optic chiasm,
and it has been shown in the mouse that most of them
make the correct one (Sretavan, 1990).
We have shown that rubral axons grow around a
lesion of their spinal pathway at about postnatal day
20 in the opossum, although relatively few rubrospinal
neurons survive axotomy (Martin and Xu, 1988; Xu
and Martin, 1989). From these observations we hypothesized that rubrospinal plasticity results primarily
from new growth, not true regeneration. In an attempt
to test that hypothesis, we injected FB into the spinal
cord at about postnatal day 18 to label rubral neurons
that innervate that level. Four days later the axons of
such neurons were cut in a second surgery. The animals were allowed to survive for about 30 days, after
which another fluorescent marker, Diamidino Yellow
(DY),was injected between the first injection and the
lesion. The intent of the second injection was to label
IPSILATERALLY PROJECTING RUBROSPINAL NEURONS
Fig. 6. Fluorescence photomicrographs of labeled neurons in one out
of three sections from the rostra1 (top) to the caudal (bottom) end of
the red nucleus contralateral (right column) and ipsilateral (left column) to the injection in a n animal subjected to a thoracic lesion of the
545
rubrospinal tract on the right and a n injection of Fast Blue into the
lumbar cord on the left a t postnatal day 20. The arrows in A and K
indicate the neurons labeled on the ipsilateral side.
546
L
X.M. XU AND G.F. MARTIN
300
3
2
71
200
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QJ
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d
100
6-
0
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0
Z
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1 mm
Fig. 7. Plot showing the locations of labeled neurons in one out of every three sections through the red
nucleus from the pouch-young opossium referred to in Figure 6. The arrow points to labeled neurons
ipsilateral to the injection. The histogram gives the average number of neurons labeled contralateral and
ipsilateral to the injection in the four cases studies at this age.
rubral neurons whose axon had grown around the lesion during the 30 day survival. Upon microscopic examination, relatively few neurons in the contralateral
red nucleus were labeled by FB, but many were labeled
by DY. Some were labeled by both markers, however,
suggesting that they survived axotomy and t h a t their
axons grew around the lesion to incorporate the second
marker. Alternative explanations include the possibility that the double-labeled neurons projected ipsilaterally and t h a t they incorporated both markers because
of bilateral spread at the injection sites. The results of
the present study suggest t h a t is not likely, however,
because so few rubrospinal neurons project ipsilaterally.
ACKNOWLEDGMENTS
The authors thank Ms. Mary Ann Jarrell for surgical
assistance, tissue processing, and typing of the manuscript; Mr. Karl Rubin for photographic help; and Mr.
Michael Pindzola for helping with the computer counts
and measurements. We are also grateful to Dr. Michael
Beattie for providing helpful comments on the manuscript. This study was supported by USPHS grants NS25095 and NS-10165 as well a s a n Academic Challenge
Award to the Neuroscience Program from the State of
Ohio.
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