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Spinal projections from the nucleus locus coeruleus and nucleus subcoeruleus in the cat and monkey as demonstrated by the retrograde transport of horseradish peroxidase
Brain Research Bulletin,
AI1 rights of reproduction
Vol. 1, pp. 229-234, 1976. Copyright 0 ANKHO International in any form reserved. Printed in the U.S.A.
Inc.
Spinal Projections from the Nucleus Locus Coeruleus and Nucleus Subcoeruleus in the Cat and Monkey as Demonstrated by the Retrograde Transport of Horseradish Peroxidase M. B. HANCOCK
Depurtme~t
ofAnatomy, The University of Texgs Medical (Received
HANCOCK, M. B. AND C. L. FOU~ER~USSE. subcoeruleus
AND C. L. FOUGEROUSSE
in the cat and monkey
as demonstrated
28 November
Branch,
Galveston TX 77550
1975)
Spinal projections from the nucleus locus coeruleus and nucleus by the retrograde transport of horseradish peroxidase. BRAIN RES.
BULL. l(2) 229-234, 1976. - The rostra1 pons of the cat and rhesus monkey were examined for the presence of labeled cells following injections of horseradish peroxidase (HRP) into the lumbar spinal cord. Labeled cells were found in the ipsilateral dorsolateral pontine tegmentum and in the contralateral ventrolateral pontine reticular formation. In both the cat and monkey, labeled cells were located in the nucleus locus coeruleus, nucleus subcoeruleus, in or near the K~lliker-Fur nucleus, and in the ventral part of the Iateral parabrachi~ nucleus. There is a striking similarity between the distribution of HRP-labeled cells in the dorsolateral pontine tegmentum of the cat and monkey and that of catecholamine-containing cells observed in this area in previous studies. Locus coeruleus
Nucleus subcoeruleus
Horseradish peroxidase
injections of a 25% solution of HRP were made in the monkey spinal cords. The injections in the monkeys totaled 1.2 ~1 and 5 ~1. The animals were allowed to survive for three or four days and then perfused with a solution of 0.4% paraformaldehyde and 2.4% glutaraldehyde in 0.1 M phosphate buffer (pH 7.4). The brainstem and spinal cord were removed and pIaced in fixative for 12 hr. The tissue was then soaked for two days in a solution of 30% sucrose in phosphate buffer fpH 7.4). Serial frozen sections (40 pm) were pretreated for 30 min in a 2% solution of diaminobenzidine in phosphate buffer (pH 6.0). Hydrogen peroxide (3 ml/l of 3% H, 0, ) was added to the solution, where the tissue remained for an additional 45 min. The tissue sections were washed in phosphate buffer (pH 7.4), mounted on chrome-alum gelatin coated slides, and lightly stained with cresyl violet. All material was scanned initially with dark-field illumination. Labeled cells detected with dark-field inspection were examined with transmitted light for the presence of granular HRP reaction product. The locations of labeled cells were indicated by scribing small circles on the cover slips with a diamond-tipped marker mounted on the microscope objective turret. Drawings were made from projections of tissue sections and the locations of labeled cells were mapped onto the drawings with the aid of the scribed circles.
THE cells of origin of a number of bulbospinal tracts in the cat were recently demonstrated with the horseradish peroxidase (HRP) method [9]. Injections of HRP in the spinal cord of the cat resulted in the labelling of neurons contributing fibers to a number of descending pathways, including the reticulospinal, solitariospinal, vestibulospinal, interstitiospinal, and rubrospinal tracts. Labeled cells were also observed in the medullary raphe, the dorsolateral pontine tegmentum, and the hypothalamus. The neurons in the dorsolateral pons were located in the nucleus locus coeruleus (LC) and the nucleus subcoeruleus (SC). In the present study, the HRP technique was employed to examine in greater detail the distribution of neurons in the rostra1 pons which send axonal projections into the spinal cord in the cat, and to determine whether similar pathways exist in the monkey. METHOD Experiments were performed on three adult cats and two adolescent rhesus monkeys (Macaca mulatta). Under sodium pentobarbital (Nembutal) anesthesia, a solution of HRP (Sigma type VI) in saline was injected into the left side of the lumbar spinal cord through a micropipette fixed to a microliter syringe. Single 0.2 ~1 injections of a 50% solution of HRP were made in the cats. Multiple 0.2 ~1 229
HANCOCK RESULTS In both the cat and monkey, large numbers of labeled cells were observed in the dorsolateral pontine tegmentum following injections of HRP into the lumbar spinal cord. In all of the animals, labeled neurons were present in the ipsilateral nucleus locus coeruleus (LC), and in the regions ventral to LC, which is homologous to the nucleus subcoeruleus (SC) [If] r Numerous pigmented cells were seen in LC of the monkey. These cells were easily detected with dark-field ~lumination, and had to be differentiated from neurons which were lightly labeled with HRP. With transmitted light at high magnifications, the pigment granules in the cells were round, appeared light brown to tan in color, and were rather homogeneous in size. These pigment granules were identical in color and shape to those observed in LC and the substantia nigra of the normal rhesus monkey and the human. In contrast, HRP reaction product appeared as red-brown granules which were heterogeneous in size and shape. Examples of HRP-labeled cells in LC of the cat and the monkey are shown in Figs. I and 2, respectively. in one of the cats and in both of the monkeys, labeled celis were present in an area intermediate between the ventral border of the brachium conjunctivum (BC) and the nucleus of the lateral lemniscus (NL,L), ipsilateral to the injection. The location of these cells appears to correspond with that of the Kolliker-Fuse nucleus (KF) [ 11. Labeled cells were also observed in the ventral part of the lateral parabrachial nucleus (PbL). Contralateral to the injection, labeled neurons were present in the ventrolateral pontine reticular formation. The distributions of HRP-labeled cells in the rostra1 pons of a cat and a monkey are shown in Figs, 3 and 4. respectively. The extent of spread of HRP from the injected side to the opposite side of the spinal cord was determined from the distribution of labeled cells in the red nuclei, since the rubrosp~nal tract in the cat and monkey is crossed [ l&131_ In the animals from which the material in Figs. 3 and 4 was taken, labeled cells were present only in the contralateral red nucleus. Two types of labeled cells were observed in LC of the cat: medium sized ceils (20-35 x 40 pm) which were generally fusiform in shape, and smaller oval or polygonal cells (ca. 20 pm). In many instances, the fusiform cells were oriented with the long axis in a dorsomedial to ventrolateral direction. The labeled cells in LC of the monkey were spindle-shaped, round, or polygonal, and were generally 20- 25 .UIII in dia. As in the cat, the fusiform cells were often oriented along a dorsomedial to ventrolateraf plane. Labeled c&s in SC of the cat and monkey were ovai or polygon&, and had diameters of 20.--X sm. Labeled cells located ventral to BC in both species, in or near K-F, wert: oval to fusiform in shape, and many of these cells in the cat were oriented horizontally. Approximately one-half of the labeled cells in the ventral part of PbL in the cat were markedly fusiform (20 x 40 pm) and were oriented vertically. The remainder of these cells were oval and had diameters of about 20 pm. The milJority of the labeled cells in the contralateral pontine reticular formation of the cat were multipolar in shape and had diameters of 30-50 pm, while those in the monkey were fusiform (15-25 x 25-40 burn), oval, or round (20-25 pm). Only a few HRP-labeled cells were observed in the brainstem when HRP injections were made into Ihe gray
AND FQLJCEROUSSE
matter through the dorsal columns of the spinal cord. However, the number of labeled cells was substantially increased when injections were made through the lateral funiculi. The increased effectiveness of the latter injections was probably due to the retrograde transport of HRP taken up by damaged axons coursing in the lateral white matter I9l.
In the present study, neurons in the dorsoiateral pontine tegmentum were labeled with HRP transported from the lumbar spinal cord in the cat and the monkey. These cells were located in LC, St, and area corresponding to the Kolliker-Fuse nucleus, and in the ventral portion of the lateral parabrachial nucleus. The majority of the fibers coursing into the spinal cord from this region of the pons descend ipsilaterally. Labeled cells were also found in the contralateral ventrolateral pontine reticular formation The results obtained in the cat in the present investigation are consistent with those of a previous repart fo] In addition, the present observations show that cells in the rostra1 ports of the rhesus monkey send axonal projections into the spinal cord, and that the distribution of tftese c&s within the dorsolateral pontine tegmentum is comparable to that in the cat. A spinat pathway originating in LC has been demonstrated in the rat on the basis of observed reductions in dopamine-fl-hydroxylase activity in the spinal cord following LC lesions [ 141. A myelinated tract originating in LC and descending to the spinal cord in the human has also been described [ 121. Since the nucleus locus coeruleus is present in all mammals [ 15 ] I a spinal pathway originating in this nucleus may be a constant feature of this class of animals. in both the car and monkey, HRP-labeled cells in the dorsolateral pontine tegm~ntum were distributed in a nearly continuous band extending from Lc’ to the ventral border of the brachium conjunctivum (Figs. 3D, 4D-E). The distribution of these cells is remarkably similar to that of catecholamine-containing cells in the pontine tegmentum 13, 6, 71 ; hence, this area of the brainstem may contribute to the population of catecholamine fibers observed in the spinal cord (2,4]. This also suggests that certain cells distributed throughout the dorsolateral pans may constitute a functianally homogenous complex which modulates spinal cord activity. Noradrenaline has been shown to inhibrt spontaneous and elicited activity in spinal neurons, and it has been proposed that noradrenaline is released from the terminals in descending pathways in ihe spinat cord where it acts as an inhibitory transmitter f 5 1. Since LC Lesions abolish the tonic components of the paradoxical phase of sleep [ 81, the inhibition of muscle tone which occurs during paradoxical sleep may depend, in part, on activity in LC eatecholamine cells which send direct projections into the spinal cord. ACKNOWLEDGEMEN’T Tlus study was supported by NIH Grants NS 09018 and GM 00459. ‘The authors wish to thank Donna Hill and Ann Ridens for their technical assistance and Dr. J. D. Coultex for providing the car material.
SPINAL PROJECTIONS
FROM NUCLEUS LOCUS COERULEUS
231
FIG. 1. Exampies of neurons in the nucleus locus coeruleus of the cat which were labeled by the retrograde transport of HRP injected into the lumbar spinal cord (L,). The cells are located ventromedial to the mesencephafic tract of the trigeminal nerve (SMT). Photographs A (100X) and B (250X) show the same three cells with dark-field j~urnjnatioxl. C (250X) was taken with transmitted light and shows cytoplasmic granules of HRP reaction product.
HANCOCK
AND FOUGEROUSSE
FIG. 2,.Labeled neuron in LC of the monkey. HKP was transported to the cell from an injection site in the ipsilateral L, spina segment. A and B (250X) were taken with dark-field illumination and transmitted light, respectively.
REFERENCES 1. Berman, A. L. The Brainstem of the Cat. A Cytoarchitectcmic Atlas with Stereotaxic Coordinates. Madison, Wisconsin: Univ. of Wisconsin Press, 1968. 2. Carlsson, A., B. Faick, K. Fuxe and N.-A. Hilfarp. Cellular localization of monoamines in the spinal cord. Acta physioZ. stand. 60: 112-119,
1964.
3. Chu, N.-S. and F. E. Bloom. The catecholamine-containing neurons in the cat dorsoiaterai pontine tegmentum: Distribution of the cell bodies and some axonal projections. Brain Res. 66: 1-21,
9. IO. 11.
1974.
4.
Dahlstrom, A. and K. Fuxe. Experimentally induced changes in the intraneuronal amine levels of bulbospinal neuron system. Acta physiol. stand. Suppl. 247: 7-36, 1964. 5. Engberg, 1. and R. W. Ryall. The inhibitory action of noradrenaline and other amines on spinal neurons. J. Physiol. 185: 298-322,1966. 6. Feiten, D. L., A. M. Laties and M. B. Carpenter. Monoaminecontaining ceil bodies in the squirrel monkey brain. Am. J. Anat. 139: 153-166,1974.
7. Garver, D. L. and J. R. Sladek, Jr. Monoamine distribution in primate brain. Catecholamine-containing perikarya in the brain stem of Maraca speciosa. J. camp. Neural. 159: 289-304, 1975.
8. Jouvet,
12. 13. 14.
15.
M. and F. Delorme. Locus coeruleus et sommeil paradoxat. C. r. Skanc. Sot. Biol. 159: 895-899.1965. Kuypers, H. G. J. M. and V. A. Maisky. Retrograde axonai transport of horseradish peroxidase from spinal cord to brain stem cell groups in the ~t.~eurosc~ Letters 1: 9-14.1975. Mifler, R. A. and N. L. Strom~ger. Efferent connections of the red nucleus in the brainstem -and spinal cord of the rhesus monkey. J. coma. Neural. 152: 327-346,1973. Olszewski, J. and D. Baxter. Cytoarchitkcture of the Human Brain Stem. New York-Base]: S. Karger, 1954. Papez, J. W. A locospinal tract. Anat. Rec. 29: 392, 1925. Pompeiano, 0. and A. Brodal. Experimental demonstration of a somatotopical origin of rubrospinal fibers in the cat. Anat. Rec. 108: 225-253.1957 Ross, R. A. and D. J. Reis. Effects of lesions of locus coeruleus on regional distribution of dopamine-P-hydroxylase activity in rat brain.Brari?Res 73: 161-166,1974. Russell, G. V. The nucleus locus coeruleus (dorsolaterahs tegmenti). Tex. Rep. Mol. Med. 13: 939-988,195s.
SPINAL PROJECTIONS
FROM NUCLEUS LOCUS COERULEUS
FIG. 3. Distribution of cells in the rostra1 pans of the cat which were labeled by the retrograde transport of HRP injected into the lumbar spinal cord (L,). The spinal cord injection site is shown at the bottom of the figure. Abbreviations: BC, brachium conjunctivum; CG, central gray; K-F, Kolliker-Fuse nucleus; LC, nucleus locus coeruleus; MLF, medial longitudinal fasciculus; 5MT, mesencephalic tract of the trigeminal nerve; NLL, nucfeus of ihe lateral lemniscus; PbL, lateral parabrachial nucleus; PbM, medial parabrachial nucleus; SC, nucleus subcoeruleus.
233
HANCOCK
AND FOUGEROUSSE
.
FIG. 4. Distribution of cells in the rostra1 pons of the rhesus monkey which were labeled by the retrograde transport of HRP injected into the lumbar spinal cord (L,). The spinal cord injection site is shown in the lower right of the figure. Abbreviations are the same as for Fig. 3.
AI1 rights of reproduction
Vol. 1, pp. 229-234, 1976. Copyright 0 ANKHO International in any form reserved. Printed in the U.S.A.
Inc.
Spinal Projections from the Nucleus Locus Coeruleus and Nucleus Subcoeruleus in the Cat and Monkey as Demonstrated by the Retrograde Transport of Horseradish Peroxidase M. B. HANCOCK
Depurtme~t
ofAnatomy, The University of Texgs Medical (Received
HANCOCK, M. B. AND C. L. FOU~ER~USSE. subcoeruleus
AND C. L. FOUGEROUSSE
in the cat and monkey
as demonstrated
28 November
Branch,
Galveston TX 77550
1975)
Spinal projections from the nucleus locus coeruleus and nucleus by the retrograde transport of horseradish peroxidase. BRAIN RES.
BULL. l(2) 229-234, 1976. - The rostra1 pons of the cat and rhesus monkey were examined for the presence of labeled cells following injections of horseradish peroxidase (HRP) into the lumbar spinal cord. Labeled cells were found in the ipsilateral dorsolateral pontine tegmentum and in the contralateral ventrolateral pontine reticular formation. In both the cat and monkey, labeled cells were located in the nucleus locus coeruleus, nucleus subcoeruleus, in or near the K~lliker-Fur nucleus, and in the ventral part of the Iateral parabrachi~ nucleus. There is a striking similarity between the distribution of HRP-labeled cells in the dorsolateral pontine tegmentum of the cat and monkey and that of catecholamine-containing cells observed in this area in previous studies. Locus coeruleus
Nucleus subcoeruleus
Horseradish peroxidase
injections of a 25% solution of HRP were made in the monkey spinal cords. The injections in the monkeys totaled 1.2 ~1 and 5 ~1. The animals were allowed to survive for three or four days and then perfused with a solution of 0.4% paraformaldehyde and 2.4% glutaraldehyde in 0.1 M phosphate buffer (pH 7.4). The brainstem and spinal cord were removed and pIaced in fixative for 12 hr. The tissue was then soaked for two days in a solution of 30% sucrose in phosphate buffer fpH 7.4). Serial frozen sections (40 pm) were pretreated for 30 min in a 2% solution of diaminobenzidine in phosphate buffer (pH 6.0). Hydrogen peroxide (3 ml/l of 3% H, 0, ) was added to the solution, where the tissue remained for an additional 45 min. The tissue sections were washed in phosphate buffer (pH 7.4), mounted on chrome-alum gelatin coated slides, and lightly stained with cresyl violet. All material was scanned initially with dark-field illumination. Labeled cells detected with dark-field inspection were examined with transmitted light for the presence of granular HRP reaction product. The locations of labeled cells were indicated by scribing small circles on the cover slips with a diamond-tipped marker mounted on the microscope objective turret. Drawings were made from projections of tissue sections and the locations of labeled cells were mapped onto the drawings with the aid of the scribed circles.
THE cells of origin of a number of bulbospinal tracts in the cat were recently demonstrated with the horseradish peroxidase (HRP) method [9]. Injections of HRP in the spinal cord of the cat resulted in the labelling of neurons contributing fibers to a number of descending pathways, including the reticulospinal, solitariospinal, vestibulospinal, interstitiospinal, and rubrospinal tracts. Labeled cells were also observed in the medullary raphe, the dorsolateral pontine tegmentum, and the hypothalamus. The neurons in the dorsolateral pons were located in the nucleus locus coeruleus (LC) and the nucleus subcoeruleus (SC). In the present study, the HRP technique was employed to examine in greater detail the distribution of neurons in the rostra1 pons which send axonal projections into the spinal cord in the cat, and to determine whether similar pathways exist in the monkey. METHOD Experiments were performed on three adult cats and two adolescent rhesus monkeys (Macaca mulatta). Under sodium pentobarbital (Nembutal) anesthesia, a solution of HRP (Sigma type VI) in saline was injected into the left side of the lumbar spinal cord through a micropipette fixed to a microliter syringe. Single 0.2 ~1 injections of a 50% solution of HRP were made in the cats. Multiple 0.2 ~1 229
HANCOCK RESULTS In both the cat and monkey, large numbers of labeled cells were observed in the dorsolateral pontine tegmentum following injections of HRP into the lumbar spinal cord. In all of the animals, labeled neurons were present in the ipsilateral nucleus locus coeruleus (LC), and in the regions ventral to LC, which is homologous to the nucleus subcoeruleus (SC) [If] r Numerous pigmented cells were seen in LC of the monkey. These cells were easily detected with dark-field ~lumination, and had to be differentiated from neurons which were lightly labeled with HRP. With transmitted light at high magnifications, the pigment granules in the cells were round, appeared light brown to tan in color, and were rather homogeneous in size. These pigment granules were identical in color and shape to those observed in LC and the substantia nigra of the normal rhesus monkey and the human. In contrast, HRP reaction product appeared as red-brown granules which were heterogeneous in size and shape. Examples of HRP-labeled cells in LC of the cat and the monkey are shown in Figs. I and 2, respectively. in one of the cats and in both of the monkeys, labeled celis were present in an area intermediate between the ventral border of the brachium conjunctivum (BC) and the nucleus of the lateral lemniscus (NL,L), ipsilateral to the injection. The location of these cells appears to correspond with that of the Kolliker-Fuse nucleus (KF) [ 11. Labeled cells were also observed in the ventral part of the lateral parabrachial nucleus (PbL). Contralateral to the injection, labeled neurons were present in the ventrolateral pontine reticular formation. The distributions of HRP-labeled cells in the rostra1 pons of a cat and a monkey are shown in Figs, 3 and 4. respectively. The extent of spread of HRP from the injected side to the opposite side of the spinal cord was determined from the distribution of labeled cells in the red nuclei, since the rubrosp~nal tract in the cat and monkey is crossed [ l&131_ In the animals from which the material in Figs. 3 and 4 was taken, labeled cells were present only in the contralateral red nucleus. Two types of labeled cells were observed in LC of the cat: medium sized ceils (20-35 x 40 pm) which were generally fusiform in shape, and smaller oval or polygonal cells (ca. 20 pm). In many instances, the fusiform cells were oriented with the long axis in a dorsomedial to ventrolateral direction. The labeled cells in LC of the monkey were spindle-shaped, round, or polygonal, and were generally 20- 25 .UIII in dia. As in the cat, the fusiform cells were often oriented along a dorsomedial to ventrolateraf plane. Labeled c&s in SC of the cat and monkey were ovai or polygon&, and had diameters of 20.--X sm. Labeled cells located ventral to BC in both species, in or near K-F, wert: oval to fusiform in shape, and many of these cells in the cat were oriented horizontally. Approximately one-half of the labeled cells in the ventral part of PbL in the cat were markedly fusiform (20 x 40 pm) and were oriented vertically. The remainder of these cells were oval and had diameters of about 20 pm. The milJority of the labeled cells in the contralateral pontine reticular formation of the cat were multipolar in shape and had diameters of 30-50 pm, while those in the monkey were fusiform (15-25 x 25-40 burn), oval, or round (20-25 pm). Only a few HRP-labeled cells were observed in the brainstem when HRP injections were made into Ihe gray
AND FQLJCEROUSSE
matter through the dorsal columns of the spinal cord. However, the number of labeled cells was substantially increased when injections were made through the lateral funiculi. The increased effectiveness of the latter injections was probably due to the retrograde transport of HRP taken up by damaged axons coursing in the lateral white matter I9l.
In the present study, neurons in the dorsoiateral pontine tegmentum were labeled with HRP transported from the lumbar spinal cord in the cat and the monkey. These cells were located in LC, St, and area corresponding to the Kolliker-Fuse nucleus, and in the ventral portion of the lateral parabrachial nucleus. The majority of the fibers coursing into the spinal cord from this region of the pons descend ipsilaterally. Labeled cells were also found in the contralateral ventrolateral pontine reticular formation The results obtained in the cat in the present investigation are consistent with those of a previous repart fo] In addition, the present observations show that cells in the rostra1 ports of the rhesus monkey send axonal projections into the spinal cord, and that the distribution of tftese c&s within the dorsolateral pontine tegmentum is comparable to that in the cat. A spinat pathway originating in LC has been demonstrated in the rat on the basis of observed reductions in dopamine-fl-hydroxylase activity in the spinal cord following LC lesions [ 141. A myelinated tract originating in LC and descending to the spinal cord in the human has also been described [ 121. Since the nucleus locus coeruleus is present in all mammals [ 15 ] I a spinal pathway originating in this nucleus may be a constant feature of this class of animals. in both the car and monkey, HRP-labeled cells in the dorsolateral pontine tegm~ntum were distributed in a nearly continuous band extending from Lc’ to the ventral border of the brachium conjunctivum (Figs. 3D, 4D-E). The distribution of these cells is remarkably similar to that of catecholamine-containing cells in the pontine tegmentum 13, 6, 71 ; hence, this area of the brainstem may contribute to the population of catecholamine fibers observed in the spinal cord (2,4]. This also suggests that certain cells distributed throughout the dorsolateral pans may constitute a functianally homogenous complex which modulates spinal cord activity. Noradrenaline has been shown to inhibrt spontaneous and elicited activity in spinal neurons, and it has been proposed that noradrenaline is released from the terminals in descending pathways in ihe spinat cord where it acts as an inhibitory transmitter f 5 1. Since LC Lesions abolish the tonic components of the paradoxical phase of sleep [ 81, the inhibition of muscle tone which occurs during paradoxical sleep may depend, in part, on activity in LC eatecholamine cells which send direct projections into the spinal cord. ACKNOWLEDGEMEN’T Tlus study was supported by NIH Grants NS 09018 and GM 00459. ‘The authors wish to thank Donna Hill and Ann Ridens for their technical assistance and Dr. J. D. Coultex for providing the car material.
SPINAL PROJECTIONS
FROM NUCLEUS LOCUS COERULEUS
231
FIG. 1. Exampies of neurons in the nucleus locus coeruleus of the cat which were labeled by the retrograde transport of HRP injected into the lumbar spinal cord (L,). The cells are located ventromedial to the mesencephafic tract of the trigeminal nerve (SMT). Photographs A (100X) and B (250X) show the same three cells with dark-field j~urnjnatioxl. C (250X) was taken with transmitted light and shows cytoplasmic granules of HRP reaction product.
HANCOCK
AND FOUGEROUSSE
FIG. 2,.Labeled neuron in LC of the monkey. HKP was transported to the cell from an injection site in the ipsilateral L, spina segment. A and B (250X) were taken with dark-field illumination and transmitted light, respectively.
REFERENCES 1. Berman, A. L. The Brainstem of the Cat. A Cytoarchitectcmic Atlas with Stereotaxic Coordinates. Madison, Wisconsin: Univ. of Wisconsin Press, 1968. 2. Carlsson, A., B. Faick, K. Fuxe and N.-A. Hilfarp. Cellular localization of monoamines in the spinal cord. Acta physioZ. stand. 60: 112-119,
1964.
3. Chu, N.-S. and F. E. Bloom. The catecholamine-containing neurons in the cat dorsoiaterai pontine tegmentum: Distribution of the cell bodies and some axonal projections. Brain Res. 66: 1-21,
9. IO. 11.
1974.
4.
Dahlstrom, A. and K. Fuxe. Experimentally induced changes in the intraneuronal amine levels of bulbospinal neuron system. Acta physiol. stand. Suppl. 247: 7-36, 1964. 5. Engberg, 1. and R. W. Ryall. The inhibitory action of noradrenaline and other amines on spinal neurons. J. Physiol. 185: 298-322,1966. 6. Feiten, D. L., A. M. Laties and M. B. Carpenter. Monoaminecontaining ceil bodies in the squirrel monkey brain. Am. J. Anat. 139: 153-166,1974.
7. Garver, D. L. and J. R. Sladek, Jr. Monoamine distribution in primate brain. Catecholamine-containing perikarya in the brain stem of Maraca speciosa. J. camp. Neural. 159: 289-304, 1975.
8. Jouvet,
12. 13. 14.
15.
M. and F. Delorme. Locus coeruleus et sommeil paradoxat. C. r. Skanc. Sot. Biol. 159: 895-899.1965. Kuypers, H. G. J. M. and V. A. Maisky. Retrograde axonai transport of horseradish peroxidase from spinal cord to brain stem cell groups in the ~t.~eurosc~ Letters 1: 9-14.1975. Mifler, R. A. and N. L. Strom~ger. Efferent connections of the red nucleus in the brainstem -and spinal cord of the rhesus monkey. J. coma. Neural. 152: 327-346,1973. Olszewski, J. and D. Baxter. Cytoarchitkcture of the Human Brain Stem. New York-Base]: S. Karger, 1954. Papez, J. W. A locospinal tract. Anat. Rec. 29: 392, 1925. Pompeiano, 0. and A. Brodal. Experimental demonstration of a somatotopical origin of rubrospinal fibers in the cat. Anat. Rec. 108: 225-253.1957 Ross, R. A. and D. J. Reis. Effects of lesions of locus coeruleus on regional distribution of dopamine-P-hydroxylase activity in rat brain.Brari?Res 73: 161-166,1974. Russell, G. V. The nucleus locus coeruleus (dorsolaterahs tegmenti). Tex. Rep. Mol. Med. 13: 939-988,195s.
SPINAL PROJECTIONS
FROM NUCLEUS LOCUS COERULEUS
FIG. 3. Distribution of cells in the rostra1 pans of the cat which were labeled by the retrograde transport of HRP injected into the lumbar spinal cord (L,). The spinal cord injection site is shown at the bottom of the figure. Abbreviations: BC, brachium conjunctivum; CG, central gray; K-F, Kolliker-Fuse nucleus; LC, nucleus locus coeruleus; MLF, medial longitudinal fasciculus; 5MT, mesencephalic tract of the trigeminal nerve; NLL, nucfeus of ihe lateral lemniscus; PbL, lateral parabrachial nucleus; PbM, medial parabrachial nucleus; SC, nucleus subcoeruleus.
233
HANCOCK
AND FOUGEROUSSE
.
FIG. 4. Distribution of cells in the rostra1 pons of the rhesus monkey which were labeled by the retrograde transport of HRP injected into the lumbar spinal cord (L,). The spinal cord injection site is shown in the lower right of the figure. Abbreviations are the same as for Fig. 3.