Abstract
The cells that project from the brain to the spinal cord have previously been mapped in a wide range of mammalian species, but have not been comprehensively studied in the mouse. We have mapped these cells in the mouse using retrograde tracing after large unilateral Fluoro-Gold (FG) and horseradish peroxidase (HRP) injections in the C1 and C2 spinal cord segments. We have identified over 30 cell groups that project to the spinal cord, and have confirmed that the pattern of major projections from the cortex, diencephalon, midbrain, and hindbrain in the mouse is typically mammalian, and very similar to that found in the rat. However, we report two novel findings: we found labeled neurons in the precuneiform area (an area which has been associated with the midbrain locomotor center in other species), and the epirubrospinal nucleus. We also found labeled cells in the medial division of central nucleus of the amygdala in a small number of cases. Our findings should be of value to researchers engaged in evaluating the impact of spinal cord injury and other spinal cord pathologies on the centers which give rise to descending pathways.
Similar content being viewed by others
References
Adli DSH, Stuesse SL, Cruce WLR (1999) Immunohistochemistry and spinal projections of the reticular formation in the northern leopard frog, Rana pipiens. J Comp Neurol 404:387–407
Aicher SA, Reis DJ, Nicolae R, Milner TA (1995) Monosynaptic projections from the medullary gigantocellular reticular formation to sympathetic preganglionic neurons in the thoracic spinal cord. J Comp Neurol 363:563–580
Akaike T, Fanardji Vv, Ito M, Kumada M, Nakajima H (1973) Electrophysiological analysis of vestibulospinal reflex pathway of rabbit.1. Classification of tract cells. Exp Brain Res 17:477–496
Altman J, Carpenter MB (1961) Fiber projections of superior colliculus in cat. J Comp Neurol 116:157–177
Arends JJ, Zeigler HP (1991) Organization of the cerebellum in the pigeon (Columba livia): II. Projections of the cerebellar nuclei. J Comp Neurol 306:245–272
Bangma GC, ten Donkelaar HJ, Dederen PJ, de Boer-van Huizen R (1984) Cerebellar efferents in the lizard Varanus exanthematicus. II. Projections of the cerebellar nuclei. J Comp Neurol 230:218–230
Bankoul S, Neuhuber WL (1992) A direct projection from the medial vestibular nucleus to the cervical spinal dorsal horn of the rat, as demonstrated by anterograde and retrograde tracing. Anat Embryol 185:77–85
Bareyre FM, Kerschensteiner M, Misgeld T, Sanes JR (2005) Transgenic labeling of the corticospinal tract for monitoring axonal responses to spinal cord injury. Nat Med 11:1355–1360
Barreiro-Iglesias A, Villar-Cervino V, Anadon R, Rodicio MC (2008) Descending brain–spinal cord projections in a primitive vertebrate, the lamprey: cerebrospinal fluid-contacting and dopaminergic neurons. J Comp Neurol 511:711–723
Basbaum AI, Fields HL (1979) The origin of descending pathways in the dorsolateral funiculus of the spinal cord of the cat and rat: further studies on the anatomy of pain modulation. J Comp Neurol 187:513–531
Batton RR, Jayaraman A III, Ruggiero D, Carpenter MB (1977) Fastigial efferent projections in the monkey: an autoradiographic study. J Comp Neurol 174:281–305
Berk ML, Finkelstein JA (1983) Long descending projections of the hypothalamus in the pigeon, Columba livia. J Comp Neurol 220:127–136
Boers J, Kirkwood PA, de Weerd H, Holstege G (2006) Ultrastructural evidence for direct excitatory retroambiguus projections to cutaneous trunci and abdominal external oblique muscle motoneurons in the cat. Brain Res Bull 68:249–256
Buhler AV, Proudfit HK, Gebhart GF (2004) Separate populations of neurons in the rostral ventromedial medulla project to the spinal cord and to the dorsolateral pons in the rat. Brain Res 1016:12–19
Burton H, Loewy AD (1977) Projections to the spinal cord from medullary somatosensory relay nuclei. J Comp Neurol 173:773–792
Burton H, Craig AD, Poulos DA, Molt JT (1979) Efferent projections from temperature sensitive recording loci within the marginal zone of the nucleus caudalis of the spinal trigeminal complex in the cat. J Comp Neurol 183:753–777
Carleton SC, Carpenter MB (1984) Distribution of primary vestibular fibers in the brainstem and cerebellum of the monkey. Brain Res 294:281–298
Carlton SM, Chung JM, Leonard RB, Willis WD (1985) Funicular trajectories of brainstem neurons projecting to the lumbar spinal cord in the monkey (Macaca fascicularis): a retrograde labeling study. J Comp Neurol 241:382–404
Carretta D, Santarelli M, Vanni D, Carrai R, Sbriccoli A, Pinto F, Minciacchi D (2001) The organisation of spinal projecting brainstem neurons in an animal model of muscular dystrophy. A retrograde tracing study on mdx mutant mice. Brain Res 895:213–222
Casale EJ, Light AR, Rustioni A (1988) Direct projection of the corticospinal tract to the superficial laminae of the spinal cord in the rat. J Comp Neurol 278:275–286
Castiglioni AJ, Gallaway MC, Coulter JD (1978) Spinal projections from midbrain in monkey. J Comp Neurol 178:329–345
Chamberlin NL, Saper CB (1998) A brainstem network mediating apneic reflexes in the rat. J Neurosci 18:6048–6056
Chiocchetti R, Bombardi C, Grandis A, Mazzuoli G, Gentile A, Pisoni L, Joechler M, Lucchi ML (2006) Cytoarchitecture, morphology, and lumbosacral spinal cord projections of the red nucleus in cattle. Am J Vet Res 67:1662–1669
Clark FM, Proudfit HK (1991) The projection of noradrenergic neurons in the A7 catecholamine cell group to the spinal cord in the rat demonstrated by anterograde tracing combined with immunocytochemistry. Brain Res 547:279–288
Cowie RJ, Holstege G (1992) Dorsal mesencephalic projections to pons, medulla, and spinal cord in the cat: limbic and non-limbic components. J Comp Neurol 319:536–559
Cox RG, Peusner KD (1990) Horseradish peroxidase labeling of the central pathways in the medulla of the ampullary nerves in the chicken, Gallus gallus. J Comp Neurol 297:564–581
Craig AD (1978) Spinal and medullary input to the lateral cervical nucleus. J Comp Neurol 181:729–743
Cruce WLR, Stuesse SL, Northcutt RG (1999) Brainstem neurons with descending projections to the spinal cord of two elasmobranch fishes: thornback guitarfish, Platyrhinoidis triseriata, and horn shark, Heterodontus francisci. J Comp Neurol 403:534–560
Crutcher KA, Humbertson AO, Martin GF (1978) The origin of brainstem-spinal pathways in the North American opossum (Didelphis virginiana). Studies using the horseradish peroxidase method. J Comp Neurol 179:169–193
de Boer-van Huizen RT, ten Donkelaar HJ (1999) Early development of descending supraspinal pathways: a tracing study in fixed and isolated rat embryos. Anat Embryol 199:539–547
Diagne M, Valla J, Delfini C, Buisseret-Delmas C, Buisseret P (2006) Trigeminovestibular and trigeminospinal pathways in rats: retrograde tracing compared with glutamic acid decarboxylase and glutamate immunohistochemistry. J Comp Neurol 496:759–772
Dobolyi A, Palkovits M, Bodnar I, Usdin TB (2003) Neurons containing tuberoinfundibular peptide of 39 residues project to limbic, endocrine, auditory and spinal areas in rat. Neuroscience 122:1093–1105
Dum RP, Strick PL (1996) Spinal cord terminations of the medial wall motor areas in macaque monkeys. J Neurosci 16:6513–6525
Edwards DL, Poletti CE, Foote WE (1987) Evidence for leucine-enkephalin immunoreactive neurons in the medulla which project to spinal cord in squirrel monkey. Brain Res 437:197–203
Ellenberger HH (1999) Nucleus ambiguus and bulbospinal ventral respiratory group neurons in the neonatal rat. Brain Res Bull 50:1–13
Franklin KBJ, Paxinos G (2008) The mouse brain in stereotaxic coordinates, 3rd edn. Elsevier Academic Press, San Diego
Fritschy JM, Lyons WE, Mullen CA, Kosofsky BE, Molliver ME, Grzanna R (1987) Distribution of locus coeruleus axons in the rat spinal cord: a combined anterograde transport and immunohistochemical study. Brain Res 437:176–180
Gahtan E, O’Malley DM (2003) Visually guided injection of identified reticulospinal neurons in zebrafish: a survey of spinal arborization patterns. J Comp Neurol 459:186–200
Galea MP, Darian-Smith I (1994) Multiple corticospinal neuron populations in the macaque monkey are specified by their unique cortical origins, spinal terminations, and connections. Cereb Cortex 4:166–194
Gerrits PO, Vodde C, Holstege G (2000) Retroambiguus projections to the cutaneus trunci motoneurons may form a pathway in the central control of mating. J Neurophysiol 83:3076–3083
Gilbey MP, Futuro-Neto HA, Zhou SY (1995) Respiratory-related discharge patterns of caudal raphe neurones projecting to the upper thoracic spinal cord in the rat. J Auton Nerv Syst 50:263–273
Glover JC, Petursdottir G (1988) Pathway specificity of reticulospinal and vestibulospinal projections in the 11-day chicken embryo. J Comp Neurol 270(25–38):21–60
Goode GE, Humbertson AO, Martin GF (1980) Projections from the brain stem reticular formation to laminae I and II of the spinal cord. Studies using light and electron microscopic techniques in the North American opossum. Brain Res 189:327–342
Graham J (1977) Autoradiographic study of efferent connections of superior colliculus in cat. J Comp Neurol 173:629–654
Gross GH, Oppenheim RW (1985) Novel sources of descending input to the spinal cord of the hatching chick. J Comp Neurol 232:162–179
Guyenet PG (1980) The coeruleospinal noradrenergic neurons: anatomical and electrophysiological studies in the rat. Brain Res 189:121–133
Hallbeck M (2000) Dynorphin mRNA-expressing neurons in the rat paraventricular hypothalamic nucleus project to the spinal cord. Neurosci Lett 285:161–164
Hallbeck M, Blomqvist A (1999) Spinal cord-projecting vasopressinergic neurons in the rat paraventricular hypothalamus. J Comp Neurol 411:201–211
Hancock MB, Fougerousse CL (1976) 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 Res Bull 1:229–234
Hardy SG, Horecky JG, Presley KG (1998) Projections of the caudal ventrolateral medulla to the thoracic spinal cord in the rat. Anat Rec 250:95–102
Harting JK (1977) Descending pathways from the superior collicullus: an autoradiographic analysis in the rhesus monkey (Macaca mulatta). J Comp Neurol 173:583–612
Hassouna E, Yamamoto M, Imagawa T, Uehara M (2001) Distribution of reticulospinal neurons in the chicken by retrograde transport of WGA-HRP. Tissue Cell 33:141–147
Hayes NL, Rustioni A (1981) Descending projections from brainstem and sensorimotor cortex to spinal enlargements in the cat. Single and double retrograde tracer studies. Exp Brain Res 41:89–107
Hobbelen JF, Gramsbergen A, van Hof MW (1992) Descending pathways and the hopping response in the rabbit. Behav Brain Res 51:217–221
Holstege G (1987a) Some anatomical observations on the projections from the hypothalamus to brainstem and spinal cord: an HRP and autoradiographic tracing study in the cat. J Comp Neurol 260:98–126
Holstege G (1987b) Anatomical evidence for an ipsilateral rubrospinal pathway and for direct rubrospinal projections to motoneurons in the cat. Neurosci Lett 74:269–274
Holstege JC (1991) Ultrastructural evidence for GABAergic brain stem projections to spinal motoneurons in the rat. J Neurosci 11:159–167
Holstege G, Tan J (1987) Supraspinal control of motoneurons innervating the striated muscles of the pelvic floor including urethral and anal sphincters in the cat. Brain 110:1323–1344
Holstege G, Tan J (1988) Projections from the red nucleus and surrounding areas to the brainstem and spinal cord in the cat. An HRP and autoradiographical tracing study. Behav Brain Res 28:33–57
Huerta MF, Harting JK (1982) Projections of the superior colliculus to the supraspinal nucleus and the cervical spinal cord gray of the cat. Brain Res 242:326–331
Huisman AM, Kuypers HGJM, Verburgh CA (1982) Differences in collateralization of the descending spinal pathways from red nucleus and other brain-stem cell groups in cat and monkey. Prog Brain Res 57:185–217
Jean A (1972) Localization and activity of medullary swallowing neurones. J Physiol 64:227–268
Kausz M (1991) Arrangement of neurons in the medullary reticular formation and raphe nuclei projecting to thoracic, lumbar and sacral segments of the spinal cord in the cat. Anat Embryol 183:151–163
Kc P, Haxhiu MA, Tolentino-Silva FP, Wu M, Trouth CO, Mack SO (2002) Paraventricular vasopressin-containing neurons project to brain stem and spinal cord respiratory-related sites. Respir Physiol Neurobiol 133:75–88
Kimmel CB, Powell SL, Metcalfe WK (1982) Brain neurons which project to the spinal cord in young larvae of the zebrafish. J Comp Neurol 205:112–127
Kitao Y, Okoyama S, Moriizumi T, Kudo M (1993) Neurogenetical segregation of the vestibulospinal neurons in the rat. Brain Res 620:149–154
Kneisley LW, Biber MP, Lavail JH (1978) Study of origin of brain-stem projections to monkey spinal-cord using retrograde transport method. Exp Neurol 60:116–139
Kuchler M, Fouad K, Weinmann O, Schwab ME, Raineteau O (2002) Red nucleus projections to distinct motor neuron pools in the rat spinal cord. J Comp Neurol 448:349–359
Kudo N, Furukawa F, Okado N (1993) Development of descending fibers to the rat embryonic spinal-cord. Neurosci Res 16:131–141
Kunzle H (1992) Meso-diencephalic regions projecting to spinal cord and dorsal column nuclear complex in the hedgehog-tenrec, Echinops telfairi. Anat Embryol 185:57–68
Kuypers HG, Maisky VA (1975) Retrograde axonal transport of horseradish peroxidase from spinal cord to brain stem cell groups in the cat. Neurosci Lett 1:9–14
Kuypers HG, Fleming WR, Farinholt JW (1962) Subcorticospinal projections in the rhesus monkey. J Comp Neurol 118:107–137
Lakke EA (1997) The projections to the spinal cord of the rat during development: a timetable of descent. Adv Anat Embryol Cell Biol 135:1–143 (I–XIV)
Lan CT, Wu WC, Ling EA, Chai CY (1997) Evidence of a direct projection from the cardiovascular-reactive dorsal medulla to the intermediolateral cell column of the spinal cord in cats as revealed by light and electron microscopy. Neuroscience 77:521–533
Leichnetz GR, Watkins L, Griffin G, Murfin R, Mayer DJ (1978) Projection from nucleus raphe magnus and other brain-stem nuclei to spinal-cord in rat—study using HRP blue-reaction. Neurosci Lett 8:119–124
Leite-Almeida H, Valle-Fernandes A, Almeida A (2006) Brain projections from the medullary dorsal reticular nucleus: an anterograde and retrograde tracing study in the rat. Neuroscience 140:577–595
Leong SK, Shieh JY, Wong WC (1984) Localizing spinal-cord-projecting neurons in adult albino rats. J Comp Neurol 228:1–17
Li XG, Florence SL, Kaas JH (1990) Areal distributions of cortical neurons projecting to different levels of the caudal brain stem and spinal cord in rats. Somatosens Mot Res 7:315–335
Loewy AD, Burton H (1978) Nuclei of the solitary tract: efferent projections to the lower brain stem and spinal cord of the cat. J Comp Neurol 181:421–449
Mantyh PW (1983) Connections of midbrain periaqueductal gray in the monkey. II. Descending efferent projections. J Neurophysiol 49:582–594
Marini G, Pianca L, Tredici G (1999) Descending projections arising from the parafascicular nucleus in rats: trajectory of fibers, projection pattern and mapping of terminations. Somatosens Mot Res 16:207–222
Martin GF (1969) Efferent tectal pathways of opossum—(Didelphis Virginiana). J Comp Neurol 135:209–224
Martin GF, Dom R (1970) The rubro-spinal tract of the opposum (Didelphis virginiana). J Comp Neurol 138:19–30
Martin GF, Cabana T, DiTirro FJ, Ho RH, Humbertson AO (1982) Reticular and raphe projections to the spinal cord of the North American opossum. Evidence for connectional heterogeneity. Prog Brain Res 57:109–129
Masino T, Knudsen EI (1992) Anatomical pathways from the optic tectum to the spinal cord subserving orienting movements in the barn owl. Exp Brain Res 92:194–208
Masson RL, Sparkes ML, Ritz LA (1991) Descending projections to the rat sacrocaudal spinal cord. J Comp Neurol 307:120–130
Matsushita M, Okado N, Ikeda M, Hosoya Y (1981) Descending projections from the spinal and mesencephalic nuclei of the trigeminal nerve to the spinal-cord in the cat—a study with the horseradish-peroxidase technique. J Comp Neurol 196:173–187
Mesulam MM (1978) Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. J Histochem Cytochem 26:106–117
Metcalfe WK, Mendelson B, Kimmel CB (1986) Segmental homologies among reticulospinal neurons in the hindbrain of the zebrafish larva. J Comp Neurol 251:147–159
Michaloudi H, Dinopoulos A, Karamanlidis AN, Papadopoulos NC, Antonopoulos J (1988) Cortical and brain-stem projections to the spinal-cord of the hedgehog (Erinaceus europaeus)—a horseradish-peroxidase study. Anat Embryol 178:259–270
Miller MW (1987) The origin of corticospinal projection neurons in rat. Exp Brain Res 67:339–351
Miller RA, Strominger NL (1973) Efferent connections of the red nucleus in the brainstem and spinal cord of the rhesus monkey. J Comp Neurol 152:327–345
Mizuno N, Takahashi O, Satoda T, Matsushima R (1985) Amygdalospinal projections in the macaque monkey. Neurosci Lett 53:327–330
Mokha SS, Iggo A (1987) Mechanisms mediating the brain stem control of somatosensory transmission in the dorsal horn of the cat’s spinal cord: an intracellular analysis. Exp Brain Res 69:93–106
Mtui EP, Anwar M, Gomez R, Reis DJ, Ruggiero DA (1993) Projections from the nucleus tractus solitarii to the spinal cord. J Comp Neurol 337:231–252
Mtui EP, Anwar M, Reis DJ, Ruggiero DA (1995) Medullary visceral reflex circuits: local afferents to nucleus tractus solitarii synthesize catecholamines and project to thoracic spinal cord. J Comp Neurol 351:5–26
New JG, Snyder BD, Woodson KL (1998) Descending neural projections to the spinal cord in the channel catfish, Ictalurus punctatus. Anat Rec 252:235–253
Newman DB, Cruce WL, Bruce LL (1983) The sources of supraspinal afferents to the spinal cord in a variety of limbed reptiles. I. Reticulospinal systems. J Comp Neurol 215:17–32
Nordlander RH, Baden ST, Ryba TMJ (1985) Development of early brain-stem projections to the tail spinal-cord of Xenopus. J Comp Neurol 231:519–529
Nudo RJ, Masterton RB (1988) Descending pathways to the spinal-cord—a comparative study of 22 mammals. J Comp Neurol 277:53–79
Nudo RJ, Masterton RB (1989) Descending pathways to the spinal cord: II. Quantitative study of the tectospinal tract in 23 mammals. J Comp Neurol 286:96–119
Nudo RJ, Masterton RB (1990) Descending pathways to the spinal cord, III: sites of origin of the corticospinal tract. J Comp Neurol 296:559–583
Nyberg-Hansen R (1964a) The location and termination of tectospinal fibers in the cat. Exp Neurol 9:212–227
Nyberg-Hansen R (1964b) Origin and termination of fibers from the vestibular nuclei descending in the medial longitudinal fasciculus. An experimental study with silver impregnation methods in the cat. J Comp Neurol 122:355–367
Nyberg-Hansen R (1965) Sites and mode of termination of reticulo-spinal fibers in the cat. An experimental study with silver impregnation methods. J Comp Neurol 124:71–99
Nyberg-Hansen R, Brodal A (1964) Sites and mode of termination of rubrospinal fibres in the cat. An experimental study with silver impregnation methods. J Anat 98:235–253
Ogawa H, Imoto T, Hayama T (1984) Responsiveness of solitario-parabrachial relay neurons to taste and mechanical stimulation applied to the oral cavity in rats. Exp Brain Res 54:349–358
Oka Y, Satou M, Ueda K (1986) Descending pathways to the spinal-cord in the hime salmon (landlocked red salmon, Oncorhynchus nerka). J Comp Neurol 254:91–103
Okado N, Oppenheim RW (1985) The onset and development of descending pathways to the spinal-cord in the chick-embryo. J Comp Neurol 232:143–161
Olivier E, Chat M, Grantyn A (1991) Rostrocaudal and lateromedial density distributions of superior colliculus neurons projecting in the predorsal bundle and to the spinal cord: a retrograde HRP study in the cat. Exp Brain Res 87:268–282
Pantaleo T, Corda M (1986) Respiration-related neurons in the medial nuclear complex of the solitary tract of the cat. Respir Physiol 64:135–148
Paxinos G, Butcher LL (1985) Organizational principles of the brain as revealed by choline acetyltransferase and acetylcholinesterase distribution and projections. In: Paxinos G (ed) The rat nervous system, 1st edn. Elsevier Academic Press, San Diego, pp 487–521
Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates, 2nd edn. Elsevier Academic Press, San Diego
Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates. Elsevier Academic Press, San Diego
Peterson BW, Coulter JD (1977) A new long spinal projection from the vestibular nuclei in the cat. Brain Res 122:351–356
Peterson BW, Maunz RA, Pitts NG, Mackel RG (1975) Patterns of projection and braching of reticulospinal neurons. Exp Brain Res 23:333–351
Peterson BW, Maunz RA, Fukushima K (1978) Properties of a new vestibulospinal projection, the caudal vestibulospinal tract. Exp Brain Res 32:287–292
Phelan KD, Falls WM (1991) A comparison of the distribution and morphology of thalamic, cerebellar and spinal projection neurons in rat trigeminal nucleus interpolaris. Neuroscience 40:497–511
Poirier LJ, Bouvier G (1966) Red nucleus and its efferent nervous pathways in monkey. J Comp Neurol 128:223–243
Pompeiano O, Brodal A (1957) Experimental demonstration of a somatotopical origin of rubrospinal fibers in the cat. J Comp Neurol 108:225–251
Prasada Rao PD, Jadhao AG, Sharma SC (1987) Descending projection neurons to the spinal cord of the goldfish, Carassius auratus. J Comp Neurol 265:96–108
Puelles L, Martinez-de-la-Torre M, Paxinos G, Watson C, Martínez S (2007) The chick brain in stereotaxic coordinates. Elsevier Academic Press, New York, p 41
Radulovacki M, Pavlovic S, Saponjic J, Carley DW (2003) Intertrigeminal region attenuates reflex apnea and stabilizes respiratory pattern in rats. Brain Res 975:66–72
Rao PD, Jadhao AG, Sharma SC (1993) Topographic organization of descending projection neurons to the spinal cord of the goldfish, Carassius auratus. Brain Res 620:211–220
Rathelot JA, Strick PL (2006) Muscle representation in the macaque motor cortex: an anatomical perspective. Proc Natl Acad Sci 103:8257–8262
Reed WR, Shum-Siu A, Magnuson DS (2008) Reticulospinal pathways in the ventrolateral funiculus with terminations in the cervical and lumbar enlargements of the adult rat spinal cord. Neuroscience 151:505–517
Rikard-Bell GC, Bystrzycka EK, Nail BS (1984) Brainstem projections to the phrenic nucleus: a HRP study in the cat. Brain Res Bull 12:469–477
Ruggiero DA, Ross CA, Reis DJ (1981) Projections from the spinal trigeminal nucleus to the entire length of the spinal cord in the rat. Brain Res 225:225–233
Russo A, Monaco S, Romeo R, Pellitteri R, Stanzani S (2004) Serotonergic collateralized projections from Barrington’s nucleus to the medial preoptic area and lumbo-sacral spinal cord. Brain Res 1019:64–67
Russo A, Pellitteri R, Romeo R, Stanzani S, Jean A (2005) Branching projections of ventrolateral reticular neurons to the medial preoptic area and lumbo-sacral spinal cord. Behav Brain Funct 1:17
Sanchez-Camacho C, Marin O, ten Donkelaar HJ, Gonzalez A (2001a) Descending supraspinal pathways in amphibians. I. A dextran amine tracing study of their cells of origin. J Comp Neurol 434:186–208
Sanchez-Camacho C, Marin O, Smeets WJ, ten Donkelaar HJ, Gonzalez A (2001b) Descending supraspinal pathways in amphibians. II. Distribution and origin of the catecholaminergic innervation of the spinal cord. J Comp Neurol 434:209–232
Sanchez-Camacho C, Martin O, ten Donkelaar HJ, Gonzalez A (2002) Descending supraspinal pathways in amphibians: III. Development of descending projections to the spinal cord in Xenopus laevis with emphasis on the catecholaminergic inputs. J Comp Neurol 446:11–24
Sandrew BB, Edwards DL, Poletti CE, Foote WE (1986) Amygdalospinal projections in the cat. Brain Res 373:235–239
Sato H, Endo K, Ikegami H, Imagawa M, Sasaki M, Uchino Y (1996) Properties of utricular nerve-activated vestibulospinal neurons in cats. Exp Brain Res 112:197–202
Sato H, Imagawa M, Isu N, Uchino Y (1997) Properties of saccular nerve-activated vestibulospinal neurons in cats. Exp Brain Res 116:381–388
Satoda T, Matsumoto H, Zhou L, Rose PK, Richmond FJ (2002) Mesencephalic projections to the first cervical segment in the cat. Exp Brain Res 144:397–413
Sawchenko PE, Swanson LW (1982) Immunohistochemical identification of neurons in the paraventricular nucleus of the hypothalamus that project to the medulla or to the spinal cord in the rat. J Comp Neurol 205:260–272
Sbriccoli A, Santarelli M, Carretta D, Pinto F, Granato F, Minciacchi D (1995) Architectural changes of the cortico-spinal system in the dystrophin defective mdx mouse. Neurosci Lett 200:53–56
Schwanzel-Fukuda M, Morrell JI, Pfaff DW (1984) Localization of forebrain neurons which project directly to the medulla and spinal cord of the rat by retrograde tracing with wheat germ agglutinin. J Comp Neurol 226:1–20
Shen P, Arnold AP, Micevych PE (1990) Supraspinal projections to the ventromedial lumbar spinal cord in adult male rats. J Comp Neurol 300:263–272
Shieh JY, Leong SK, Wong WC (1983) Origin of the rubrospinal tract in neonatal, developing, and mature rats. J Comp Neurol 214:79–86
Sirkin DW, Feng AS (1987) Autoradiographic study of descending pathways from the pontine reticular formation and the mesencephalic trigeminal nucleus in the rat. J Comp Neurol 256:483–493
Smeets WJ, Timerick SJ (1981) Cells of origin of pathways descending to the spinal cord in two chondrichthyans, the shark Scyliorhinus canicula and the ray Raja clavata. J Comp Neurol 202:473–491
Smith JC, Morrison DE, Ellenberger HH, Otto MR, Feldman JL (1989) Brainstem projections to the major respiratory neuron populations in the medulla of the cat. J Comp Neurol 281:69–96
Song G, Yu Y, Poon CS (2006) Cytoarchitecture of pneumotaxic integration of respiratory and nonrespiratory information in the rat. J Neurosci 26:300–310
Stockx EM, Anderson CR, Murphy SM, Cooke IR, Berger PJ (2007) The development of descending projections from the brainstem to the spinal cord in the fetal sheep. BMC Neurosci 8:40
Swanson LW (1998) Brain maps: structure of the rat brain, 2nd edn. Elsevier Academic Press, New York
Takada M (1993) Widespread dopaminergic projections of the subparafascicular thalamic nucleus in the rat. Brain Res Bull 32:301–309
ten Donkelaar HJ (1976) Descending pathways from the brain stem to the spinal cord in some reptiles. I. Origin. J Comp Neurol 167:421–442
ten Donkelaar HJ, de Boer-van Huizen R (1982) Observations on the development of descending pathways from the brain stem to the spinal cord in the clawed toad Xenopus laevis. Anat Embryol 163:461–473
ten Donkelaar HJ, de Boer-van Huizen R, Schouten FT, Eggen SJ (1981) Cells of origin of descending pathways to the spinal cord in the clawed toad (Xenopus laevis). Neuroscience 6:2297–2312
Torvik A, Brodal A (1957) The origin of reticulospinal fibers in the cat—an experimental study. Anat Rec 128:113–137
Tracey D (2004) Ascending and descending tracts in the spinal cord. In: Paxinos G (ed) The rat nervous system, 3rd edn. Elsevier Academic Press, San Diego, pp 149–164
Tsukamoto Y, Yamamoto T, Okado H, Nibu K, Terashima T (2003) Retrograde labeling of mouse spinal descending tracts by a recombinant adenovirus. Arch Histol Cytol 66:209–220
van Mier P, ten Donkelaar HJ (1984) Early development of descending pathways from the brain stem to the spinal cord in Xenopus laevis. Anat Embryol 170:295–306
Vanderhorst VG (2005) Nucleus retroambiguus-spinal pathway in the mouse: localization, gender differences, and effects of estrogen treatment. J Comp Neurol 488:180–200
VanderHorst VG, Ulfhake B (2006) The organization of the brainstem and spinal cord of the mouse: relationships between monoaminergic, cholinergic, and spinal projection systems. J Chem Neuroanat 31:2–36
Wada N, Sugita S, Jouzaki A, Tokuriki M (1993) Descending projections to coccygeal spinal segments in the cat. J Anat 182:259–265
Warner G, Watson CR (1972) The rubrospinal tract in a diprotodont marsupial (Trichosurus vulpecula). Brain Res 41:180–183
Warren S, Waitzman DM, May PJ (2008) Anatomical evidence for interconnections between the central mesencephalic reticular formation and cervical spinal cord in the cat and macaque. Anat Rec 291:141–160
Watson C, Harvey AR (2009) Projections from the brain to the spinal cord. In: Watson C, Paxinos G, Kayalioglu G (eds) The spinal cord. Elsevier Academic Press, San Diego, pp 168–171
Webster DM, Steeves JD (1988) Origins of brainstem-spinal projections in the duck and goose. J Comp Neurol 273:573–583
Webster DM, Steeves JD (1991) Funicular organization of avian brainstem-spinal projections. J Comp Neurol 312:467–476
Wild JM, Cabot JB, Cohen DH, Karten HJ (1979) Origin, course and terminations of the rubrospinal tract in the pigeon (Columba livia). J Comp Neurol 187:639–654
Xu XM, Martin GF (1989) Developmental plasticity of the rubrospinal tract in the North American opossum. J Comp Neurol 279:368–381
Zemlan FP, Pfaff DW (1979) Topographical organization in medullary reticulospinal systems as demonstrated by the horseradish peroxidase technique. Brain Res 174:161–166
Acknowledgments
We thank Professor Gulgun Kayalioglu, Dr Yuhong Fu, Dr Yue Qi, and Dr Erika Gyengesi for their helpful suggestions, and we thank Mr Peter Zhao for technical support. This work was supported by the Christopher and Dana Reeve Foundation and an Australia Fellowship awarded to Professor George Paxinos by the National Health and Medical Research Council (NHMRC) (466028).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Liang, H., Paxinos, G. & Watson, C. Projections from the brain to the spinal cord in the mouse. Brain Struct Funct 215, 159–186 (2011). https://doi.org/10.1007/s00429-010-0281-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-010-0281-x