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Published in: Brain Structure and Function 1/2014

01-01-2014 | Original Article

Musculotopic organization of the motor neurons supplying the mouse hindlimb muscles: a quantitative study using Fluoro-Gold retrograde tracing

Authors: Tímea Bácskai, Zoltán Rusznák, George Paxinos, Charles Watson

Published in: Brain Structure and Function | Issue 1/2014

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Abstract

We have mapped the motor neurons (MNs) supplying the major hindlimb muscles of transgenic (C57/BL6J-ChAT-EGFP) and wild-type (C57/BL6J) mice. The fluorescent retrograde tracer Fluoro-Gold was injected into 19 hindlimb muscles. Consecutive transverse spinal cord sections were harvested, the MNs counted, and the MN columns reconstructed in 3D. Three longitudinal MN columns were identified. The dorsolateral column extends from L4 to L6 and consists of MNs innervating the crural muscles and the foot. The ventrolateral column extends from L1 to L6 and accommodates MNs supplying the iliopsoas, gluteal, and quadriceps femoris muscles. The middle part of the ventral horn hosts the central MN column, which extends between L2 and L6 and consists of MNs for the thigh adductor, hamstring, and quadratus femoris muscles. Within these longitudinal columns, the arrangement of the different MN groups reflects their somatotopic organization. MNs innervating muscles developing from the dorsal (e.g., quadriceps) and ventral muscle mass (e.g., hamstring) are situated in the lateral and medial part of the ventral gray, respectively. MN pools belonging to proximal muscles (e.g., quadratus femoris and iliopsoas) are situated ventral to those supplying more distal ones (e.g., plantar muscles). Finally, MNs innervating flexors (e.g., posterior crural muscles) are more medial than those belonging to extensors of the same joint (e.g., anterior crural muscles). These data extend and modify the MN maps in the recently published atlas of the mouse spinal cord and may help when assessing neuronal loss associated with MN diseases.
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Literature
go back to reference Abercrombie M (1946) Estimation of nuclear population from microtome sections. Anat Rec 94:239–247PubMedCrossRef Abercrombie M (1946) Estimation of nuclear population from microtome sections. Anat Rec 94:239–247PubMedCrossRef
go back to reference Ashwell KW, Watson CRR (1983) The development of facial motoneurons in the mouse—neuronal death and the innervation of the facial muscles. J Embryol Exp Morphol 77:117–141PubMed Ashwell KW, Watson CRR (1983) The development of facial motoneurons in the mouse—neuronal death and the innervation of the facial muscles. J Embryol Exp Morphol 77:117–141PubMed
go back to reference Azzouz M, Ralph GS, Storkebaum E, Walmsley LE, Mitrophanous KA, Kingsman SM, Carmeliet P, Mazarakis ND (2004) VEGF delivery with retrogradely transported lentivector prolongs survival in a mouse ALS model. Nature 429:413–417PubMedCrossRef Azzouz M, Ralph GS, Storkebaum E, Walmsley LE, Mitrophanous KA, Kingsman SM, Carmeliet P, Mazarakis ND (2004) VEGF delivery with retrogradely transported lentivector prolongs survival in a mouse ALS model. Nature 429:413–417PubMedCrossRef
go back to reference Bachurin SO, Shelkovnikova TA, Ustyugov AA, Peters O, Khritankova I, Afanasieva MA, Tarasova TV, Alentov II, Buchman VL, Ninkina NN (2011) Dimebon slows progression of proteinopathy in γ-synuclein transgenic mice. Neurotox Res 22:33–42PubMedCentralPubMedCrossRef Bachurin SO, Shelkovnikova TA, Ustyugov AA, Peters O, Khritankova I, Afanasieva MA, Tarasova TV, Alentov II, Buchman VL, Ninkina NN (2011) Dimebon slows progression of proteinopathy in γ-synuclein transgenic mice. Neurotox Res 22:33–42PubMedCentralPubMedCrossRef
go back to reference Bácskai T, Fu Y, Sengul G, Rusznák Z, Paxinos G, Watson C (2012) Musculotopic organization of the motor neurons supplying forelimb and shoulder girdle muscles in the mouse. Brain Struct Funct (Epub ahead of print) Bácskai T, Fu Y, Sengul G, Rusznák Z, Paxinos G, Watson C (2012) Musculotopic organization of the motor neurons supplying forelimb and shoulder girdle muscles in the mouse. Brain Struct Funct (Epub ahead of print)
go back to reference Bensimon G, Lacomblez L, Meininger V, ALS/Riluzole Study Group (1994) A controlled trial of riluzole in amyotrophic lateral sclerosis. N Engl J Med 330:585–591PubMedCrossRef Bensimon G, Lacomblez L, Meininger V, ALS/Riluzole Study Group (1994) A controlled trial of riluzole in amyotrophic lateral sclerosis. N Engl J Med 330:585–591PubMedCrossRef
go back to reference Boillée S, Vande Velde C, Cleveland DW (2006) ALS: a disease of motor neurons and their nonneuronal neighbors. Neuron 52:39–59PubMedCrossRef Boillée S, Vande Velde C, Cleveland DW (2006) ALS: a disease of motor neurons and their nonneuronal neighbors. Neuron 52:39–59PubMedCrossRef
go back to reference Chi L, Ke Y, Luo C, Li B, Gozal D, Kalyanaraman B, Liu R (2006) Motor neuron degeneration promotes neural progenitor cell proliferation, migration, and neurogenesis in the spinal cords of amyotrophic lateral sclerosis mice. Stem Cells 24:34–43PubMedCentralPubMedCrossRef Chi L, Ke Y, Luo C, Li B, Gozal D, Kalyanaraman B, Liu R (2006) Motor neuron degeneration promotes neural progenitor cell proliferation, migration, and neurogenesis in the spinal cords of amyotrophic lateral sclerosis mice. Stem Cells 24:34–43PubMedCentralPubMedCrossRef
go back to reference Crouch JE (1969) Text-atlas of cat anatomy. Lea and Febiger, Philadelphia Crouch JE (1969) Text-atlas of cat anatomy. Lea and Febiger, Philadelphia
go back to reference Cudkowicz M, Bozik ME, Ingersoll EW, Miller R, Mitsumoto H, Shefner J, Moore DH, Schoenfeld D, Mather JL, Archibald D, Sullivan M, Amburgey C, Moritz J, Gribkoff VK (2011) The effects of dexpramipexole (KNS-760704) in individuals with amyotrophic lateral sclerosis. Nat Med 17:1652–1656PubMedCrossRef Cudkowicz M, Bozik ME, Ingersoll EW, Miller R, Mitsumoto H, Shefner J, Moore DH, Schoenfeld D, Mather JL, Archibald D, Sullivan M, Amburgey C, Moritz J, Gribkoff VK (2011) The effects of dexpramipexole (KNS-760704) in individuals with amyotrophic lateral sclerosis. Nat Med 17:1652–1656PubMedCrossRef
go back to reference de Hemptinne I, Boucherie C, Pochet R, Bantubungi K, Schiffmann SN, Maloteaux JM, Hermans E (2006) Unilateral induction of progenitors in the spinal cord of hSOD1 (G93A) transgenic rats correlates with an asymmetrical hind limb paralysis. Neurosci Lett 401:25–29PubMedCrossRef de Hemptinne I, Boucherie C, Pochet R, Bantubungi K, Schiffmann SN, Maloteaux JM, Hermans E (2006) Unilateral induction of progenitors in the spinal cord of hSOD1 (G93A) transgenic rats correlates with an asymmetrical hind limb paralysis. Neurosci Lett 401:25–29PubMedCrossRef
go back to reference Emsley JG, Lu X, Hagg T (2001) Retrograde tracing techniques influence reported cell death rates of adult rat nigrostriatial neurons. Exp Neurol 168:425–433PubMedCrossRef Emsley JG, Lu X, Hagg T (2001) Retrograde tracing techniques influence reported cell death rates of adult rat nigrostriatial neurons. Exp Neurol 168:425–433PubMedCrossRef
go back to reference Fischer LR, Culver DG, Tennant P, Davis AA, Wang M, Castellano-Sanchez A, Khan J, Polak MA, Glass JD (2004) Amyotrophic lateral sclerosis is a distal axonopathy: evidence in mice and man. Exp Neurol 185:232–240PubMedCrossRef Fischer LR, Culver DG, Tennant P, Davis AA, Wang M, Castellano-Sanchez A, Khan J, Polak MA, Glass JD (2004) Amyotrophic lateral sclerosis is a distal axonopathy: evidence in mice and man. Exp Neurol 185:232–240PubMedCrossRef
go back to reference Franklin TR, Druhan JP (2000) The retrograde tracer fluoro-gold interferes with the expression of fos-related antigens. J Neurosci Methods 98:1–8PubMedCrossRef Franklin TR, Druhan JP (2000) The retrograde tracer fluoro-gold interferes with the expression of fos-related antigens. J Neurosci Methods 98:1–8PubMedCrossRef
go back to reference Frey D, Schneider C, Xu L, Borg J, Spooren W, Caroni P (2000) Early and selective loss of neuromuscular synapse subtypes with low sprouting competence in motoneuron diseases. J Neurosci 20:2534–2542PubMed Frey D, Schneider C, Xu L, Borg J, Spooren W, Caroni P (2000) Early and selective loss of neuromuscular synapse subtypes with low sprouting competence in motoneuron diseases. J Neurosci 20:2534–2542PubMed
go back to reference Garrett WT, McBride RL, Williams JK, Feringa ER (1991) Fluoro-Gold’s toxicity makes it inferior to True Blue for long-term studies of dorsal root ganglion neurons and motoneurons. Neurosci Lett 128:137–139PubMedCrossRef Garrett WT, McBride RL, Williams JK, Feringa ER (1991) Fluoro-Gold’s toxicity makes it inferior to True Blue for long-term studies of dorsal root ganglion neurons and motoneurons. Neurosci Lett 128:137–139PubMedCrossRef
go back to reference Green EC (1959) Anatomy of the rat. Hafner, New York Green EC (1959) Anatomy of the rat. Hafner, New York
go back to reference Gurney ME, Pu H, Chiu AY, Dal Canto MC, Polchow CY, Alexander DD, Caliendo J, Hentati A, Kwon YW, Deng HX, Zhai P, Sufit RL, Siddique T (1994) Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science 264:1772–1775PubMedCrossRef Gurney ME, Pu H, Chiu AY, Dal Canto MC, Polchow CY, Alexander DD, Caliendo J, Hentati A, Kwon YW, Deng HX, Zhai P, Sufit RL, Siddique T (1994) Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science 264:1772–1775PubMedCrossRef
go back to reference Haenggeli C, Kato AC (2002) Rapid and reproducible methods using fluorogold for labelling a subpopulation of cervical motoneurons: application in the wobbler mouse. J Neurosci Methods 116:119–124PubMedCrossRef Haenggeli C, Kato AC (2002) Rapid and reproducible methods using fluorogold for labelling a subpopulation of cervical motoneurons: application in the wobbler mouse. J Neurosci Methods 116:119–124PubMedCrossRef
go back to reference Hanyu N, Oguchi K, Yanagisawa N, Tsukagoshi H (1982) Degeneration and regeneration of ventral root motor fibers in amyotrophic lateral sclerosis. Morphometric studies of cervical ventral roots. J Neurol Sci 55:99–115PubMedCrossRef Hanyu N, Oguchi K, Yanagisawa N, Tsukagoshi H (1982) Degeneration and regeneration of ventral root motor fibers in amyotrophic lateral sclerosis. Morphometric studies of cervical ventral roots. J Neurol Sci 55:99–115PubMedCrossRef
go back to reference Hebel R, Stromberg MW (1976) Anatomy of the laboratory rat. Williams & Wilkins, Baltimore Hebel R, Stromberg MW (1976) Anatomy of the laboratory rat. Williams & Wilkins, Baltimore
go back to reference Joyce PI, Fratta P, Fisher EMC, Acevedo-Arozena A (2011) SOD1 and TDP-43 animal models of amyotrophic lateral sclerosis: recent advances in understanding disease toward the development of clinical treatments. Mamm Genome 22:420–448PubMedCrossRef Joyce PI, Fratta P, Fisher EMC, Acevedo-Arozena A (2011) SOD1 and TDP-43 animal models of amyotrophic lateral sclerosis: recent advances in understanding disease toward the development of clinical treatments. Mamm Genome 22:420–448PubMedCrossRef
go back to reference Kaiser O (1891) Die Functionen der Ganglienzellen des Halsmarkes. Haag Kaiser O (1891) Die Functionen der Ganglienzellen des Halsmarkes. Haag
go back to reference Kong J, Xu Z (1998) Massive mitochondrial degeneration in motor neurons triggers the onset of amyotrophic lateral sclerosis in mice expressing a mutant SOD1. J Neurosci 18:3241–3250PubMed Kong J, Xu Z (1998) Massive mitochondrial degeneration in motor neurons triggers the onset of amyotrophic lateral sclerosis in mice expressing a mutant SOD1. J Neurosci 18:3241–3250PubMed
go back to reference Kwiatkowski TJ Jr, Bosco DA, Leclerc AL, Tamrazian E, Vanderburg CR, Russ C, Davis A, Gilchrist J, Kasarskis EJ, Munsat T, Valdmanis P, Rouleau GA, Hosler BA, Cortelli P, de Jong PJ, Yoshinaga Y, Haines JL, Pericak-Vance MA, Yan J, Ticozzi N, Siddique T, McKenna-Yasek D, Sapp PC, Horvitz HR, Landers JE, Brown RH Jr (2009) Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science 27:1205–1208CrossRef Kwiatkowski TJ Jr, Bosco DA, Leclerc AL, Tamrazian E, Vanderburg CR, Russ C, Davis A, Gilchrist J, Kasarskis EJ, Munsat T, Valdmanis P, Rouleau GA, Hosler BA, Cortelli P, de Jong PJ, Yoshinaga Y, Haines JL, Pericak-Vance MA, Yan J, Ticozzi N, Siddique T, McKenna-Yasek D, Sapp PC, Horvitz HR, Landers JE, Brown RH Jr (2009) Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science 27:1205–1208CrossRef
go back to reference Lance Jones C (1979) The morphogenesis of the thigh of the mouse with special reference to tetrapod muscle homologies. J Morphol 162:275–310CrossRef Lance Jones C (1979) The morphogenesis of the thigh of the mouse with special reference to tetrapod muscle homologies. J Morphol 162:275–310CrossRef
go back to reference Mackenzie IR, Rademakers R, Neumann M (2010) TDP-43 and FUS in amyotrophic lateral sclerosis and frontotemporal dementia. Lancet Neurol 9:995–1007PubMedCrossRef Mackenzie IR, Rademakers R, Neumann M (2010) TDP-43 and FUS in amyotrophic lateral sclerosis and frontotemporal dementia. Lancet Neurol 9:995–1007PubMedCrossRef
go back to reference McClellan AD, Zhang L, Palmer R (2006) Flurogold labeling of descending brain neurons in larval lamprey does not cause cell death. Neurosci Lett 401:119–124PubMedCrossRef McClellan AD, Zhang L, Palmer R (2006) Flurogold labeling of descending brain neurons in larval lamprey does not cause cell death. Neurosci Lett 401:119–124PubMedCrossRef
go back to reference McHanwell S, Biscoe TJ (1981a) The localization of motor neurons supplying the hindlimb muscles of the mouse. Philos Trans R Soc Lond B Biol Sci 293:477–508PubMedCrossRef McHanwell S, Biscoe TJ (1981a) The localization of motor neurons supplying the hindlimb muscles of the mouse. Philos Trans R Soc Lond B Biol Sci 293:477–508PubMedCrossRef
go back to reference McHanwell S, Biscoe TJ (1981b) The sizes of motoneurons supplying hindlimb muscles in the mouse. Proc R Soc Lond B 213:201–216PubMedCrossRef McHanwell S, Biscoe TJ (1981b) The sizes of motoneurons supplying hindlimb muscles in the mouse. Proc R Soc Lond B 213:201–216PubMedCrossRef
go back to reference McHanwell S, Watson C (2009) Localization of motoneurons in the spinal cord. In: Watson C, Paxinos G, Kayalioglu G (eds) Spinal cord. A Christopher and Dana Reeve Foundation Text and Atlas. Elsevier, San Diego, pp 94–114 McHanwell S, Watson C (2009) Localization of motoneurons in the spinal cord. In: Watson C, Paxinos G, Kayalioglu G (eds) Spinal cord. A Christopher and Dana Reeve Foundation Text and Atlas. Elsevier, San Diego, pp 94–114
go back to reference McLaren A, Michie D (1954) Factors affecting vertebral variation in mice. 1. Variation within an inbred strain. J Embryol Exp Morphol 2:149–160 McLaren A, Michie D (1954) Factors affecting vertebral variation in mice. 1. Variation within an inbred strain. J Embryol Exp Morphol 2:149–160
go back to reference McLaren A, Michie D (1958) Factors affecting vertebral variation in mice. 4. Experimental proof of the uterine basis of a maternal effect. J Embryol Exp Morphol 6:645–659PubMed McLaren A, Michie D (1958) Factors affecting vertebral variation in mice. 4. Experimental proof of the uterine basis of a maternal effect. J Embryol Exp Morphol 6:645–659PubMed
go back to reference Miller TM, Kaspar BK, Kops GJ, Yamanaka K, Christian LJ, Gage FH, Cleveland DW (2005) Virus-delivered small RNA silencing sustains strength in amyotrophic lateral sclerosis. Ann Neurol 57:773–776PubMedCentralPubMedCrossRef Miller TM, Kaspar BK, Kops GJ, Yamanaka K, Christian LJ, Gage FH, Cleveland DW (2005) Virus-delivered small RNA silencing sustains strength in amyotrophic lateral sclerosis. Ann Neurol 57:773–776PubMedCentralPubMedCrossRef
go back to reference Mohajeri MH, Figlewicz DA, Bohn MC (1998) Selective loss of α motoneurons innervating the medial gastrocnemium muscle in a mouse model of amyotrophic lateral sclerosis. Exp Neurol 150:329–336PubMedCrossRef Mohajeri MH, Figlewicz DA, Bohn MC (1998) Selective loss of α motoneurons innervating the medial gastrocnemium muscle in a mouse model of amyotrophic lateral sclerosis. Exp Neurol 150:329–336PubMedCrossRef
go back to reference Nagano I, Ilieva H, Shiote M, Murakami T, Yokoyama M, Shoji M, Abe K (2005a) Therapeutic benefit of intrathecal injection of insulin-like growth factor-1 in a mouse model of amyotrophic lateral sclerosis. J Neurol Sci 235:61–68PubMedCrossRef Nagano I, Ilieva H, Shiote M, Murakami T, Yokoyama M, Shoji M, Abe K (2005a) Therapeutic benefit of intrathecal injection of insulin-like growth factor-1 in a mouse model of amyotrophic lateral sclerosis. J Neurol Sci 235:61–68PubMedCrossRef
go back to reference Nagano I, Shiote M, Murakami T, Kamada H, Hamakawa Y, Matsubara E, Yokoyama M, Moritaz K, Shoji M, Abe K (2005b) Beneficial effects of intrathecal IGF-1 administration in patients with amyotrophic lateral sclerosis. Neurol Res 27:768–772PubMedCrossRef Nagano I, Shiote M, Murakami T, Kamada H, Hamakawa Y, Matsubara E, Yokoyama M, Moritaz K, Shoji M, Abe K (2005b) Beneficial effects of intrathecal IGF-1 administration in patients with amyotrophic lateral sclerosis. Neurol Res 27:768–772PubMedCrossRef
go back to reference Naumann T, Härtig W, Frotscher M (2000) Retrograde tracing with Fluoro-Gold: different methods of tracer detection at the ultrastructural level and neurodegenerative changes of back-filled neurons in long-term studies. J Neurosci Methods 103:11–21PubMedCrossRef Naumann T, Härtig W, Frotscher M (2000) Retrograde tracing with Fluoro-Gold: different methods of tracer detection at the ultrastructural level and neurodegenerative changes of back-filled neurons in long-term studies. J Neurosci Methods 103:11–21PubMedCrossRef
go back to reference Nicolopoulos-Stournas S, Iles JF (1983) Motor neuron columns in the lumbar spinal cord of the rat. J Comp Neurol 217:27–85 Nicolopoulos-Stournas S, Iles JF (1983) Motor neuron columns in the lumbar spinal cord of the rat. J Comp Neurol 217:27–85
go back to reference Orrell RW (2010) Motor neuron disease: systematic reviews of treatment for ALS and SMA. Br Med Bull 93:145–159PubMedCrossRef Orrell RW (2010) Motor neuron disease: systematic reviews of treatment for ALS and SMA. Br Med Bull 93:145–159PubMedCrossRef
go back to reference Portal JJ, Corio M, Viala D (1991) Localization of the lumbar pools of motoneurones which provide hindlimb muscles in the rabbit. Neurosci Lett 124:105–107PubMedCrossRef Portal JJ, Corio M, Viala D (1991) Localization of the lumbar pools of motoneurones which provide hindlimb muscles in the rabbit. Neurosci Lett 124:105–107PubMedCrossRef
go back to reference Pun S, Santos AF, Saxena S, Xu L, Caroni P (2006) Selective vulnerability and pruning of phasic motoneuron axons in motoneuron disease alleviated by CNTF. Nat Neurosci 9:408–419PubMedCrossRef Pun S, Santos AF, Saxena S, Xu L, Caroni P (2006) Selective vulnerability and pruning of phasic motoneuron axons in motoneuron disease alleviated by CNTF. Nat Neurosci 9:408–419PubMedCrossRef
go back to reference Ralph GS, Radcliffe PA, Day DM, Carthy JM, Leroux MA, Lee DC, Wong LF, Bilsland LG, Greensmith L, Kingsman SM, Mitrophanous KA, Mazarakis ND, Azzouz M (2005) Silencing mutant SOD1 using RNAi protects against neurodegeneration and extends survival in an ALS model. Nat Med 11:429–433PubMedCrossRef Ralph GS, Radcliffe PA, Day DM, Carthy JM, Leroux MA, Lee DC, Wong LF, Bilsland LG, Greensmith L, Kingsman SM, Mitrophanous KA, Mazarakis ND, Azzouz M (2005) Silencing mutant SOD1 using RNAi protects against neurodegeneration and extends survival in an ALS model. Nat Med 11:429–433PubMedCrossRef
go back to reference Rigaud M, Gemes G, Barabas ME, Chernoff DI, Abram SE, Stucky CL, Hogan QH (2008) Species and strain differences in rodent sciatic nerve anatomy: implications for studies of neuropathic pain. Pain 136:188–201PubMedCentralPubMedCrossRef Rigaud M, Gemes G, Barabas ME, Chernoff DI, Abram SE, Stucky CL, Hogan QH (2008) Species and strain differences in rodent sciatic nerve anatomy: implications for studies of neuropathic pain. Pain 136:188–201PubMedCentralPubMedCrossRef
go back to reference Romanes GJ (1941) The development and significance of the cell columns in the ventral horn of the cervical and upper thoracic spinal cord of the rabbit. J Anat 76:112–130PubMed Romanes GJ (1941) The development and significance of the cell columns in the ventral horn of the cervical and upper thoracic spinal cord of the rabbit. J Anat 76:112–130PubMed
go back to reference Romanes GJ (1951) The motor cell columns of the lumbosacral spinal cord of the cat. J Comp Neurol 94:313–363PubMedCrossRef Romanes GJ (1951) The motor cell columns of the lumbosacral spinal cord of the cat. J Comp Neurol 94:313–363PubMedCrossRef
go back to reference Romanes GJ (1964) The motor pools of the spinal cord. Progr Brain Res 11:93–119CrossRef Romanes GJ (1964) The motor pools of the spinal cord. Progr Brain Res 11:93–119CrossRef
go back to reference Routal RV, Pal GP (1999) A study of motoneurone groups and motor columns of the human spinal cord. J Anat 195:211–234PubMedCrossRef Routal RV, Pal GP (1999) A study of motoneurone groups and motor columns of the human spinal cord. J Anat 195:211–234PubMedCrossRef
go back to reference Ryan JM, Cushman J, Jordan B, Samuels A, Frazer H, Baier C (1998) Topographic position of forelimb motoneuron pools is conserved in vertebrate evolution. Brain Behav Evol 51:90–99PubMedCrossRef Ryan JM, Cushman J, Jordan B, Samuels A, Frazer H, Baier C (1998) Topographic position of forelimb motoneuron pools is conserved in vertebrate evolution. Brain Behav Evol 51:90–99PubMedCrossRef
go back to reference Sasabe J, Miyoshib Y, Suzuki M, Mita M, Konno R, Matsuoka M, Hamase K, Aiso S (2012) D-Amino acid oxidase controls motoneuron degeneration through d-serine. Proc Natl Acad Sci USA 109:627–632PubMedCrossRef Sasabe J, Miyoshib Y, Suzuki M, Mita M, Konno R, Matsuoka M, Hamase K, Aiso S (2012) D-Amino acid oxidase controls motoneuron degeneration through d-serine. Proc Natl Acad Sci USA 109:627–632PubMedCrossRef
go back to reference Schmued LC, Fallon JH (1986) Fluoro-Gold: a new fluorescent retrograde axonal tracer with numerous unique properties. Brain Res 377:147–154PubMedCrossRef Schmued LC, Fallon JH (1986) Fluoro-Gold: a new fluorescent retrograde axonal tracer with numerous unique properties. Brain Res 377:147–154PubMedCrossRef
go back to reference Sengul G, Tanaka I, Paxinos G, Watson C (2012) Atlas of spinal cords of the rat, mouse, marmoset, macaque, and human. Elsevier Academic Press, San Diego Sengul G, Tanaka I, Paxinos G, Watson C (2012) Atlas of spinal cords of the rat, mouse, marmoset, macaque, and human. Elsevier Academic Press, San Diego
go back to reference Sherrington CS (1910) Flexion-reflex of the limb, crossed extension-reflex, and reflex stepping and standing. J Physiol 40:28–121PubMed Sherrington CS (1910) Flexion-reflex of the limb, crossed extension-reflex, and reflex stepping and standing. J Physiol 40:28–121PubMed
go back to reference Sobue G, Hashizume Y, Mitsuma T, Takahashi A (1987) Size-dependent myelinated fiber loss in the corticospinal tract in Shy–Drager syndrome and amyotrophic lateral sclerosis. Neurology 37:529–532PubMedCrossRef Sobue G, Hashizume Y, Mitsuma T, Takahashi A (1987) Size-dependent myelinated fiber loss in the corticospinal tract in Shy–Drager syndrome and amyotrophic lateral sclerosis. Neurology 37:529–532PubMedCrossRef
go back to reference Traynor BJ, Brujin L, Conwit R, Beal F, O’Neill G, Fagan SC, Cudkowicz ME (2006) Neuroprotective agents for clinical trials in ALS: a systematic assessment. Neurology 67:20–27PubMedCrossRef Traynor BJ, Brujin L, Conwit R, Beal F, O’Neill G, Fagan SC, Cudkowicz ME (2006) Neuroprotective agents for clinical trials in ALS: a systematic assessment. Neurology 67:20–27PubMedCrossRef
go back to reference Vanderhorst VGJM, Holstege G (1997) Organization of lumbosacral motoneuronal cell groups innervating hindlimb, pelvic floor, and axial muscles in the cat. J Comp Neurol 382:46–76PubMedCrossRef Vanderhorst VGJM, Holstege G (1997) Organization of lumbosacral motoneuronal cell groups innervating hindlimb, pelvic floor, and axial muscles in the cat. J Comp Neurol 382:46–76PubMedCrossRef
go back to reference Waldeyer W (1888) Das Gorilla-Rückenmark. Abh der Königlichen Akad der Wissensch Berlin Phys-Math Classe, Abh III:1–147 Waldeyer W (1888) Das Gorilla-Rückenmark. Abh der Königlichen Akad der Wissensch Berlin Phys-Math Classe, Abh III:1–147
go back to reference Watson CRR, Sakai S, Armstrong W (1982) The organization of the facial nucleus in the rat. Brain Behav Evol 20:19–28PubMedCrossRef Watson CRR, Sakai S, Armstrong W (1982) The organization of the facial nucleus in the rat. Brain Behav Evol 20:19–28PubMedCrossRef
go back to reference Watson C, Paxinos G, Kayalioglu G, Heise C (2009a) Atlas of the mouse spinal cord. In: Watson C, Paxinos G, Kayalioglu G (eds) Spinal cord. A Christopher and Dana Reeve Foundation Text and Atlas. Elsevier, San Diego, pp 308–379 Watson C, Paxinos G, Kayalioglu G, Heise C (2009a) Atlas of the mouse spinal cord. In: Watson C, Paxinos G, Kayalioglu G (eds) Spinal cord. A Christopher and Dana Reeve Foundation Text and Atlas. Elsevier, San Diego, pp 308–379
go back to reference Watson C, Paxinos G, Kayalioglu G, Heise C (2009b) Atlas of the rat spinal cord. In: Watson C, Paxinos G, Kayalioglu G (eds) Spinal cord. A Christopher and Dana Reeve Foundation Text and Atlas. Elsevier, San Diego, pp 238–306 Watson C, Paxinos G, Kayalioglu G, Heise C (2009b) Atlas of the rat spinal cord. In: Watson C, Paxinos G, Kayalioglu G (eds) Spinal cord. A Christopher and Dana Reeve Foundation Text and Atlas. Elsevier, San Diego, pp 238–306
go back to reference Wiedau-Pazos M, Goto JJ, Rabizadeh S, Gralla EB, Roe JA, Lee MK, Valentine JS, Bredesen DE (1996) Altered reactivity of superoxide dismutase in familial amyotrophic lateral sclerosis. Science 271:515–518PubMedCrossRef Wiedau-Pazos M, Goto JJ, Rabizadeh S, Gralla EB, Roe JA, Lee MK, Valentine JS, Bredesen DE (1996) Altered reactivity of superoxide dismutase in familial amyotrophic lateral sclerosis. Science 271:515–518PubMedCrossRef
go back to reference Yan J, Aizawa Y, Hitomi J (2007) Localization of motoneurons that extend axons through the ventral rami of cervical nerves to innervate the trapezius muscle: a study using fluorescent dyes and 3D reconstruction method. Clin Anat 20:41–47PubMedCrossRef Yan J, Aizawa Y, Hitomi J (2007) Localization of motoneurons that extend axons through the ventral rami of cervical nerves to innervate the trapezius muscle: a study using fluorescent dyes and 3D reconstruction method. Clin Anat 20:41–47PubMedCrossRef
Metadata
Title
Musculotopic organization of the motor neurons supplying the mouse hindlimb muscles: a quantitative study using Fluoro-Gold retrograde tracing
Authors
Tímea Bácskai
Zoltán Rusznák
George Paxinos
Charles Watson
Publication date
01-01-2014
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 1/2014
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-012-0501-7

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