Neuronal networks within the spinal cord of mammals are responsible for generating various rhythmic movements, such as walking, running, swimming, and scratching. The ability to generate multiple rhythmic movements highlights the complexity and flexibility of the mammalian spinal circuitry. The present review describes features of some rhythmic motor behaviors generated by the mammalian spinal cord and discusses how the spinal circuitry is able to produce different rhythmic movements with their own sets of goals and demands.
ArmstrongDM. 1988. The supraspinal control of mammalian locomotion. J Physiol405:1–37.
2.
ArshavskyYIKotsYMOrlovskyGNRodionovIMShikML. 1965. Biophysics of complex systems and mathematical models. Investigation of the biomechanics of running by the dog. Biophysics10:737–46.
3.
BarbeauHRossignolS. 1987. Recovery of locomotion after chronic spinalization in the adult cat. Brain Res412:84–95.
4.
BarbeauHRossignolS. 1990. The effects of serotonergic drugs on the locomotor pattern and on cutaneous reflexes of the adult chronic spinal cat. Brain Res514:55–67.
5.
BarriereGFrigonALeblondHProvencherJRossignolS. 2010. Dual spinal lesion paradigm in the cat: evolution of the kinematic locomotor pattern. J Neurophysiol104:1119–33.
6.
BergRWAlaburdaAHounsgaardJ. 2007. Balanced inhibition and excitation drive spike activity in spinal half-centers. Science315:390–3.
7.
BerkowitzA. 2007. Spinal interneurons that are selectively activated during fictive flexion reflex. J Neurosci27:4634–41.
8.
BerkowitzA. 2008. Physiology and morphology of shared and specialized spinal interneurons for locomotion and scratching. J Neurophysiol99:2887–901.
9.
BrownstoneRMWilsonJM. 2008. Strategies for delineating spinal locomotor rhythm-generating networks and the possible role of Hb9 interneurones in rhythmogenesis. Brain Res Rev57:64–76.
10.
BrusteinERossignolS. 1998. Recovery of locomotion after ventral and ventrolateral spinal lesions in the cat: I. Deficits and adaptive mechanisms. J Neurophysiol80:1245–67.
11.
CazaletsJRSqalli-HoussainiYClaracF. 1992. Activation of the central pattern generators for locomotion by serotonin and excitatory amino acids in neonatal rat. J Physiol455:187–204.
12.
CazaletsJRSqalli-HoussainiYClaracF. 1994. GABAergic inactivation of the central pattern generators for locomotion in isolated neonatal rat spinal cord. J Physiol474:173–81.
13.
ConwayBAHultbornHKiehnO. 1987. Proprioceptive input resets central locomotor rhythm in the spinal cat. Exp Brain Res68:643–56.
CourtineGGerasimenkoYvan den BrandRYewAMusienkoPZhongH and others. 2009. Transformation of nonfunctional spinal circuits into functional states after the loss of brain input. Nat Neurosci12:1333–42.
16.
CowleyKCSchmidtBJ. 1994. A comparison of motor patterns induced by N-methyl-D-aspartate, acetylcholine and serotonin in the in vitro neonatal rat spinal cord. Neurosci Lett171:147–50.
17.
CowleyKCSchmidtBJ. 1995. Effects of inhibitory amino acid antagonists on reciprocal inhibitory interactions during rhythmic motor activity in the in vitro neonatal rat spinal cord. J Neurophysiol74:1109–17.
18.
DegtyarenkoAMSimonESNorden-KrichmarTBurkeRE. 1998. Modulation of oligosynaptic cutaneous and muscle afferent reflex pathways during fictive locomotion and scratching in the cat. J Neurophysiol79:447–63.
19.
DeliaginaTGFeldmanAGGelfandIMOrlovskyGN. 1975. On the role of central program and afferent inflow in the control of scratching movements in the cat. Brain Res100:297–313.
20.
DeliaginaTGOrlovskyGN. 1980. Activity of Ia inhibitory interneurons during fictitious scratch reflex in the cat. Brain Res193:439–47.
21.
DeliaginaTGOrlovskyGNPerretC. 1981. Efferent activity during fictitious scratch reflex in the cat. J Neurophysiol45:595–604.
22.
DietzVMichelJ. 2009. Human bipeds use quadrupedal coordination during locomotion. Ann N Y Acad Sci1164:97–103.
23.
EndoTKiehnO. 2008. Asymmetric operation of the locomotor central pattern generator in the neonatal mouse spinal cord. J Neurophysiol100:3043–54.
24.
EtlinABlivisDBen-ZwiMLev-TovA. 2010. Long and short multifunicular projections of sacral neurons are activated by sensory input to produce locomotor activity in the absence of supraspinal control. J Neurosci30:10324–36.
25.
FeldmanAGOrlovskyGN. 1975. Activity of interneurons mediating reciprocal Ia inhibition during locomotion. Brain Res84:181–94.
26.
FrigonA. 2009. Reconfiguration of the spinal interneuronal network during locomotion in vertebrates. J Neurophysiol101:2201–203.
27.
FrigonAGossardJP. 2009. Asymmetric control of cycle period by the spinal locomotor rhythm generator in the adult cat. J Physiol587:4617–28.
28.
FrigonAGossardJP. 2010. Evidence for specialized rhythm-generating mechanisms in the adult mammalian spinal cord. J Neurosci30:7061–71.
FrigonASiroisJGossardJ-P. 2010. The effects of ankle and hip muscle afferent inputs on rhythm generation during fictive locomotion. J Neurophysiol103:1591–605.
31.
GeertsenSSStecinaKMeehanCFNielsenJBHultbornH. 2011. Reciprocal Ia inhibition contributes to motoneuronal hyperpolarisation during the inactive phase of locomotion and scratching in the cat. J Physiol 589(Pt 1):119–34.
32.
GiulianiCASmithJL. 1985. Development and characteristics of airstepping in chronic spinal cats. J Neurosci5:1276–82.
33.
GosgnachSLanuzaGMButtSJSaueressigHZhangYVelasquezT and others. 2006. V1 spinal neurons regulate the speed of vertebrate locomotor outputs. Nature440:215–9.
34.
GrassoRIvanenkoYPZagoMMolinariMScivolettoGCastellanoV and others. 2004. Distributed plasticity of locomotor pattern generators in spinal cord injured patients. Brain127:1019–34.
35.
GrillnerS. 1981. Control of locomotion in bipeds, tetrapods, and fish. In: BrookhartJMMountcastleVB editors. Handbook of physiology: the nervous system II. Bethesda, MD: American Physiology Society. p 1179–236.
36.
GrillnerSDubucR. 1988. Control of locomotion in vertebrates: spinal and supraspinal mechanisms. In: WaxmanDG editor. Functional recovery in neurological disease. New York: Raven. p 425–53.
37.
GrillnerSGeorgopoulosAPJordanLM. 1997. Selection and initiation of motor behavior. In: SteinPSGGrillnerSSelverstonAIStuartDG, editors. Neurons, networks, and motor behavior. Cambridge, MA: MIT Press. p 3–19.
38.
GrillnerSHalbertsmaJNillssonJThorstenssonA. 1979. The adaptation to speed in human locomotion. Brain Res165:177–82.
39.
GrillnerSJessellTM. 2009. Measured motion: searching for simplicity in spinal locomotor networks. Curr Opin Neurobiol19:572–86.
40.
GrillnerSZanggerP. 1979. On the central generation of locomotion in the low spinal cat. Exp Brain Res34:241–61.
41.
GuertinPAngelMJPerreaultM-CMcCreaDA. 1995. Ankle extensor group I afferents excite extensors throughout the hindlimb during fictive locomotion in the cat. J Physiol487:197–209.
42.
HalbertsmaJM. 1983. The stride cycle of the cat: the modelling of locomotion by computerized analysis of automatic recordings. Acta Physiol Scand Suppl521:1–75.
43.
HarveyPJLiXLiYBennettDJ. 2006. 5-HT2 receptor activation facilitates a persistent sodium current and repetitive firing in spinal motoneurons of rats with and without chronic spinal cord injury. J Neurophysiol96:1158–70.
44.
HultbornH. 2006. Spinal reflexes, mechanisms and concepts: from Eccles to Lundberg and beyond. Prog Neurobiol78:215–32.
45.
JiangWDrewT. 1996. Effects of bilateral lesions of the dorsolateral funiculi and dorsal columns at the level of the low thoracic spinal cord on the control of locomotion in the adult cat: I. Treadmill walking. J Neurophysiol76:849–66.
46.
JordanLM. 1998. Initiation of locomotion in mammals. Ann N Y Acad Sci860:83–93.
47.
JordanLMLiuJHedlundPBAkayTPearsonKG. 2008. Descending command systems for the initiation of locomotion in mammals. Brain Res Rev57:183–91.
JuvinLSimmersJMorinD. 2007. Locomotor rhythmogenesis in the isolated rat spinal cord: a phase-coupled set of symmetrical flexion extension oscillators. J Physiol583:115–28.
50.
KiehnO. 2011. Development and functional organization of spinal locomotor circuits. Curr Opin Neurobiol21:100–9.
51.
KiehnOKjaerulffO. 1996. Spatiotemporal characteristics of 5-HT and dopamine-induced rhythmic hindlimb activity in the in vitro neonatal rat. J Neurophysiol75:1472–82.
52.
KleinDAPatinoATreschMC. 2010. Flexibility of motor pattern generation across stimulation conditions by the neonatal rat spinal cord. J Neurophysiol103:1580–90.
53.
KleinDATreschMC. 2010. Specificity of intramuscular activation during rhythms produced by spinal patterning systems in the in vitro neonatal rat with hindlimb attached preparation. J Neurophysiol104:2158–68.
54.
KoshlandGFSmithJL. 1989. Mutable and immutable features of paw-shake responses after hindlimb deafferentation in the cat. J Neurophysiol62:162–73.
55.
KrouchevNKalaskaJFDrewT. 2006. Sequential activation of muscle synergies during locomotion in the intact cat as revealed by cluster analysis and direct decomposition. J Neurophysiol96:1991–2010.
56.
KuhtaPCSmithJL. 1990. Scratch responses in normal cats: hindlimb kinematics and muscle synergies. J Neurophysiol64:1653–67.
57.
Lafreniere-RoulaMMcCreaDA. 2005. Deletions of rhythmic motoneuron activity during fictive locomotion and scratch provide clues to the organization of the mammalian central pattern generator. J Neurophysiol94:1120–32.
58.
Lev-TovAEtlinABlivisD. 2010. Sensory-induced activation of pattern generators in the absence of supraspinal control. Ann N Y Acad Sci1198:54–62.
59.
LiWCSautoisBRobertsASoffeSR. 2007. Reconfiguration of a vertebrate motor network: specific neuron recruitment and context-dependent synaptic plasticity. J Neurosci27:12267–76.
60.
LiXMurrayKHarveyPJBallouEWBennettDJ. 2007. Serotonin facilitates a persistent calcium current in motoneurons of rats with and without chronic spinal cord injury. J Neurophysiol97:1236–46.
61.
MarderEBucherD. 2001. Central pattern generators and the control of rhythmic movements. Curr Biol11:R986–96.
62.
McCreaDARybakIA. 2008. Organization of mammalian locomotor rhythm and pattern generation. Brain Res Rev57:134–46.
63.
MurrayKCNakaeAStephensMJRankMD’AmicoJHarveyPJ and others. 2010. Recovery of motoneuron and locomotor function after spinal cord injury depends on constitutive activity in 5-HT2C receptors. Nat Med16:694–700.
64.
MusselmanKEYangJF. 2007. Loading the limb during rhythmic leg movements lengthens the duration of both flexion and extension in human infants. J Neurophysiol97:1247–57.
65.
NusbaumMPBeenhakkerMP. 2002. A small-systems approach to motor pattern generation. Nature417:343–50.
66.
OrsalDCabelguenJ-MPerretC. 1990. Interlimb coordination during fictive locomotion in the thalamic cat. Exp Brain Res82:536–46.
67.
PearsonKGMisiaszekJEFouadK. 1998. Enhancement and resetting of locomotor activity by muscle afferents. Ann N Y Acad Sci860:203–15.
68.
PearsonKGRossignolS. 1991. Fictive motor patterns in chronic spinal cats. J Neurophysiol66:1874–87.
69.
PerreaultM-CEnriquez-DentonMHultbornH. 1999. Proprioceptive control of extensor activity during fictive scratching and weight support compared to fictive locomotion. J Neurosci19:10966–76.
70.
PerretCCabelguenJ-M. 1976. Central and reflex participation in the timing of locomotor activations of a bifunctional muscle, the semi-tendinosus, in the cat. Brain Res106:390–5.
71.
PowerKEMcCreaDAFedirchukB. 2010. Intraspinally mediated state-dependent enhancement of motoneurone excitability during fictive scratch in the adult decerebrate cat. J Physiol588:2839–57.
72.
QuinlanKAKiehnO. 2007. Segmental, synaptic actions of commissural interneurons in the mouse spinal cord. J Neurosci27:6521–30.
73.
RankMMLiXBennettDJGorassiniMA. 2007. Role of endogenous release of norepinephrine in muscle spasms after chronic spinal cord injury. J Neurophysiol97:3166–80.
74.
RossignolSBarriereGAlluinOFrigonA. 2009. Re-expression of locomotor function after partial spinal cord injury. Physiology (Bethesda)24:127–39.
75.
RossignolSDubucRGossardJP. 2006. Dynamic sensorimotor interactions in locomotion. Physiol Rev86:89–154.
76.
SchmidtBJJordanLM. 2000. The role of serotonin in reflex modulation and locomotor rhythm production in the mammalian spinal cord. Brain Res Bull53:689–710.
77.
SchomburgEDPetersenNBarajonIHultbornH. 1998. Flexor reflex afferents reset the step cycle during fictive locomotion in the cat. Exp Brain Res122:339–50.
78.
SherringtonCS. 1906. The integrative action of the nervous system. New Haven, CT: Yale University Press.
79.
SherringtonCS. 1910. Notes on the scratch-reflex of the cat. Quart J Exp Physiol3:213–20.
80.
SmetanaRJuvinLDubucRAlfordS. 2010. A parallel cholinergic brainstem pathway for enhancing locomotor drive. Nat Neurosci13:731–8.
81.
SmithJLHoyMGKoshlandGFPhillipsDMZernickeRF. 1985. Intralimb coordination of the paw-shake response: a novel mixed synergy. J Neurophysiol54:1271–81.
82.
StecinaKQuevedoJMcCreaDA. 2005. Parallel reflex pathways from flexor muscle afferents evoking resetting and flexion enhancement during fictive locomotion and scratch in the cat. J Physiol569:275–90.
83.
TreschMCJarcA. 2009. The case for and against muscle synergies. Curr Opin Neurobiol19:601–7.
84.
VasudevanEVBastianAJ. 2010. Split-belt treadmill adaptation shows different functional networks for fast and slow human walking. J Neurophysiol103:183–91.
85.
WhelanPJ. 2010. Shining light into the black box of spinal locomotor networks. Philos Trans R Soc Lond B Biol Sci365:2383–95.
86.
YakovenkoSMcCreaDAStecinaKProchazkaA. 2005. Control of locomotor cycle durations. J Neurophysiol94:1057–65.
87.
ZanggerP. 1981. The effect of 4-aminopyridine on the spinal locomotor rhythm induced by L-Dopa. Brain Res215:211–23.
88.
ZehrEPHundzaSRVasudevanEV. 2009. The quadrupedal nature of human bipedal locomotion. Exerc Sport Sci Rev37:102–8.
