XB-ART-49349
Front Neural Circuits
2014 Jun 16;8:55. doi: 10.3389/fncir.2014.00055.
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Dopamine: a parallel pathway for the modulation of spinal locomotor networks.
Sharples SA
,
Koblinger K
,
Humphreys JM
,
Whelan PJ
.
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The spinal cord contains networks of neurons that can produce locomotor patterns. To readily respond to environmental conditions, these networks must be flexible yet at the same time robust. Neuromodulators play a key role in contributing to network flexibility in a variety of invertebrate and vertebrate networks. For example, neuromodulators contribute to altering intrinsic properties and synaptic weights that, in extreme cases, can lead to neurons switching between networks. Here we focus on the role of dopamine in the control of stepping networks in the spinal cord. We first review the role of dopamine in modulating rhythmic activity in the stomatogastric ganglion (STG) and the leech, since work from these preparations provides a foundation to understand its role in vertebrate systems. We then move to a discussion of dopamine's role in modulation of swimming in aquatic species such as the larval xenopus, lamprey and zebrafish. The control of terrestrial walking in vertebrates by dopamine is less studied and we review current evidence in mammals with a focus on rodent species. We discuss data suggesting that the source of dopamine within the spinal cord is mainly from the A11 area of the diencephalon, and then turn to a discussion of dopamine's role in modulating walking patterns from both in vivo and in vitro preparations. Similar to the descending serotonergic system, the dopaminergic system may serve as a potential target to promote recovery of locomotor function following spinal cord injury (SCI); evidence suggests that dopaminergic agonists can promote recovery of function following SCI. We discuss pharmacogenetic and optogenetic approaches that could be deployed in SCI and their potential tractability. Throughout the review we draw parallels with both noradrenergic and serotonergic modulatory effects on spinal cord networks. In all likelihood, a complementary monoaminergic enhancement strategy should be deployed following SCI.
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Species referenced: Xenopus
Genes referenced: camp dbh pnmt slc18a2 slc6a3 tbx2 th trhd
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Figure 1. The canonical catecholaminergic neuron is one that generates dopamine, noradrenaline or adrenaline. Catecholamines are synthesized from tyrosine through a series of biosynthetic steps progressing from tyrosine hydroxylase (TH) producing L-DOPA, aromatic amino acid decarboxylase (AADC) producing dopamine, dopamine-β-hydroxylase (DBH) producing noradrenaline and phenylethanolamine-N-methyl-transferase (PNMT) producing adrenaline. These neurons also express the vesicular monoaminergic transporter (VMAT2) to pump catecholamines into synaptic vesicles. A canonical dopaminergic neuron will also express dopamine reuptake transporters (DAT) and inhibitory D2 autoreceptors to regulate presynaptic release of dopamine. Post synaptic targets of dopamine include the excitatory D1-like and inhibitory D2-like receptors that act through G-protein second messenger cascades, increasing and decreasing intracellular cAMP levels respectively. |
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Figure 2. Descending dopaminergic fibres within the spinal cord originate in the A11. (A) Dopamine acts on all five dopamine receptors that are distributed non-uniformly through the dorsal and ventral horns of the spinal cord (Adapted with permission from Zhu et al., 2007). Descending noradrenergic fibres originating in the A5, A6 and A7 nuclei of the pons innervate the spinal cord. Schematic adapted with permission from Björklund and Dunnett (2007). |
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Figure 3. Dopaminergic modulation of spinal CPG activity. (A) Schematic of an in vitro isolated neonatal mouse spinal cord showing ventral root neurograms from the left and right L2 segment. (B) Spontaneous activity (Bi) is converted to a rhythmic slow non-locomotor rhythmic pattern (Bii) following bath application of dopamine (DA). (C and D) When DA is bath-applied during ongoing locomotor activity elicited by 5-HT and NMA it stabilizes and reduces the frequency of the rhythm. The spectrogram (D) depicts a cross-wavelet analysis of a locomotor rhythm evoked by 5-HT and NMA (box 1) and effect of dopamine (DA) on the pre-existing rhythm (box 2 and 3). Rhythm frequency is displayed on the y-axis and rhythm power displayed as warm or cool colors with warmer colors representing higher power or more stable rhythm. Dopamine also increases burst amplitude (Ei and Eii). (Ei) Graph displays an increase in burst amplitude over a 10 min period immediately following the addition of dopamine and (Eii) shows an average L2 neurogram burst from a representative experiment with bursts evoked by 5-HT and NMA (black) and following addition of dopamine (red) (Adapted from Humphreys and Whelan, 2012). |
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Figure 4. Known effects of dopamine on cellular components of the locomotor network. Ventral root neurograms from the L2, L5 and S1 segments and ventrolateral funiculus (VLF) of a spinal cord isolation preparation with fast synaptic transmission blocked (CNQX, AP5, PTX and Strychnine) indicates that dopamine increases the excitability of motor neurons projecting through ventral roots and interneurons projecting through the VLF (A) (Adapted from Han et al., 2007). Intracellular recordings from motor neurons show that dopamine increases motor neuron excitability indicated by an increase in the slope of the frequency-current relationship (Bi and Bii). This effect is in part mediated by a reduction in IA and SKCa conductances. Dopamine also increases AMPA conductances (Ci and Cii) via a D1-like receptor mechanisms (Adapted with permission from Han and Whelan, 2009). Dopamine reduces recurrent excitatory feedback to the locomotor CPG (Humphreys and Whelan, 2012) and Renshaw cells via D2-like receptor mechanisms (Maitra et al., 1993). A summary of all these effects are depicted in panel (D). |
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Figure 5. Recovery of motor function following spinal cord injury may be facilitated using combinatorial therapies to promote plasticity within motor networks. This could be accomplished by targeting monoaminergic systems through the activation of descending brain nuclei using optogenetic or pharmacogenetic approaches, implantation of fetal or embryonic cells from the dopaminergic ventral tegmental area, noradrenergic locus coeruleus or serotonergic raphe nucleus caudal to the site of injury, intrathecal injection of catecholamines and systemic injection of L-DOPA. While these approaches may not be optimal in isolation, they may serve as an effective complementary treatment with rehabilitation and other therapies to reduce secondary injury and promote regeneration of damaged descending tracts to promote the recovery of motor function. |
References [+] :
Abrahamson,
The posterior hypothalamic area: chemoarchitecture and afferent connections.
2001, Pubmed
Abrahamson, The posterior hypothalamic area: chemoarchitecture and afferent connections. 2001, Pubmed
Airan, Temporally precise in vivo control of intracellular signalling. 2009, Pubmed
Aston-Jones, Recent advances in optogenetics and pharmacogenetics. 2013, Pubmed
Baker, L-dopa-induced locomotor-like activity in ankle flexor and extensor nerves of chronic and acute spinal cats. 1984, Pubmed
Barbeau, Initiation and modulation of the locomotor pattern in the adult chronic spinal cat by noradrenergic, serotonergic and dopaminergic drugs. 1991, Pubmed
Barbeau, Recovery of locomotion after chronic spinalization in the adult cat. 1987, Pubmed
Barbeau, Enhancement of locomotor recovery following spinal cord injury. 1994, Pubmed
Barraud, Neuroanatomical study of the A11 diencephalospinal pathway in the non-human primate. 2010, Pubmed
Barreiro-Iglesias, Descending brain-spinal cord projections in a primitive vertebrate, the lamprey: cerebrospinal fluid-contacting and dopaminergic neurons. 2008, Pubmed
Barrière, Neuromodulation of the locomotor network by dopamine in the isolated spinal cord of newborn rat. 2004, Pubmed
Barrière, Prominent role of the spinal central pattern generator in the recovery of locomotion after partial spinal cord injuries. 2008, Pubmed
Benoit-Marand, Inhibition of dopamine release via presynaptic D2 receptors: time course and functional characteristics in vivo. 2001, Pubmed
Björklund, Dopamine neuron systems in the brain: an update. 2007, Pubmed
Björklund, Evidence for a major spinal cord projection from the diencephalic A11 dopamine cell group in the rat using transmitter-specific fluorescent retrograde tracing. 1979, Pubmed
Blessing, Direct projection of catecholamine (presumably dopamine)-containing neurons from hypothalamus to spinal cord. 1979, Pubmed
Boido, Embryonic and adult stem cells promote raphespinal axon outgrowth and improve functional outcome following spinal hemisection in mice. 2009, Pubmed
Boulenguez, Strategies to restore motor functions after spinal cord injury. 2009, Pubmed
Bregman, Development of serotonin immunoreactivity in the rat spinal cord and its plasticity after neonatal spinal cord lesions. 1987, Pubmed
Briggman, Optical imaging of neuronal populations during decision-making. 2005, Pubmed
Bruinstroop, Spinal projections of the A5, A6 (locus coeruleus), and A7 noradrenergic cell groups in rats. 2012, Pubmed
Brustein, Steps during the development of the zebrafish locomotor network. 2003, Pubmed
Buchanan, 5-Hydroxytryptamine depresses reticulospinal excitatory postsynaptic potentials in motoneurons of the lamprey. 1991, Pubmed
Bucher, Axonal dopamine receptors activate peripheral spike initiation in a stomatogastric motor neuron. 2003, Pubmed
CARLSSON, Cellular localization of brain monoamines. 1962, Pubmed
Carp, Dopamine receptor-mediated depression of spinal monosynaptic transmission. 1982, Pubmed
Chatelin, Neuronal promoter of human aromatic L-amino acid decarboxylase gene directs transgene expression to the adult floor plate and aminergic nuclei induced by the isthmus. 2001, Pubmed
Chau, Effects of intrathecal alpha1- and alpha2-noradrenergic agonists and norepinephrine on locomotion in chronic spinal cats. 1998, Pubmed
Chetrit, Inhibiting subthalamic D5 receptor constitutive activity alleviates abnormal electrical activity and reverses motor impairment in a rat model of Parkinson's disease. 2013, Pubmed
Christie, Monoaminergic establishment of rostrocaudal gradients of rhythmicity in the neonatal mouse spinal cord. 2005, Pubmed
Ciliax, Immunocytochemical localization of the dopamine transporter in human brain. 1999, Pubmed
Clark, The projection of locus coeruleus neurons to the spinal cord in the rat determined by anterograde tracing combined with immunocytochemistry. 1991, Pubmed
Clemens, Opposing modulatory effects of D1- and D2-like receptor activation on a spinal central pattern generator. 2012, Pubmed , Xenbase
Commissiong, Development of catecholaminergic nerves in the spinal cord of the rat. 1983, Pubmed
Commissiong, Fetal locus coeruleus transplanted into the transected spinal cord of the adult rat: some observations and implications. 1984, Pubmed
Commissiong, Spinal cord dopaminergic neurons: evidence for an uncrossed nigrospinal pathway. 1979, Pubmed
Crisp, A cephalic projection neuron involved in locomotion is dye coupled to the dopaminergic neural network in the medicinal leech. 2004, Pubmed
Crisp, Mechanisms contributing to the dopamine induction of crawl-like bursting in leech motoneurons. 2012, Pubmed
DAHLSTROEM, EVIDENCE FOR THE EXISTENCE OF MONOAMINE-CONTAINING NEURONS IN THE CENTRAL NERVOUS SYSTEM. I. DEMONSTRATION OF MONOAMINES IN THE CELL BODIES OF BRAIN STEM NEURONS. 1964, Pubmed
Dahlström, Localization of monoamines in the lower brain stem. 1964, Pubmed
Demchyshyn, Dopamine D5 receptor agonist high affinity and constitutive activity profile conferred by carboxyl-terminal tail sequence. 2000, Pubmed
Fong, Recovery of control of posture and locomotion after a spinal cord injury: solutions staring us in the face. 2009, Pubmed
Ford, The role of D2-autoreceptors in regulating dopamine neuron activity and transmission. 2014, Pubmed
Forssberg, The locomotion of the acute spinal cat injected with clonidine i.v. 1973, Pubmed
Fritschy, Demonstration of two separate descending noradrenergic pathways to the rat spinal cord: evidence for an intragriseal trajectory of locus coeruleus axons in the superficial layers of the dorsal horn. 1990, Pubmed
Gabriel, Serotonergic modulation of locomotion in zebrafish: endogenous release and synaptic mechanisms. 2009, Pubmed
Gentleman, Dopamine-activated adenylate cyclase of spinal cord: supersensitivity following transection of the cord. 1981, Pubmed
Gerin, Direct evidence for the link between monoaminergic descending pathways and motor activity. I. A study with microdialysis probes implanted in the ventral funiculus of the spinal cord. 1995, Pubmed
Gerin, Direct evidence for the link between monoaminergic descending pathways and motor activity: II. A study with microdialysis probes implanted in the ventral horn of the spinal cord. 1998, Pubmed
Gordon, Monoaminergic control of cauda-equina-evoked locomotion in the neonatal mouse spinal cord. 2006, Pubmed
Goulding, Circuits controlling vertebrate locomotion: moving in a new direction. 2009, Pubmed
Grillner, On the central generation of locomotion in the low spinal cat. 1979, Pubmed
Gruhn, Dopamine modulation of two delayed rectifier potassium currents in a small neural network. 2005, Pubmed
Guertin, Effects on locomotion, muscle, bone, and blood induced by a combination therapy eliciting weight-bearing stepping in nonassisted spinal cord-transected mice. 2011, Pubmed
Gutierrez, Multiple mechanisms switch an electrically coupled, synaptically inhibited neuron between competing rhythmic oscillators. 2013, Pubmed
Hammar, The actions of monoamines and distribution of noradrenergic and serotoninergic contacts on different subpopulations of commissural interneurons in the cat spinal cord. 2004, Pubmed
Han, Dopaminergic modulation of spinal neuronal excitability. 2007, Pubmed
Han, Modulation of AMPA currents by D(1)-like but not D(2)-like receptors in spinal motoneurons. 2009, Pubmed
Harris-Warrick, Dopamine modulation of transient potassium current evokes phase shifts in a central pattern generator network. 1995, Pubmed
Harris-Warrick, Checks and balances in neuromodulation. 2010, Pubmed
Harris-Warrick, Distributed effects of dopamine modulation in the crustacean pyloric network. 1998, Pubmed
Harris-Warrick, Serotonin modulates the central pattern generator for locomotion in the isolated lamprey spinal cord. 1985, Pubmed
Heckman, Active properties of motoneurone dendrites: diffuse descending neuromodulation, focused local inhibition. 2008, Pubmed
Hellal, Microtubule stabilization reduces scarring and causes axon regeneration after spinal cord injury. 2011, Pubmed
Hill, 5-HT inhibits N-type but not L-type Ca(2+) channels via 5-HT1A receptors in lamprey spinal neurons. 2003, Pubmed
Hinckley, Locomotor-like rhythms in a genetically distinct cluster of interneurons in the mammalian spinal cord. 2005, Pubmed
Hökfelt, Chemical anatomy of the brain. 1984, Pubmed
Humphreys, Dopamine exerts activation-dependent modulation of spinal locomotor circuits in the neonatal mouse. 2012, Pubmed
Jaeger, Some neurons of the rat central nervous system contain aromatic-L-amino-acid decarboxylase but not monoamines. 1983, Pubmed
Jankowska, The effect of DOPA on the spinal cord. 5. Reciprocal organization of pathways transmitting excitatory action to alpha motoneurones of flexors and extensors. 1967, Pubmed
Jankowska, The effect of DOPA on the spinal cord. 6. Half-centre organization of interneurones transmitting effects from the flexor reflex afferents. 1967, Pubmed
Jensen, Effects of an intrathecal dopamine agonist, apomorphine, on thermal and chemical evoked noxious responses in rats. 1984, Pubmed
Jiang, An in vitro functionally mature mouse spinal cord preparation for the study of spinal motor networks. 1999, Pubmed
Johnson, Interactions between focused synaptic inputs and diffuse neuromodulation in the spinal cord. 2010, Pubmed
Johnson, Aminergic modulation of graded synaptic transmission in the lobster stomatogastric ganglion. 1990, Pubmed
Johnson, Dopamine modulation of phasing of activity in a rhythmic motor network: contribution of synaptic and intrinsic modulatory actions. 2005, Pubmed
Johnson, Differential modulation of synaptic strength and timing regulate synaptic efficacy in a motor network. 2011, Pubmed
Jordan, Descending command systems for the initiation of locomotion in mammals. 2008, Pubmed
Kadiri, Dopamine-induced oscillations of the pyloric pacemaker neuron rely on release of calcium from intracellular stores. 2011, Pubmed
Karoum, Regional differences in catecholamine formation and metabolism in the rat spinal cord. 1981, Pubmed
Keeler, Increased excitability of spinal pain reflexes and altered frequency-dependent modulation in the dopamine D3-receptor knockout mouse. 2012, Pubmed
Kehr, Evidence for a receptor-mediated feedback control of striatal tyrosine hydroxylase activity. 1972, Pubmed
Kemnitz, Modulation of swimming in the lamprey, Petromyzon marinus, by serotonergic and dopaminergic drugs. 1995, Pubmed
Kemnitz, Dopaminergic modulation of spinal neurons and synaptic potentials in the lamprey spinal cord. 1997, Pubmed
Kiehn, Spatiotemporal characteristics of 5-HT and dopamine-induced rhythmic hindlimb activity in the in vitro neonatal rat. 1996, Pubmed
Kiehn, Effects of noradrenaline on locomotor rhythm-generating networks in the isolated neonatal rat spinal cord. 1999, Pubmed
Kloppenburg, Dopamine modulates two potassium currents and inhibits the intrinsic firing properties of an identified motor neuron in a central pattern generator network. 1999, Pubmed
Kvarta, Neuromodulator-evoked synaptic metaplasticity within a central pattern generator network. 2012, Pubmed
Kwon, Inflammatory and structural biomarkers in acute traumatic spinal cord injury. 2011, Pubmed
Lambert, The conserved dopaminergic diencephalospinal tract mediates vertebrate locomotor development in zebrafish larvae. 2012, Pubmed
Lapointe, Synergistic effects of D1/5 and 5-HT1A/7 receptor agonists on locomotor movement induction in complete spinal cord-transected mice. 2008, Pubmed
Lapointe, Specific role of dopamine D1 receptors in spinal network activation and rhythmic movement induction in vertebrates. 2009, Pubmed
Lee, DREADDs: novel tools for drug discovery and development. 2014, Pubmed
Levant, D(3) dopamine receptors in rat spinal cord: implications for sensory and motor function. 2001, Pubmed
Li, Synthesis, transport, and metabolism of serotonin formed from exogenously applied 5-HTP after spinal cord injury in rats. 2014, Pubmed
Lindvall, Dopamine-containing neurons in the spinal cord: anatomy and some functional aspects. 1983, Pubmed
Liu, Stimulation of the parapyramidal region of the neonatal rat brain stem produces locomotor-like activity involving spinal 5-HT7 and 5-HT2A receptors. 2005, Pubmed
Lorang, Cell-type-specific expression of catecholamine transporters in the rat brain. 1994, Pubmed
Madriaga, Modulation of locomotor activity by multiple 5-HT and dopaminergic receptor subtypes in the neonatal mouse spinal cord. 2004, Pubmed
Maitra, Dopaminergic influence on the excitability of antidromically activated Renshaw cells in the lumbar spinal cord of the rat. 1993, Pubmed
Majczyński, Serotonin-related enhancement of recovery of hind limb motor functions in spinal rats after grafting of embryonic raphe nuclei. 2005, Pubmed
Manconi, Preferential D2 or preferential D3 dopamine agonists in restless legs syndrome. 2011, Pubmed
Marder, Neuromodulation of neuronal circuits: back to the future. 2012, Pubmed
Maric, Levodopa therapy in incomplete spinal cord injury. 2008, Pubmed
Masino, TTX-resistant NMDA receptor-mediated membrane potential oscillations in neonatal mouse Hb9 interneurons. 2012, Pubmed
McCrea, Dopamine D1 and D2 antagonists block L-DOPA-induced air-stepping in decerebrate neonatal rats. 1997, Pubmed
McDearmid, Aminergic modulation of glycine release in a spinal network controlling swimming in Xenopus laevis. 1997, Pubmed , Xenbase
McEwen, L-DOPA and quipazine elicit air-stepping in neonatal rats with spinal cord transections. 1997, Pubmed
McLean, Divergent actions of serotonin receptor activation during fictive swimming in frog embryos. 2004, Pubmed , Xenbase
McLean, Metamodulation of a spinal locomotor network by nitric oxide. 2004, Pubmed , Xenbase
McPherson, Modulation of lamprey fictive swimming and motoneuron physiology by dopamine, and its immunocytochemical localization in the spinal cord. 1994, Pubmed
Miles, Neuromodulation of vertebrate locomotor control networks. 2011, Pubmed
Missale, Dopamine receptors: from structure to function. 1998, Pubmed
Montague, Nonuniform distribution of contacts from noradrenergic and serotonergic boutons on the dendrites of cat splenius motoneurons. 2013, Pubmed
Moore, Central catecholamine neuron systems: anatomy and physiology of the norepinephrine and epinephrine systems. 1979, Pubmed
Murray, Recovery of motoneuron and locomotor function after spinal cord injury depends on constitutive activity in 5-HT2C receptors. 2010, Pubmed
Musienko, Controlling specific locomotor behaviors through multidimensional monoaminergic modulation of spinal circuitries. 2011, Pubmed
Ochi, Comparative study of the monoamine neuron system in the spinal cord of the lamprey and hagfish. 1979, Pubmed
Oh, Expression of transgenes in midbrain dopamine neurons using the tyrosine hydroxylase promoter. 2009, Pubmed
Pappas, Neonatal androgen-dependent sex differences in lumbar spinal cord dopamine concentrations and the number of A11 diencephalospinal dopamine neurons. 2010, Pubmed
Pappas, Lack of D2 receptor mediated regulation of dopamine synthesis in A11 diencephalospinal neurons in male and female mice. 2008, Pubmed
Peck, Amine modulation of Ih in a small neural network. 2006, Pubmed
Peyron, Origin of the dopaminergic innervation of the rat dorsal raphe nucleus. 1995, Pubmed
Pierre, Immunocytochemical localization of dopamine and its synthetic enzymes in the central nervous system of the lamprey Lampetra fluviatilis. 1997, Pubmed
Prinz, Similar network activity from disparate circuit parameters. 2004, Pubmed
Puhl, Dopamine activates the motor pattern for crawling in the medicinal leech. 2008, Pubmed
Puhl, Necessary, sufficient and permissive: a single locomotor command neuron important for intersegmental coordination. 2012, Pubmed
Qu, Projections of diencephalic dopamine neurons into the spinal cord in mice. 2006, Pubmed
Rajaofetra, Immunocytochemical mapping of noradrenergic projections to the rat spinal cord with an antiserum against noradrenaline. 1992, Pubmed
Rajaofetra, Pre- and post-natal ontogeny of serotonergic projections to the rat spinal cord. 1989, Pubmed
Rauscent, Opposing aminergic modulation of distinct spinal locomotor circuits and their functional coupling during amphibian metamorphosis. 2009, Pubmed , Xenbase
Reimer, Dopamine from the brain promotes spinal motor neuron generation during development and adult regeneration. 2013, Pubmed
Rémy-Néris, Effects of intrathecal clonidine injection on spinal reflexes and human locomotion in incomplete paraplegic subjects. 1999, Pubmed
Ridet, Spinal dopaminergic system of the rat: light and electron microscopic study using an antiserum against dopamine, with particular emphasis on synaptic incidence. 1992, Pubmed
Rossignol, Pharmacological activation and modulation of the central pattern generator for locomotion in the cat. 1998, Pubmed
Rossignol, Recovery of locomotion after spinal cord injury: some facts and mechanisms. 2011, Pubmed
Rowland, Current status of acute spinal cord injury pathophysiology and emerging therapies: promise on the horizon. 2008, Pubmed
Ryu, Orthopedia homeodomain protein is essential for diencephalic dopaminergic neuron development. 2007, Pubmed
Schmidt, The role of serotonin in reflex modulation and locomotor rhythm production in the mammalian spinal cord. 2000, Pubmed
Schotland, Control of lamprey locomotor neurons by colocalized monoamine transmitters. 1995, Pubmed
Shapiro, Unparalleled control of neural activity using orthogonal pharmacogenetics. 2012, Pubmed
Shupliakov, Synaptic vesicle depletion in reticulospinal axons is reduced by 5-hydroxytryptamine: direct evidence for presynaptic modulation of glutamatergic transmission. 1995, Pubmed
Sickles, Dopamine D1 and D2 antagonists block L-dopa-elicited air-stepping in neonatal rats. 1992, Pubmed
Sillar, Development and aminergic neuromodulation of a spinal locomotor network controlling swimming in Xenopus larvae. 1998, Pubmed , Xenbase
Skagerberg, Organization of diencephalic dopamine neurones projecting to the spinal cord in the rat. 1985, Pubmed
Smith, Dopamine enhances glutamate-activated currents in spinal motoneurons. 1995, Pubmed
Sqalli-Houssaini, Noradrenergic control of locomotor networks in the in vitro spinal cord of the neonatal rat. 2000, Pubmed
Stuart, Thomas Graham Brown (1882--1965), Anders Lundberg (1920-), and the neural control of stepping. 2008, Pubmed
Svensson, Endogenous dopaminergic modulation of the lamprey spinal locomotor network. 2003, Pubmed
Tamae, Direct inhibition of substantia gelatinosa neurones in the rat spinal cord by activation of dopamine D2-like receptors. 2005, Pubmed
Tarazi, Comparative postnatal development of dopamine D(1), D(2) and D(4) receptors in rat forebrain. 2000, Pubmed
Taylor, Noradrenergic alpha-1 and alpha-2 antagonists block L-dopa-induced air-stepping in neonatal rats. 1994, Pubmed
Thirumalai, Endogenous dopamine suppresses initiation of swimming in prefeeding zebrafish larvae. 2008, Pubmed
Ugrumov, Non-dopaminergic neurons partly expressing dopaminergic phenotype: distribution in the brain, development and functional significance. 2009, Pubmed
Van Dongen, 5-Hydroxytryptamine (serotonin) causes a reduction in the afterhyperpolarization following the action potential in lamprey motoneurons and premotor interneurons. 1986, Pubmed
Vidal-Gadea, Caenorhabditis elegans selects distinct crawling and swimming gaits via dopamine and serotonin. 2011, Pubmed
Wallén, Effects of 5-hydroxytryptamine on the afterhyperpolarization, spike frequency regulation, and oscillatory membrane properties in lamprey spinal cord neurons. 1989, Pubmed
Wang, 5-HT and dopamine modulates CaV1.3 calcium channels involved in postinhibitory rebound in the spinal network for locomotion in lamprey. 2011, Pubmed
Whelan, Properties of rhythmic activity generated by the isolated spinal cord of the neonatal mouse. 2000, Pubmed
Wilson, Conditional rhythmicity of ventral spinal interneurons defined by expression of the Hb9 homeodomain protein. 2005, Pubmed
Wolf, Autoreceptor regulation of dopamine synthesis. 1990, Pubmed
Yoshida, Existence of new dopaminergic terminal plexus in the rat spinal cord: assessment by immunohistochemistry using anti-dopamine serum. 1988, Pubmed
Zhao, Spinal cord dopamine receptor expression and function in mice with 6-OHDA lesion of the A11 nucleus and dietary iron deprivation. 2007, Pubmed
Zhu, Expression and distribution of all dopamine receptor subtypes (D(1)-D(5)) in the mouse lumbar spinal cord: a real-time polymerase chain reaction and non-autoradiographic in situ hybridization study. 2007, Pubmed