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Motor Neurons

Jorn Hounsgaard

10.1002/cphy.c160025

Source: Volume 7, Issue 2, April 2017

Published online: March 2017

Full Article on Wiley Online Library



ABSTRACT

Motor neurons translate synaptic input from widely distributed premotor networks into patterns of action potentials that orchestrate motor unit force and motor behavior. Intercalated between the CNS and muscles, motor neurons add to and adjust the final motor command. The identity and functional properties of this facility in the path from synaptic sites to the motor axon is reviewed with emphasis on voltage sensitive ion channels and regulatory metabotropic transmitter pathways. The catalog of the intrinsic response properties, their underlying mechanisms, and regulation obtained from motoneurons in in vitro preparations is far from complete. Nevertheless, a foundation has been provided for pursuing functional significance of intrinsic response properties in motoneurons in vivo during motor behavior at levels from molecules to systems. © 2017 American Physiological Society. Compr Physiol 7:463‐484, 2017.

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Figure 1. Figure 1. Hypothetical evolution from an all‐inclusive primordial sensory‐motor epithelial cell (left) into a chain of separate sensory‐epithelial cells, motor‐ganglion cells, and myo‐epithelial cells connected by synapses (right). Modified, with permission, from (33).
Figure 2. Figure 2. Simulated centrifugal and centripetal electrotonic conduction in a motoneuron. The morphological structure of the neuron in A is expressed in electrotonic transforms in B for centripetal and centrifugal conduction of AC and DC signals. Scale bar in B is 1 λ, the distance over which the voltage attenuation is 1/e. In C, the graph illustrates the centripetal attenuation of a simulated epsp from the mid‐dendritic site of initiation (d1) to the cell body (S). D illustrates the simulated soma recorded epsp generated by the same synaptic conductance applied at the cell body (S), at a mid‐dendritic site (d1) and at a distal dendritic site (d2). All modeling data obtained from the cell morphologically reconstructed in A. Modified, with permission, from (210)
Figure 3. Figure 3. Action potential and after‐potentials. (A) IS‐SD components of action potential demonstrated by superimposed sweeps of antidromic action potentials at three stimulus frequencies (1, 10, and 40 Hz). Action potential safety factor lowered by maintained hyperpolarizing holding current. (B) Configuration of afterpotentials during low‐frequency firing maintained by depolarizing holding current. Modified, with permission, from (95)
Figure 4. Figure 4. Specialized membrane microdomains in spinal motoneurons. (A) Differential distribution of Na channels in the axon initial segment. Nav1.6 widely expressed in the axon initial segment but replaced by Nav1.1 most proximally. (B) Distribution of specific ion channels and receptors in the peri‐ and subsynaptic membrane in soma and proximal dendrites of motoneurons. A modified, with permission, from (57,58). B modified, with permission, from (52).
Figure 5. Figure 5. The mAHP stabilize repetitive firing in motoneurons. Apamin increases frequency of firing during depolarizing current pulse (A, B) by eliminating the mAHP (C) and increases firing variability in steady‐state firing frequency (D). Modified, with permission, from (143).
Figure 6. Figure 6. Persistent Na+ current (IpNa) contributes to repetitive firing properties in motoneurons. The TTX sensitive IpNa activates below the threshold for action potentials in current clamp (A) and in voltage clamp (B). Elimination of IpNa in dynamic clamp decreases excitability by increasing the rheobase current (C), and further narrows integration window by increasing the gain (D). A, C, and D, modified, with permission, from (73). B, unpublished results from Robertas Guzulaitis and Jorn Hounsgaard used with permission.
Figure 7. Figure 7. Motoneuron resting membrane potential regulated by two‐pore domain TASK channels. (A) Reduced TASK conductance by 8‐Hydroxy‐2‐(dipropylamino)tetralin hydrobromide (8‐OH DPAT) activation of 5HT1A receptors increases excitability due to depolarization and increased input resistance in motoneurons. (B) The volatile anesthetics halothane induces hyperpolarization by activating TASK channels in motoneurons. The hyperpolarization is eliminated by acidification‐induced block of TASK channels. A modified, with permission, from (160). B modified, with permission, from (198).
Figure 8. Figure 8. Threshold for action potentials in motoneurons regulated by functional network activity. (A) The spike threshold observed during a depolarizing ramp current injected through the recording electrode observed at rest (blue bar, left) was hyperpolarized and spiking increased for the same level of depolarization during locomotor network activity (red bar, right). (B) Reduced excitability of motoneurons (upper panel) by iontophoretic activation of 5‐HT1A receptors on the axon initial segment (middle panel). The decreased excitability is caused by depolarized spike threshold (lower panel). A modified, with permission, from (119). B modified, with permission, from (47).
Figure 9. Figure 9. Plateau potential in motoneurons. (A) Depolarization evoked plateau potential promoted by 5‐HT in turtle motoneuron. (B) Depolarization evoked plateau potential promoted by scratch network activity in motoneuron (above) blocked by antagonist of mGluR‐I receptors (below) in an ex vivo preparation from the turtle. A modified, with permission, from (164). B modified, with permission, from (1).
Figure 10. Figure 10. Windup of plateau potential and [Ca2+]i in motoneuron. (A) Image of OGB‐1 filled turtle motoneuron during parallel whole‐cell patch recording and two‐photon microscopy in transverse spinal cord slice. (B) Parallel windup of plateau potential and [Ca2+]i buildup during train of depolarizing current pulses. (C) [Ca2+]i‐induced clustering of Cav1.3S L‐type Ca channels (145) as hypothesized mechanism for windup. (A, B) Unpublished results by Robertas Guzulaitis and Jorn Hounsgaard used with permission. C modified, with permission, from (145).
Figure 11. Figure 11. Functional motor network activity affects intrinsic properties of motoneurons. (A) mAHP in motoneurons attenuated during fictive locomotion. (B) Irregular firing during scratch network activity. (C) High conductance during scratch network activity. A modified, with permission, from (32). B modified, with permission, from (23). C modified, with permission, from (85).
Figure 12. Figure 12. Motor unit activity compatible with plateau potentials in human motoneurons. (A) Sequentially activated motor units maintain a steady frequency upon recruitment during ramp contractions. (B) Force threshold for recruitment of unit b during ascending force ramp, much higher than derecruitment force threshold during descending force ramp. A modified, with permission, from (116). B modified, with permission, from (80).


Figure 1. Hypothetical evolution from an all‐inclusive primordial sensory‐motor epithelial cell (left) into a chain of separate sensory‐epithelial cells, motor‐ganglion cells, and myo‐epithelial cells connected by synapses (right). Modified, with permission, from (33).


Figure 2. Simulated centrifugal and centripetal electrotonic conduction in a motoneuron. The morphological structure of the neuron in A is expressed in electrotonic transforms in B for centripetal and centrifugal conduction of AC and DC signals. Scale bar in B is 1 λ, the distance over which the voltage attenuation is 1/e. In C, the graph illustrates the centripetal attenuation of a simulated epsp from the mid‐dendritic site of initiation (d1) to the cell body (S). D illustrates the simulated soma recorded epsp generated by the same synaptic conductance applied at the cell body (S), at a mid‐dendritic site (d1) and at a distal dendritic site (d2). All modeling data obtained from the cell morphologically reconstructed in A. Modified, with permission, from (210)


Figure 3. Action potential and after‐potentials. (A) IS‐SD components of action potential demonstrated by superimposed sweeps of antidromic action potentials at three stimulus frequencies (1, 10, and 40 Hz). Action potential safety factor lowered by maintained hyperpolarizing holding current. (B) Configuration of afterpotentials during low‐frequency firing maintained by depolarizing holding current. Modified, with permission, from (95)


Figure 4. Specialized membrane microdomains in spinal motoneurons. (A) Differential distribution of Na channels in the axon initial segment. Nav1.6 widely expressed in the axon initial segment but replaced by Nav1.1 most proximally. (B) Distribution of specific ion channels and receptors in the peri‐ and subsynaptic membrane in soma and proximal dendrites of motoneurons. A modified, with permission, from (57,58). B modified, with permission, from (52).


Figure 5. The mAHP stabilize repetitive firing in motoneurons. Apamin increases frequency of firing during depolarizing current pulse (A, B) by eliminating the mAHP (C) and increases firing variability in steady‐state firing frequency (D). Modified, with permission, from (143).


Figure 6. Persistent Na+ current (IpNa) contributes to repetitive firing properties in motoneurons. The TTX sensitive IpNa activates below the threshold for action potentials in current clamp (A) and in voltage clamp (B). Elimination of IpNa in dynamic clamp decreases excitability by increasing the rheobase current (C), and further narrows integration window by increasing the gain (D). A, C, and D, modified, with permission, from (73). B, unpublished results from Robertas Guzulaitis and Jorn Hounsgaard used with permission.


Figure 7. Motoneuron resting membrane potential regulated by two‐pore domain TASK channels. (A) Reduced TASK conductance by 8‐Hydroxy‐2‐(dipropylamino)tetralin hydrobromide (8‐OH DPAT) activation of 5HT1A receptors increases excitability due to depolarization and increased input resistance in motoneurons. (B) The volatile anesthetics halothane induces hyperpolarization by activating TASK channels in motoneurons. The hyperpolarization is eliminated by acidification‐induced block of TASK channels. A modified, with permission, from (160). B modified, with permission, from (198).


Figure 8. Threshold for action potentials in motoneurons regulated by functional network activity. (A) The spike threshold observed during a depolarizing ramp current injected through the recording electrode observed at rest (blue bar, left) was hyperpolarized and spiking increased for the same level of depolarization during locomotor network activity (red bar, right). (B) Reduced excitability of motoneurons (upper panel) by iontophoretic activation of 5‐HT1A receptors on the axon initial segment (middle panel). The decreased excitability is caused by depolarized spike threshold (lower panel). A modified, with permission, from (119). B modified, with permission, from (47).


Figure 9. Plateau potential in motoneurons. (A) Depolarization evoked plateau potential promoted by 5‐HT in turtle motoneuron. (B) Depolarization evoked plateau potential promoted by scratch network activity in motoneuron (above) blocked by antagonist of mGluR‐I receptors (below) in an ex vivo preparation from the turtle. A modified, with permission, from (164). B modified, with permission, from (1).


Figure 10. Windup of plateau potential and [Ca2+]i in motoneuron. (A) Image of OGB‐1 filled turtle motoneuron during parallel whole‐cell patch recording and two‐photon microscopy in transverse spinal cord slice. (B) Parallel windup of plateau potential and [Ca2+]i buildup during train of depolarizing current pulses. (C) [Ca2+]i‐induced clustering of Cav1.3S L‐type Ca channels (145) as hypothesized mechanism for windup. (A, B) Unpublished results by Robertas Guzulaitis and Jorn Hounsgaard used with permission. C modified, with permission, from (145).


Figure 11. Functional motor network activity affects intrinsic properties of motoneurons. (A) mAHP in motoneurons attenuated during fictive locomotion. (B) Irregular firing during scratch network activity. (C) High conductance during scratch network activity. A modified, with permission, from (32). B modified, with permission, from (23). C modified, with permission, from (85).


Figure 12. Motor unit activity compatible with plateau potentials in human motoneurons. (A) Sequentially activated motor units maintain a steady frequency upon recruitment during ramp contractions. (B) Force threshold for recruitment of unit b during ascending force ramp, much higher than derecruitment force threshold during descending force ramp. A modified, with permission, from (116). B modified, with permission, from (80).
References
 1.Alaburda A, Hounsgaard J. Metabotropic modulation of motoneurons by scratch‐like spinal network activity. J Neurosci 23: 8625‐8629, 2003.
 2.Alaburda A, Perrier JF, Hounsgaard J. An M‐like outward current regulates the excitability of spinal motoneurones in the adult turtle. J Physiol 540: 875‐881, 2002.
 3.Alaburda A, Russo R, MacAulay N, Hounsgaard J. Periodic high‐conductance states in spinal neurons during scratch‐like network activity in adult turtles. J Neurosci 25: 6316‐6321, 2005.
 4.Alzheimer C, Schwindt PC, Crill WE. Modal gating of Na+ channels as a mechanism of persistent Na+ current in pyramidal neurons from rat and cat sensorimotor cortex. J Neurosci 13: 660‐673, 1993.
 5.Andres C, Aguilar J, Gonzalez‐Ramirez R, Elias‐Vinas D, Felix R, Delgado‐Lezama R. Extrasynaptic alpha6 subunit‐containing GABAA receptors modulate excitability in turtle spinal motoneurons. PloS One 9: e115378, 2014.
 6.Araki T, Otani T. Response of single motoneurons to direct stimulation in toad's spinal cord. J Neurophysiol 18: 472‐485, 1955.
 7.Araki T, Otani T, Furukawa T. The electrical activities of single motoneurones in toad's spinal cord, recorded with intracellular electrodes. Jpn J Physiol 3: 254‐267, 1953.
 8.Araki T, Terzuolo CA. Membrane currents in spinal motoneurons associated with the action potential and synaptic activity. J Neurophysiol 25: 772‐789, 1962.
 9.Baldissera F, Gustafsson B. Regulation of repetitive firing in motoneurones by the afterhyperpolarization conductance. Brain Research 30: 431‐434, 1971.
 10.Barrett EF, Barret JN. Separation of two voltage‐sensitive potassium currents, and demonstration of a tetrodotoxin‐resistant calcium current in frog motoneurones. J Physiol 255: 737‐774, 1976.
 11.Barrett EF, Barrett JN, Crill WE. Voltage‐sensitive outward currents in cat motoneurones. J Physiol 304: 251‐276, 1980.
 12.Barrett JN, Crill WE. Specific membrane properties of cat motoneurones. J Physiol 239: 301‐324, 1974.
 13.Barrett JN, Crill WE. Voltage clamp of cat motoneurone somata: Properties of the fast inward current. J Physiol 304: 231‐249, 1980.
 14.Barron DH, Matthews BH. The interpretation of potential changes in the spinal cord. J Physiol 92: 276‐321, 1938.
 15.Bautista W, Aguilar J, Loeza‐Alcocer JE, Delgado‐Lezama R. Pre‐ and postsynaptic modulation of monosynaptic reflex by GABAA receptors on turtle spinal cord. J Physiol 588: 2621‐2631, 2010.
 16.Bayliss DA, Umemiya M, Berger AJ. Inhibition of N‐ and P‐type calcium currents and the after‐hyperpolarization in rat motoneurones by serotonin. J Physiol 485(Pt 3): 635‐647, 1995.
 17.Bayliss DA, Viana F, Bellingham MC, Berger AJ. Characteristics and postnatal development of a hyperpolarization‐activated inward current in rat hypoglossal motoneurons in vitro. J Neurophysiol 71: 119‐128, 1994.
 18.Bayliss DA, Viana F, Berger AJ. Mechanisms underlying excitatory effects of thyrotropin‐releasing hormone on rat hypoglossal motoneurons in vitro. J Neurophysiol 68: 1733‐1745, 1992.
 19.Bayliss DA, Viana F, Talley EM, Berger AJ. Neuromodulation of hypoglossal motoneurons: Cellular and developmental mechanisms. Respir Physiol 110: 139‐150, 1997.
 20.Bender KJ, Trussell LO. The physiology of the axon initial segment. Annu Rev Neurosci 35: 249‐265, 2012.
 21.Bennett DJ, Hultborn H, Fedirchuk B, Gorassini M. Short‐term plasticity in hindlimb motoneurons of decerebrate cats. J Neurophysiol 80: 2038‐2045, 1998.
 22.Bennett DJ, Hultborn H, Fedirchuk B, Gorassini M. Synaptic activation of plateaus in hindlimb motoneurons of decerebrate cats. J Neurophysiol 80: 2023‐2037, 1998.
 23.Berg RW, Alaburda A, Hounsgaard J. Balanced inhibition and excitation drive spike activity in spinal half‐centers. Science 315: 390‐393, 2007.
 24.Berg RW, Ditlevsen S, Hounsgaard J. Intense synaptic activity enhances temporal resolution in spinal motoneurons. PloS One 3: e3218, 2008.
 25.Berg AP, Talley EM, Manger JP, Bayliss DA. Motoneurons express heteromeric TWIK‐related acid‐sensitive K+ (TASK) channels containing TASK‐1 (KCNK3) and TASK‐3 (KCNK9) subunits. J Neurosci 24: 6693‐6702, 2004.
 26.Berger AJ, Bayliss DA, Viana F. Modulation of neonatal rat hypoglossal motoneuron excitability by serotonin. Neurosci Lett 143: 164‐168, 1992.
 27.Berger AJ, Bayliss DA, Viana F. Development of hypoglossal motoneurons. J Appl Physiol 81: 1039‐1048, 1996.
 28.Bradley K, Somjen GG. Accommodation in motoneurones of the rat and the cat. J Physiol 156: 75‐92, 1961.
 29.Brocard C, Plantier V, Boulenguez P, Liabeuf S, Bouhadfane M, Viallat‐Lieutaud A, Vinay L, Brocard F. Cleavage of Na(+) channels by calpain increases persistent Na(+) current and promotes spasticity after spinal cord injury. Nat Med 22: 404‐411, 2016.
 30.Brock LG, Coombs JS, Eccles JC. The recording of potentials from motoneurones with an intracellular electrode. J Physiol 117: 431‐460, 1952.
 31.Brock LG, Coombs JS, Eccles JC. Intracellular recording from antidromically activated motoneurones. J Physiol 122: 429‐461, 1953.
 32.Brownstone RM, Jordan LM, Kriellaars DJ, Noga BR, Shefchyk SJ. On the regulation of repetitive firing in lumbar motoneurones during fictive locomotion in the cat. Exp Brain Res 90: 441‐455, 1992.
 33.Brunet T, Arendt D. From damage response to action potentials: Early evolution of neural and contractile modules in stem eukaryotes. Philos Trans R Soc Lond B Biol Sci 371: 20150043, 2016.
 34.Burke RE, Rudomin P. Spinal Neurons and Synapses. Compr Physiol 2011, Supplement 1: Handbook of Physiology, The Nervous System, Cellular Biology of Neurons: 877-944. First published in print 1977. doi: 10.1002/cphy.cp010124.
 35.Calin‐Jageman I, Yu K, Hall RA, Mei L, Lee A. Erbin enhances voltage‐dependent facilitation of Ca(v)1.3 Ca2+ channels through relief of an autoinhibitory domain in the Ca(v)1.3 alpha1 subunit. J Neurosci 27: 1374‐1385, 2007.
 36.Calvin WH, Schwindt PC. Steps in production of motoneuron spikes during rhythmic firing. J Neurophysiol 35: 297‐310, 1972.
 37.Canto‐Bustos M, Loeza‐Alcocer E, Gonzalez‐Ramirez R, Gandini MA, Delgado‐Lezama R, Felix R. Functional expression of T‐type Ca2+ channels in spinal motoneurons of the adult turtle. PloS One 9: e108187, 2014.
 38.Carlen PL, McCrea DAD, Dendrites and motoneuronal integration. In: Davidoff RA, editor. Handbook of the Spinal Cord. New York Basel: Dekker, 1984, pp. 243‐267.
 39.Carlin KP, Bui TV, Dai Y, Brownstone RM. Staircase currents in motoneurons: Insight into the spatial arrangement of calcium channels in the dendritic tree. J Neurosci 29: 5343‐5353, 2009.
 40.Carlin KP, Jones KE, Jiang Z, Jordan LM, Brownstone RM. Dendritic L‐type calcium currents in mouse spinal motoneurons: Implications for bistability. Eur J Neurosci 12: 1635‐1646, 2000.
 41.Chandler SH, Hsaio CF, Inoue T, Goldberg LJ. Electrophysiological properties of guinea pig trigeminal motoneurons recorded in vitro. J Neurophysiol 71: 129‐145, 1994.
 42.Christel C, Lee A. Ca2+‐dependent modulation of voltage‐gated Ca2+ channels. Biochim Biophys Acta 1820: 1243‐1252, 2012.
 43.Conway BA, Hultborn H, Kiehn O, Mintz I. Plateau potentials in alpha‐motoneurones induced by intravenous injection of L‐dopa and clonidine in the spinal cat. J Physiol 405: 369‐384, 1988.
 44.Coombs JS, Curtis DR, Eccles JC. The generation of impulses in motoneurones. J Physiol 139: 232‐249, 1957.
 45.Coombs JS, Curtis DR, Eccles JC. The interpretation of spike potentials of motoneurones. J Physiol 139: 198‐231, 1957.
 46.Coombs JS, Eccles JC, Fatt P. The electrical properties of the motoneurone membrane. J Physiol 130: 291‐325, 1955.
 47.Cotel F, Exley R, Cragg SJ, Perrier JF. Serotonin spillover onto the axon initial segment of motoneurons induces central fatigue by inhibiting action potential initiation. Proc Natl Acad Sci U S A 110: 4774‐4779, 2013.
 48.Cramer NP, Li Y, Keller A. The whisking rhythm generator: A novel mammalian network for the generation of movement. J Neurophysiol 97: 2148‐2158, 2007.
 49.Crill WE. Persistent sodium current in mammalian central neurons. Annu Rev Physiol 58: 349‐362, 1996.
 50.D'Amico JM, Yavuz SU, Saracoglu A, Atis ES, Gorassini MA, Turker KS. Activation properties of trigeminal motoneurons in participants with and without bruxism. J Neurophysiol 110: 2863‐2872, 2013.
 51.D'Arco M, Dolphin AC. L‐type calcium channels: On the fast track to nuclear signaling. Sci Signal 5: pe34, 2012.
 52.Deardorff AS, Romer SH, Sonner PM, Fyffe RE. Swimming against the tide: Investigations of the C‐bouton synapse. Front Neural Circuits 8: 106, 2014.
 53.Delgado‐Lezama R, Perrier JF, Hounsgaard J. Local facilitation of plateau potentials in dendrites of turtle motoneurones by synaptic activation of metabotropic receptors. J Physiol 515(Pt 1): 203‐207, 1999.
 54.Delgado‐Lezama R, Perrier JF, Nedergaard S, Svirskis G, Hounsgaard J. Metabotropic synaptic regulation of intrinsic response properties of turtle spinal motoneurones. J Physiol 504(Pt 1): 97‐102, 1997.
 55.Dixon RE, Moreno CM, Yuan C, Opitz‐Araya X, Binder MD, Navedo MF, Santana LF. Graded Ca(2)(+)/calmodulin‐dependent coupling of voltage‐gated CaV1.2 channels. Elife 4: e05608, 2015.
 56.Dolphin AC. Facilitation of Ca2+ current in excitable cells. Trends Neurosci 19: 35‐43, 1996.
 57.Duflocq A, Chareyre F, Giovannini M, Couraud F, Davenne M. Characterization of the axon initial segment (AIS) of motor neurons and identification of a para‐AIS and a juxtapara‐AIS, organized by protein 4.1B. BMC Biol 9: 66, 2011.
 58.Duflocq A, Le Bras B, Bullier E, Couraud F, Davenne M. Nav1.1 is predominantly expressed in nodes of Ranvier and axon initial segments. Mol Cell Neurosci 39: 180‐192, 2008.
 59.Eccles JC. The Physiology of Nerve Cells. Baltimore: The Johns Hopkins Press, 1957.
 60.Eccles JC, Hoff HE. The rhythmic discharge of motoneurons. Proc Roy Soc B 110: 483‐514, 1932.
 61.Eken T. Spontaneous electromyographic activity in adult rat soleus muscle. J Neurophysiol 80: 365‐376, 1998.
 62.Eken T, Elder GC, Lomo T. Development of tonic firing behavior in rat soleus muscle. J Neurophysiol 99: 1899‐1905, 2008.
 63.Eken T, Kiehn O. Bistable firing properties of soleus motor units in unrestrained rats. Acta Physiol Scand 136: 383‐394, 1989.
 64.Engberg I, Lundberg A, Ryall RW. Is the tonic decerebrate inhibition of reflex paths mediated by monoaminergic pathways? Acta Physiol Scand 72: 123‐133, 1968.
 65.Eyzaguirre C, Kuffler SW. Further study of soma, dendrite, and axon excitation in single neurons. J Gen Physiol 39: 121‐153, 1955.
 66.Farina D, Negro F, Muceli S, Enoka RM. Principles of motor unit physiology evolve with advances in technology. Physiology (Bethesda) 31: 83‐94, 2016.
 67.Fedirchuk B, Dai Y. Monoamines increase the excitability of spinal neurones in the neonatal rat by hyperpolarizing the threshold for action potential production. J Physiol 557: 355‐361, 2004.
 68.Forsythe ID, Redman SJ. The dependence of motoneurone membrane potential on extracellular ion concentrations studied in isolated rat spinal cord. J Physiol 404: 83‐99, 1988.
 69.Foster M.; Sherrington CS. A Textbook of Physiology, Part Three: The Central Nervous System. London: MacMillan, 1897.
 70.Fritzsch B, Glover JC. Evolution of the deuterostome central nervous system: An intercalation of developmental patterning processes with cellular specification processes. In: Kaas JH, editor. Evolution of Nervous Systems. Oxford: Academic Press, 2007, pp. 1‐24.
 71.Fuglevand AJ, Dutoit AP, Johns RK, Keen DA. Evaluation of plateau‐potential‐mediated ‘warm up’ in human motor units. J Physiol 571: 683‐693, 2006.
 72.Fuortes MG, Frank K, Becker MC. Steps in the production of motoneuron spikes. J Gen Physiol 40: 735‐752, 1957.
 73.Gabrielaitis M, Buisas R, Guzulaitis R, Svirskis G, Alaburda A. Persistent sodium current decreases transient gain in turtle motoneurons. Brain Res 1373: 11‐16, 2011.
 74.Gilmore J, Fedirchuk B. The excitability of lumbar motoneurones in the neonatal rat is increased by a hyperpolarization of their voltage threshold for activation by descending serotonergic fibres. J Physiol 558: 213‐224, 2004.
 75.Gorassini M, Bennett DJ, Kiehn O, Eken T, Hultborn H. Activation patterns of hindlimb motor units in the awake rat and their relation to motoneuron intrinsic properties. J Neurophysiol 82: 709‐717, 1999.
 76.Gorassini MA, Bennett DJ, Yang JF. Self‐sustained firing of human motor units. Neurosci Lett 247: 13‐16, 1998.
 77.Gorassini M, Eken T, Bennett DJ, Kiehn O, Hultborn H. Activity of hindlimb motor units during locomotion in the conscious rat. J Neurophysiol 83: 2002‐2011, 2000.
 78.Gorassini MA, Knash ME, Harvey PJ, Bennett DJ, Yang JF. Role of motoneurons in the generation of muscle spasms after spinal cord injury. Brain 127: 2247‐2258, 2004.
 79.Gorassini M, Yang JF, Siu M, Bennett DJ. Intrinsic activation of human motoneurons: Possible contribution to motor unit excitation. J Neurophysiol 87: 1850‐1858, 2002.
 80.Gorassini M, Yang JF, Siu M, Bennett DJ. Intrinsic activation of human motoneurons: Reduction of motor unit recruitment thresholds by repeated contractions. J Neurophysiol 87: 1859‐1866, 2002.
 81.Granit R, Kernell D, Shortess GK. The behaviour of mammalian motoneurones during long‐lasting orthodromic, antidromic and trans‐membrane stimulation. J Physiol 169: 743‐754, 1963.
 82.Granit R, Kernell D, Shortess GK. Quantitative aspects of repetitive firing of mammalian motoneurones, caused by injected currents. J Physiol 168: 911‐931, 1963.
 83.Gregory FD, Pangrsic T, Calin‐Jageman IE, Moser T, Lee A. Harmonin enhances voltage‐dependent facilitation of Cav1.3 channels and synchronous exocytosis in mouse inner hair cells. J Physiol 591: 3253‐3269, 2013.
 84.Grunnet M, Jespersen T, Perrier JF. 5‐HT1A receptors modulate small‐conductance Ca2+‐activated K+ channels. J Neurosci Res 78: 845‐854, 2004.
 85.Guzulaitis R, Hounsgaard J, Alaburda A. Irregular firing and high‐conductance states in spinal motoneurons during scratching and swimming. J Neurosci 36: 5799‐5807, 2016.
 86.Harvey PJ, Li X, Li Y, Bennett DJ. 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 Neurophysiol 96: 1158‐1170, 2006.
 87.Harvey PJ, Li X, Li Y, Bennett DJ. Endogenous monoamine receptor activation is essential for enabling persistent sodium currents and repetitive firing in rat spinal motoneurons. J Neurophysiol 96: 1171‐1186, 2006.
 88.Harvey PJ, Li Y, Li X, Bennett DJ. Persistent sodium currents and repetitive firing in motoneurons of the sacrocaudal spinal cord of adult rats. J Neurophysiol 96: 1141‐1157, 2006.
 89.Heckman CJ, Enoka RM. Motor unit. Compr Physiol 2: 2629‐2682, 2012.
 90.Hounsgaard J, Hultborn H, Jespersen B, Kiehn O. Intrinsic membrane properties causing a bistable behaviour of alpha‐motoneurones. Exp Brain Res 55: 391‐394, 1984.
 91.Hounsgaard J, Hultborn H, Jespersen B, Kiehn O. Bistability of alpha‐motoneurones in the decerebrate cat and in the acute spinal cat after intravenous 5‐hydroxytryptophan. J Physiol 405: 345‐367, 1988.
 92.Hounsgaard J, Kiehn O. Ca++ dependent bistability induced by serotonin in spinal motoneurons. Exp Brain Res 57: 422‐425, 1985.
 93.Hounsgaard J, Kiehn O. Serotonin‐induced bistability of turtle motoneurones caused by a nifedipine‐sensitive calcium plateau potential. J Physiol 414: 265‐282, 1989.
 94.Hounsgaard J, Kiehn O. Calcium spikes and calcium plateaux evoked by differential polarization in dendrites of turtle motoneurones in vitro. J Physiol 468: 245‐259, 1993.
 95.Hounsgaard J, Kiehn O, Mintz I. Response properties of motoneurones in a slice preparation of the turtle spinal cord. J Physiol 398: 575‐589, 1988.
 96.Hounsgaard J, Mintz I. Calcium conductance and firing properties of spinal motoneurones in the turtle. J Physiol 398: 591‐603, 1988.
 97.Hsiao CF, Chandler SH. Characteristics of a fast transient outward current in guinea pig trigeminal motoneurons. Brain Res 695: 217‐226, 1995.
 98.Hsiao CF, Del Negro CA, Trueblood PR, Chandler SH. Ionic basis for serotonin‐induced bistable membrane properties in guinea pig trigeminal motoneurons. J Neurophysiol 79: 2847‐2856, 1998.
 99.Hsiao CF, Trueblood PR, Levine MS, Chandler SH. Multiple effects of serotonin on membrane properties of trigeminal motoneurons in vitro. J Neurophysiol 77: 2910‐2924, 1997.
 100.Hsiao CF, Wu N, Chandler SH. Voltage‐dependent calcium currents in trigeminal motoneurons of early postnatal rats: Modulation by 5‐HT receptors. J Neurophysiol 94: 2063‐2072, 2005.
 101.Hudmon A, Lebel E, Roy H, Sik A, Schulman H, Waxham MN, De Koninck P. A mechanism for Ca2+/calmodulin‐dependent protein kinase II clustering at synaptic and nonsynaptic sites based on self‐association. J Neurosci 25: 6971‐6983, 2005.
 102.Huguenard JR, Hamill OP, Prince DA. Developmental changes in Na +conductances in rat neocortical neurons: Appearance of a slowly inactivating component. J Neurophysiol 59: 778‐795, 1988.
 103.Inoue T, Itoh S, Kobayashi M, Kang Y, Matsuo R, Wakisaka S, Morimoto T. Serotonergic modulation of the hyperpolarizing spike afterpotential in rat jaw‐closing motoneurons by PKA and PKC. J Neurophysiol 82: 626‐637, 1999.
 104.Ireland MF, Funk GD, Bellingham MC. Muscarinic acetylcholine receptors enhance neonatal mouse hypoglossal motoneuron excitability in vitro. J Appl Physiol 113: 1024‐1039, 2012.
 105.Ito M, Oshima T. Temporal summation of after‐hyperpolarization following a motoneurone spike. Nature 195: 910, 1962.
 106.Ito M, Oshima T. Electrical behaviour of the motoneurone membrane during intracellularly applied current steps. J Physiol 180: 607‐635, 1965.
 107.Iwagaki N, Miles GB. Activation of group I metabotropic glutamate receptors modulates locomotor‐related motoneuron output in mice. J Neurophysiol 105: 2108‐2120, 2011.
 108.Jessell TM, Surmeli G, Kelly JS. Motor neurons and the sense of place. Neuron 72: 419‐424, 2011.
 109.Jiang Z, Rempel J, Li J, Sawchuk MA, Carlin KP, Brownstone RM. Development of L‐type calcium channels and a nifedipine‐sensitive motor activity in the postnatal mouse spinal cord. Eur J Neurosci 11: 3481‐3487, 1999.
 110.Katz B. Action potentials from a sensory nerve ending. J Physiol 111: 248‐260, 1950.
 111.Kernell D. The adaptation and the relation between discharge frequency and current strength of cat lumbosacral motoneurones stimulated by long‐lasting injected currents. Acta Physiol Scand 65: 65‐73, 1965.
 112.Kernell D. High‐frequency repetitive firing of cat lumbosacral motoneurones stimulated by long‐lasting injected currents. Acta Physiol Scand 65: 74‐86, 1965.
 113.Kernell D. The limits of firing frequency in cat lumbosacral motoneurones possessing different time course of afterhyperpolarization. Acta Physiol Scand 65: 87‐100, 1965.
 114.Kernell D. Synaptic influence on the repetitive activity elicited in cat lumbosacral motoneurones by long‐lasting injected currents. Acta Physiol Scand 63: 409‐410, 1965.
 115.Kernell D. The Motoneurone and its Muscle Fibres. Oxford New York: Oxford University Press, 2006.
 116.Kiehn O, Eken T. Prolonged firing in motor units: Evidence of plateau potentials in human motoneurons? J Neurophysiol 78: 3061‐3068, 1997.
 117.Kjaerulff O, Kiehn O. 5‐HT modulation of multiple inward rectifiers in motoneurons in intact preparations of the neonatal rat spinal cord. J Neurophysiol 85: 580‐593, 2001.
 118.Koschak A, Reimer D, Huber I, Grabner M, Glossmann H, Engel J, Striessnig J. alpha 1D (Cav1.3) subunits can form l‐type Ca2+ channels activating at negative voltages. J Biol Chem 276: 22100‐22106, 2001.
 119.Krawitz S, Fedirchuk B, Dai Y, Jordan LM, McCrea DA. State‐dependent hyperpolarization of voltage threshold enhances motoneurone excitability during fictive locomotion in the cat. J Physiol 532: 271‐281, 2001.
 120.Kuo JJ, Lee RH, Zhang L, Heckman CJ. Essential role of the persistent sodium current in spike initiation during slowly rising inputs in mouse spinal neurones. J Physiol 574: 819‐834, 2006.
 121.Lape R, Nistri A. Voltage‐activated K+ currents of hypoglossal motoneurons in a brain stem slice preparation from the neonatal rat. J Neurophysiol 81: 140‐148, 1999.
 122.Lape R, Nistri A. Current and voltage clamp studies of the spike medium afterhyperpolarization of hypoglossal motoneurons in a rat brain stem slice preparation. J Neurophysiol 83: 2987‐2995, 2000.
 123.Lape R, Nistri A. Characteristics of fast Na(+) current of hypoglossal motoneurons in a rat brainstem slice preparation. Eur J Neurosci 13: 763‐772, 2001.
 124.Larkman PM, Kelly JS. Ionic mechanisms mediating 5‐hydroxytryptamine‐ and noradrenaline‐evoked depolarization of adult rat facial motoneurones. J Physiol 456: 473‐490, 1992.
 125.Larkman PM, Kelly JS. Characterization of 5‐HT‐sensitive potassium conductances in neonatal rat facial motoneurones in vitro. J Physiol 508(Pt 1): 67‐81, 1998.
 126.Larkman PM, Kelly JS, Takahashi T. Adenosine 3′:5′‐cyclic monophosphate mediates a 5‐hydroxytryptamine‐induced response in neonatal rat motoneurones. Pflugers Arch 430: 763‐769, 1995.
 127.Larkman PM, Perkins EM. A TASK‐like pH‐ and amine‐sensitive ‘leak’ K+ conductance regulates neonatal rat facial motoneuron excitability in vitro. Eur J Neurosci 21: 679‐691, 2005.
 128.Lazarenko RM, Willcox SC, Shu S, Berg AP, Jevtovic‐Todorovic V, Talley EM, Chen X, Bayliss DA. Motoneuronal TASK channels contribute to immobilizing effects of inhalational general anesthetics. J Neurosci 30: 7691‐7704, 2010.
 129.Le Bras B, Freal A, Czarnecki A, Legendre P, Bullier E, Komada M, Brophy PJ, Davenne M, Couraud F. In vivo assembly of the axon initial segment in motor neurons. Brain Struct Funct 219: 1433‐1450, 2014.
 130.Lee RH, Heckman CJ. Influence of voltage‐sensitive dendritic conductances on bistable firing and effective synaptic current in cat spinal motoneurons in vivo. J Neurophysiol 76: 2107‐2110, 1996.
 131.Lee RH, Heckman CJ. Enhancement of bistability in spinal motoneurons in vivo by the noradrenergic alpha1 agonist methoxamine. J Neurophysiol 81: 2164‐2174, 1999.
 132.Lee RH, Heckman CJ. Essential role of a fast persistent inward current in action potential initiation and control of rhythmic firing. J Neurophysiol 85: 472‐475, 2001.
 133.Lesage F, Reyes R, Fink M, Duprat F, Guillemare E, Lazdunski M. Dimerization of TWIK‐1 K+ channel subunits via a disulfide bridge. EMBO J 15: 6400‐6407, 1996.
 134.Li Y, Bennett DJ. Persistent sodium and calcium currents cause plateau potentials in motoneurons of chronic spinal rats. J Neurophysiol 90: 857‐869, 2003.
 135.Li X, Bennett DJ. Apamin‐sensitive calcium‐activated potassium currents (SK) are activated by persistent calcium currents in rat motoneurons. J Neurophysiol 97: 3314‐3330, 2007.
 136.Li Y, Gorassini MA, Bennett DJ. Role of persistent sodium and calcium currents in motoneuron firing and spasticity in chronic spinal rats. J Neurophysiol 91: 767‐783, 2004.
 137.Li Y, Li X, Harvey PJ, Bennett DJ. Effects of baclofen on spinal reflexes and persistent inward currents in motoneurons of chronic spinal rats with spasticity. J Neurophysiol 92: 2694‐2703, 2004.
 138.Li X, Murray K, Harvey PJ, Ballou EW, Bennett DJ. Serotonin facilitates a persistent calcium current in motoneurons of rats with and without chronic spinal cord injury. J Neurophysiol 97: 1236‐1246, 2007.
 139.Lichtneckert RR, Reichert H. Origin and evolution of the first nervous system. In: Kaas JH, editor. Evolution of Nervous Systems. Academic Press, 2007, pp. 289‐315.
 140.Lintz TL. Primitive Nervous Systems. New Haven and London: Yale University Press, 1968.
 141.Llinas RR. I of the Vortex, from Neurons to Self. Cambridge, MA: MIT Press, 2002.
 142.Lux HD, Schubert P. Some aspects of the electroanatomy of dendrites. Adv Neurol 12: 29‐44, 1975.
 143.Miles GB, Dai Y, Brownstone RM. Mechanisms underlying the early phase of spike frequency adaptation in mouse spinal motoneurones. J Physiol 566: 519‐532, 2005.
 144.Miles GB, Hartley R, Todd AJ, Brownstone RM. Spinal cholinergic interneurons regulate the excitability of motoneurons during locomotion. Proc Natl Acad Sci U S A 104: 2448‐2453, 2007.
 145.Moreno CM, Dixon RE, Tajada S, Yuan C, Opitz‐Araya X, Binder MD, Santana LF. Ca(2+) entry into neurons is facilitated by cooperative gating of clustered CaV1.3 channels. Elife 5: e15744, 2016.
 146.Moritz AT, Newkirk G, Powers RK, Binder MD. Facilitation of somatic calcium channels can evoke prolonged tail currents in rat hypoglossal motoneurons. J Neurophysiol 98: 1042‐1047, 2007.
 147.Mosfeldt Laursen A, Rekling JC. Electrophysiological properties of hypoglossal motoneurons of guinea‐pigs studied in vitro. Neuroscience 30: 619‐637, 1989.
 148.Murray KC, Nakae A, Stephens MJ, Rank M, D'Amico J, Harvey PJ, Li X, Harris RL, Ballou EW, Anelli R, Heckman CJ, Mashimo T, Vavrek R, Sanelli L, Gorassini MA, Bennett DJ, Fouad K. Recovery of motoneuron and locomotor function after spinal cord injury depends on constitutive activity in 5‐HT2C receptors. Nat Med 16: 694‐700, 2010.
 149.Murray KC, Stephens MJ, Ballou EW, Heckman CJ, Bennett DJ. Motoneuron excitability and muscle spasms are regulated by 5‐HT2B and 5‐HT2C receptor activity. J Neurophysiol 105: 731‐748, 2011.
 150.Nelson PG, Lux HD. Some electrical measurements of motoneuron parameters. Biophys J 10: 55‐73, 1970.
 151.Nishimura Y, Schwindt PC, Crill WE. Electrical properties of facial motoneurons in brainstem slices from guinea pig. Brain Res 502: 127‐142, 1989.
 152.Numata JM, van Brederode JF, Berger AJ. Lack of an endogenous GABAA receptor‐mediated tonic current in hypoglossal motoneurons. J Physiol 590: 2965‐2976, 2012.
 153.Pan Z, Kao T, Horvath Z, Lemos J, Sul JY, Cranstoun SD, Bennett V, Scherer SS, Cooper EC. A common ankyrin‐G‐based mechanism retains KCNQ and NaV channels at electrically active domains of the axon. J Neurosci 26: 2599‐2613, 2006.
 154.Parker GH. The Elementary Nervous System. Philadelphia and London: J.B. Lippincott Company, 1919.
 155.Parkis MA, Bayliss DA, Berger AJ. Actions of norepinephrine on rat hypoglossal motoneurons. J Neurophysiol 74: 1911‐1919, 1995.
 156.Parkis MA, Berger AJ. Clonidine reduces hyperpolarization‐activated inward current (Ih) in rat hypoglossal motoneurons. Brain Res 769: 108‐118, 1997.
 157.Patel AJ, Honore E, Lesage F, Fink M, Romey G, Lazdunski M. Inhalational anesthetics activate two‐pore‐domain background K+ channels. Nat Neurosci 2: 422‐426, 1999.
 158.Perreault MC. Motoneurons have different membrane resistance during fictive scratching and weight support. J Neurosci 22: 8259‐8265, 2002.
 159.Perrier JF, Alaburda A, Hounsgaard J. Spinal plasticity mediated by postsynaptic L‐type Ca2+ channels. Brain Res Brain Res Rev 40: 223‐229, 2002.
 160.Perrier JF, Alaburda A, Hounsgaard J. 5‐HT1A receptors increase excitability of spinal motoneurons by inhibiting a TASK‐1‐like K+ current in the adult turtle. J Physiol 548: 485‐492, 2003.
 161.Perrier JF, Cotel F. Serotonin differentially modulates the intrinsic properties of spinal motoneurons from the adult turtle. J Physiol 586: 1233‐1238, 2008.
 162.Perrier JF, Delgado‐Lezama R. Synaptic release of serotonin induced by stimulation of the raphe nucleus promotes plateau potentials in spinal motoneurons of the adult turtle. J Neurosci 25: 7993‐7999, 2005.
 163.Perrier JF, Hounsgaard J. Development and regulation of response properties in spinal cord motoneurons. Brain Res Bull 53: 529‐535, 2000.
 164.Perrier JF, Hounsgaard J. 5‐HT2 receptors promote plateau potentials in turtle spinal motoneurons by facilitating an L‐type calcium current. J Neurophysiol 89: 954‐959, 2003.
 165.Perrier JF, Mejia‐Gervacio S, Hounsgaard J. Facilitation of plateau potentials in turtle motoneurones by a pathway dependent on calcium and calmodulin. J Physiol 528(Pt 1): 107‐113, 2000.
 166.Perrier JF, Rasmussen HB, Christensen RK, Petersen AV. Modulation of the intrinsic properties of motoneurons by serotonin. Curr Pharm Des 19: 4371‐4384, 2013.
 167.Petersen AV, Cotel F, Perrier JF. Plasticity of the axon initial segment: Fast and slow processes with multiple functional roles. Neuroscientist 2016. doi: 10.1177/1073858416648311.
 168.Phillis JW, Tebecis AK, York DH. Depression of spinal motoneurones by noradrenaline, 5‐hydroxytryptamine and histamine. Eur J Pharmacol 4: 471‐475, 1968.
 169.Power KE, Carlin KP, Fedirchuk B. Modulation of voltage‐gated sodium channels hyperpolarizes the voltage threshold for activation in spinal motoneurones. Exp Brain Res 217: 311‐322, 2012.
 170.Power KE, McCrea DA, Fedirchuk B. Intraspinally mediated state‐dependent enhancement of motoneurone excitability during fictive scratch in the adult decerebrate cat. J Physiol 588: 2839‐2857, 2010.
 171.Powers RK, Binder MD. Input‐output functions of mammalian motoneurons. Rev Physiol Biochem Pharmacol 143: 137‐263, 2001.
 172.Powers RK, Binder MD. Persistent sodium and calcium currents in rat hypoglossal motoneurons. J Neurophysiol 89: 615‐624, 2003.
 173.Powers RK, Sawczuk A, Musick JR, Binder MD. Multiple mechanisms of spike‐frequency adaptation in motoneurones. J Physiol Paris 93: 101‐114, 1999.
 174.Rall W. Branching dendritic trees and motoneuron membrane resistivity. Exp Neurol 1: 491‐527, 1959.
 175.Rall W. Membrane potential transients and membrane time constant of motoneurons. Exp Neurol 2: 503‐532, 1960.
 176.Rall W. Core Conductor Theory and Cable Properties of Neurons. Compr Physiol 2011, Supplement 1: Handbook of Physiology, The Nervous System, Cellular Biology of Neurons: 39-97. First published in print 1977. doi: 10.1002/cphy.cp010103.
 177.Rall W, Burke RE, Holmes WR, Jack JJ, Redman SJ, Segev I. Matching dendritic neuron models to experimental data. Physiol Rev 72: S159‐186, 1992.
 178.Rall W, Burke RE, Smith TG, Nelson PG, Frank K. Dendritic location of synapses and possible mechanisms for the monosynaptic EPSP in motoneurons. J Neurophysiol 30: 1169‐1193, 1967.
 179.Ramón y Cajal S. The Croonian Lecture. La fine structure des centres nerveux. Proc R Soc Lond B 55: 444‐468, 1894.
 180.Rasband MN. The axon initial segment and the maintenance of neuronal polarity. Nat Rev Neurosci 11: 552‐562, 2010.
 181.Redman SJ. The attenuation of passively propagating dendritic potentials in a motoneurone cable model. J Physiol 234: 637‐664, 1973.
 182.Rekling JC, Funk GD, Bayliss DA, Dong XW, Feldman JL. Synaptic control of motoneuronal excitability. Physiol Rev 80: 767‐852, 2000.
 183.Romanes GJ. The motor cell columns of the lumbo‐sacral spinal cord of the cat. J Comp Neurol 94: 313‐363, 1951.
 184.Safronov BV, Vogel W. Single voltage‐activated Na+ and K+ channels in the somata of rat motoneurones. J Physiol 487(Pt 1): 91‐106, 1995.
 185.Safronov BV, Vogel W. Large conductance Ca(2+)‐activated K+ channels in the soma of rat motoneurones. J Membr Biol 162: 9‐15, 1998.
 186.Safronov BV, Wolff M, Vogel W. Excitability of the soma in central nervous system neurons. Biophys J 78: 2998‐3010, 2000.
 187.Schwindt PC. Membrane‐potential trajectories underlying motoneuron rhythmic firing at high rates. J Neurophysiol 36: 434‐439, 1973.
 188.Schwindt PC, Calvin WH. Membrane‐potential trajectories between spikes underlying motoneuron firing rates. J Neurophysiol 35: 311‐325, 1972.
 189.Schwindt P, Crill WE. A persistent negative resistance in cat lumbar motoneurons. Brain Res 120: 173‐178, 1977.
 190.Schwindt P, Crill W. Role of a persistent inward current in motoneuron bursting during spinal seizures. J Neurophysiol 43: 1296‐1318, 1980.
 191.Schwindt PC, Crill WE. Effects of barium on cat spinal motoneurons studied by voltage clamp. J Neurophysiol 44: 827‐846, 1980.
 192.Schwindt PC, Crill WE. Properties of a persistent inward current in normal and TEA‐injected motoneurons. J Neurophysiol 43: 1700‐1724, 1980.
 193.Schwindt PC, Crill WE. Differential effects of TEA and cations on outward ionic currents of cat motoneurons. J Neurophysiol 46: 1‐16, 1981.
 194.Schwindt PC, Crill WE. Factors influencing motoneuron rhythmic firing: Results from a voltage‐clamp study. J Neurophysiol 48: 875‐890, 1982.
 195.Schwindt PC, Crill WE. Membrane properties of cat motoneurons. In: Davidoff RA, editor. Handbook of the Spinal Cord. New York, Basel: Marcel Dekker, 1984.
 196.Sherrington CS. Correlation of reflexes and the principle of the common path. In: Report of the British Association for the Advancement of Science 74th Meeting Cambridge. London: John Murray, Albemarle Street, 1904, pp. 728‐741.
 197.Simon M, Perrier JF, Hounsgaard J. Subcellular distribution of L‐type Ca2+ channels responsible for plateau potentials in motoneurons from the lumbar spinal cord of the turtle. Eur J Neurosci 18: 258‐266, 2003.
 198.Sirois JE, Lei Q, Talley EM, Lynch C, III, Bayliss DA. The TASK‐1 two‐pore domain K+ channel is a molecular substrate for neuronal effects of inhalation anesthetics. J Neurosci 20: 6347‐6354, 2000.
 199.Skydsgaard M, Hounsgaard J. Multiple actions of iontophoretically applied serotonin on motorneurones in the turtle spinal cord in vitro. Acta Physiol Scand 158: 301‐310, 1996.
 200.Svirskis G, Baginskas A, Hounsgaard J, Gutman A. Electrotonic measurements by electric field‐induced polarization in neurons: Theory and experimental estimation. Biophys J 73: 3004‐3015, 1997.
 201.Svirskis G, Gutman A, Hounsgaard J. Electrotonic structure of motoneurons in the spinal cord of the turtle: Inferences for the mechanisms of bistability. J Neurophysiol 85: 391‐398, 2001.
 202.Svirskis G, Hounsgaard J. Depolarization‐induced facilitation of a plateau‐generating current in ventral horn neurons in the turtle spinal cord. J Neurophysiol 78: 1740‐1742, 1997.
 203.Svirskis G, Hounsgaard J. Transmitter regulation of plateau properties in turtle motoneurons. J Neurophysiol 79: 45‐50, 1998.
 204.Taddese A, Bean BP. Subthreshold sodium current from rapidly inactivating sodium channels drives spontaneous firing of tuberomammillary neurons. Neuron 33: 587‐600, 2002.
 205.Takahashi T, Berger AJ. Direct excitation of rat spinal motoneurones by serotonin. J Physiol 423: 63‐76, 1990.
 206.Talley EM, Bayliss DA. Modulation of TASK‐1 (Kcnk3) and TASK‐3 (Kcnk9) potassium channels: Volatile anesthetics and neurotransmitters share a molecular site of action. J Biol Chem 277: 17733‐17742, 2002.
 207.Talley EM, Lei Q, Sirois JE, Bayliss DA. TASK‐1, a two‐pore domain K+ channel, is modulated by multiple neurotransmitters in motoneurons. Neuron 25: 399‐410, 2000.
 208.Talley EM, Sadr NN, Bayliss DA. Postnatal development of serotonergic innervation, 5‐HT1A receptor expression, and 5‐HT responses in rat motoneurons. J Neurosci 17: 4473‐4485, 1997.
 209.Terzuolo CA, Araki T. An analysis of intra‐ versus extracellular potential changes associated with activity of single spinal motoneurons. Ann NY Acad Sci 94: 547‐558, 1961.
 210.Thurbon D, Luscher HR, Hofstetter T, Redman SJ. Passive electrical properties of ventral horn neurons in rat spinal cord slices. J Neurophysiol 79: 2485‐2502, 1998.
 211.Umemiya M, Berger AJ. Properties and function of low‐ and high‐voltage‐activated Ca2+ channels in hypoglossal motoneurons. J Neurosci 14: 5652‐5660, 1994.
 212.Venugopal S, Hamm TM, Crook SM, Jung R. Modulation of inhibitory strength and kinetics facilitates regulation of persistent inward currents and motoneuron excitability following spinal cord injury. J Neurophysiol 106: 2167‐2179, 2011.
 213.Venugopal S, Hamm TM, Jung R. Differential contributions of somatic and dendritic calcium‐dependent potassium currents to the control of motoneuron excitability following spinal cord injury. Cogn Neurodyn 6: 283‐293, 2012.
 214.Viana F, Bayliss DA, Berger AJ. Calcium conductances and their role in the firing behavior of neonatal rat hypoglossal motoneurons. J Neurophysiol 69: 2137‐2149, 1993.
 215.Viana F, Bayliss DA, Berger AJ. Multiple potassium conductances and their role in action potential repolarization and repetitive firing behavior of neonatal rat hypoglossal motoneurons. J Neurophysiol 69: 2150‐2163, 1993.
 216.Viana F, Bayliss DA, Berger AJ. Repetitive firing properties of developing rat brainstem motoneurones. J Physiol 486(Pt 3): 745‐761, 1995.
 217.Walton K, Fulton BP. Ionic mechanisms underlying the firing properties of rat neonatal motoneurons studied in vitro. Neuroscience 19: 669‐683, 1986.
 218.Walton KW, Slaney G, Ashton F. Atherosclerosis in vascular grafts for peripheral vascular disease. Part 2. Synthetic arterial prostheses. Atherosclerosis 61: 155‐167, 1986.
 219.Washizu Y. The effect of TEA on the electrical activities of spinal motoneurons. Jpn J Physiol 9: 311‐321, 1959.
 220.Westenbroek RE, Hoskins L, Catterall WA. Localization of Ca2+ channel subtypes on rat spinal motor neurons, interneurons, and nerve terminals. J Neurosci 18: 6319‐6330, 1998.
 221.Witts EC, Zagoraiou L, Miles GB. Anatomy and function of cholinergic C bouton inputs to motor neurons. J Anat 224: 52‐60, 2014.
 222.Xu XF, Tsai HJ, Li L, Chen YF, Zhang C, Wang GF. Modulation of leak K(+) channel in hypoglossal motoneurons of rats by serotonin and/or variation of pH value. Sheng Li Xue Bao 61: 305‐316, 2009.
 223.Zhang L, Krnjevic K. Apamin depresses selectively the after‐hyperpolarization of cat spinal motoneurons. Neurosci Lett 74: 58‐62, 1987.
 224.Zhang M, Moller M, Broman J, Sukiasyan N, Wienecke J, Hultborn H. Expression of calcium channel CaV1.3 in cat spinal cord: Light and electron microscopic immunohistochemical study. J Comp Neurol 507: 1109‐1127, 2008.
 225.Ziskind‐Conhaim L, Seebach BS, Gao BX. Changes in serotonin‐induced potentials during spinal cord development. J Neurophysiol 69: 1338‐1349, 1993.

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Article Title: Motor Neurons
 

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Jorn Hounsgaard. Motor Neurons. Compr Physiol 2017, 7: 463-484. doi: 10.1002/cphy.c160025