Motor Neurons and Spinal Control of Movement

Abstract

Motor neurons are among the largest neurons in the central nervous system and have long axons that travel along peripheral nerves to innervate skeletal muscles. They are the final common pathway through which the brain controls bodily movement. Motor neurons receive excitatory and inhibitory synaptic inputs from sensory afferents and from pathways of supraspinal origin either directly or via interneurons. The intrinsic properties of motor neurons determine how these inputs are transformed into a sequence of action potentials that elicit muscle contraction. Motor neuron intrinsic properties are affected by neuromodulatory inputs from supraspinal and spinal pathways. Motor neurons are recruited in ways that make effective use of the muscle fibres they innervate. All motor actions – whether stereotyped behaviours (such as locomotion or withdrawal reflexes), or uniquely specified sequences of muscle contraction – reflect the interaction of supraspinal commands, sensory inputs and spinal cord interneurons.

Key Concepts:

  • Motor neurons are large neurons in the brainstem and spinal cord that innervate skeletal muscle; those innervating the same muscle are grouped in proximity to form a motor neuron pool.

  • The electrophysiological properties of an individual motor neuron are appropriately matched to the contractile properties of the muscle fibres it innervates; together, a motor neuron and its muscle fibres form a motor unit.

  • Motor neurons receive two types of synaptic inputs from descending pathways, spinal interneurons and segmental afferents: (1) excitatory and inhibitory inputs that directly affect membrane potential and (2) neuromodulatory inputs that alter the effects of the excitatory and inhibitory inputs on membrane potential.

  • The intrinsic properties of a motor neuron and the neuromodulatory influences it receives determine how its excitatory and inhibitory synaptic inputs are translated into a firing pattern that elicits muscle contraction.

  • Motor neurons are recruited in a stereotyped order according to the ‘size principle’, in which low‐force motor units are activated first, and sequentially higher force motor units are subsequently added to produce the total muscle force appropriate for the current action.

  • Networks (often called central pattern generators) composed of spinal interneurons support locomotion and other cyclical movement patterns by distributing rhythmic synaptic activity among different motor neuron pools in appropriate temporal sequences.

Keywords: spinal cord; motoneuron; motor neuron; reflex; movement; motor control; neuromodulation

Figure 1.

(a) Motor neuron nuclei of cat medial gastrocnemius (MG) and soleus (SOL) muscles. Right: Dorsal view of spinal cord with positions (dots) of MG (left hemicord) and SOL (right hemicord) motor neurons shown. L6–L7 and L7–S1 segmental boundaries are indicated by horizontal heavy lines. Vertical dashed line indicates midline. Horizontal dashed lines (A–E) indicate levels of cross sections shown on the left. In these sections, heavy lines are the grey–white matter boundaries and light lines are the cord boundaries. Neurons (dots) shown at each level are within 300 μm of that level. Modified from Burke et al.. (b) Reconstruction of cat triceps surae motor neuron. The solid line is the lateral boundary of the spinal cord (ventral is towards the bottom) and the dashed line is the border of the grey matter. Note that numerous dendrites enter the white matter. The dashed line emerging from the soma is the axon. Modified from Brown and Fyffe .

Figure 2.

(a) Tension produced by cat gastrocnemius motor units of three different types during 40 s−1 tetani, each lasting 330 ms and repeated once per second for the time shown. The fast fatiguable unit is strong and fatigues quickly, the slow unit is weak and does not fatigue, and the fast fatigue‐resistant unit has intermediate properties. Modified from Burke et al.. (b) Steady‐state firing rates of human extensor digitorum communis motor units versus total force. As force rises, motor units begin firing and those already firing increase their rates. Modified from Monster and Chan .

Figure 3.

Amplification and prolongation of synaptic input (generated by 1.5 s of high‐frequency activation of monosynaptic muscle spindle Ia afferent input) by the persistent inward current (PIC) in a low‐threshold, slow motor neuron. The current traces in panels A and B were recorded using the voltage‐clamp technique, in which a target voltage level is maintained by injecting (and recording) current through the electrode into the cell; the voltage traces in panel C were recorded under unclamped conditions. (a) At a hyperpolarised holding potential (−90 mV; green trace), this input produced a steady current with a sharp onset and offset. At a depolarised holding potential (∼−55 mV; red trace), the very same input is greatly amplified and prolonged by the PIC. Baseline holding currents are removed to allow the traces to be superimposed. (b) The difference between the currents in (a) reflects the net contribution of the PIC. (c) In unclamped conditions, the same input produces a steady excitatory postsynaptic potential (EPSP) at hyperpolarised levels (∼−90 mV). At a more depolarised level (−70 mV), the same input evokes intense repetitive firing, followed by continued, self‐sustained firing at a lower level when the input is removed. The voltage traces are shown on an expanded vertical scale (which truncates the peaks of the action potentials) to highlight the difference in response at the two voltage levels. Adapted from Heckman CJ, Johnson M, Mottram C and Schuster J (2008) Persistent inward currents in spinal motoneurons and their influence on human motoneuron firing patterns. Neuroscientist14(3):12. With permission from Sage Publications.

Figure 4.

(a) Triphasic pattern of muscle contraction (i.e. rectified electromyographic (EMG) activity) associated with a rapid voluntary limb movement. First, activation of the agonist muscle accelerates the limb to maximum velocity. Then, agonist activity ceases and antagonist activation stops the limb. Finally, agonist activation stabilises the limb and maintains the new position. Modified from Ghez . (b) Average rectified EMG response of human wrist extensor muscles to sudden flexion of the wrist (indicated by change in wrist angle trace). Vertical line indicates beginning of flexion torque. The individual had been instructed to return the handle to its initial position as quickly as possible. The series of EMG peaks reflects the succession of monosynaptic segmental excitation of the motor neuron, oligosynaptic segmental and suprasegmental excitation, and purely voluntary excitation. Modified from Lee and Tatton .

Figure 5.

Treadmill location in a cat in which transection of the thoracic spinal cord has isolated the lumbosacral segments. After recovery from surgery, placement on the treadmill induces reciprocal activation of hind limb extensor and flexor muscles which produces relatively normal stance and swing phases of walking. Modified from Pearson .

close

References

Alaburda A, Russo R, MacAulay N and Hounsgaard J (2005) Periodic high‐conductance states in spinal neurons during scratch‐like network activity in adult turtles. Journal of Neuroscience 25: 6316–6321.

Baldissera F, Hultborn H and Illert M (1981) Integration in spinal neuronal systems. In: Brooks VB (ed.) Handbook of Physiology, sect. I: The Nervous System, vol. II: Motor Control, part I, pp. 509–595. Baltimore: Williams and Wilkins.

Brown AG and Fyffe RE (1981) Direct observations on the contacts made between Ia afferent fibres and alpha‐motoneurones in the cat's lumbosacral spinal cord. Journal of Physiology (London) 313: 121–140.

Brown TG (1911) The intrinsic factors in the act of progression in the mammal. Proceedings of the Royal Society of London. Series B: Biological Sciences 84: 308–319.

Burke RE (1981) Motor units: anatomy, physiology, and functional organization. In: Brooks VB (ed.) Handbook of Physiology, sect. I: The Nervous System, vol. II: Motor Control, part I, pp. 345–422. Baltimore: Williams and Wilkins.

Burke RE (1998) Spinal cord: ventral horn. In: Shepherd GM (ed.) The Synaptic Organization of the Brain, pp. 77–120. New York: Oxford University Press.

Burke RE, Levine DN, Tsairis P and Zajac FE III (1973) Physiological types and histochemical profiles in motor units of cat gastrocnemius. Journal of Physiology (London) 234: 723–748.

Burke RE, Strick PL, Kanda K, Kim CC and Walmsley B (1977) Anatomy of medial gastrocnemius and soleus motor nuclei in cat spinal cord. Journal of Neurophysiology 40: 667–680.

Capaday C and Stein RB (1986) Amplitude modulation of the soleus H‐reflex in the human during walking and standing. Journal of Neuroscience 6: 1308–1313.

Capaday C and Stein RB (1987) Difference in the amplitude of the human soleus H reflex during walking and running. Journal of Physiology (London) 392: 513–522.

Cifra A, Nani F, Sharifullina E and Nistri A (2009) A repertoire of rhythmic bursting produced by hypoglossal motoneurons in physiological and pathological conditions. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 364: 2493–2500.

DeJong RN and Haerer AF (1998) Case taking and the neurologic examination. In: Joynt RJ and Griggs RC (eds.) Clinical Neurology, vol. I, pp. 1–89. Philadelphia: Lippincott‐Raven.

Delgado‐Lezama R, Perrier JF, Nedergaard S, Svirskis G and Hounsgaard J (1997) Metabotropic synaptic regulation of intrinsic response properties of turtle spinal motoneurones. Journal of Physiology 504: 97–102.

Duysens J and van der Crommert HWAA (1998) Neural control of locomotion. Part 1: the central pattern generator from cats to humans. Gait and Posture 7: 131–141.

Ghez C (1991) Muscles: effectors of the motor systems. In: Kandel ER, Schwartz JH and Jessell TM (eds) Principles of Neural Science, pp. 548–563. New York: Elsevier.

Grillner S (1981) Control of locomotion in bipeds, tetrapods, and fish. In: Brooks VB (ed.) Handbook of Physiology, sect. I: The Nervous System, vol. II: Motor Control, part II, pp. 1179–1236. Baltimore: Williams and Wilkins.

Harvey PJ, Li X, Li Y and Bennett DJ (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. Journal of Neurophysiology 96: 1158–1170.

Heckmann CJ, Gorassini MA and Bennett DJ (2005) Persistent inward currents in motoneuron dendrites: implications for motor output. Muscle & Nerve 31: 135–156.

Henneman E and Mendell LM (1981) Functional organization of motoneuron pool and inputs. In: Brooks VB (ed.), Handbook of Physiology, sect. I: The Nervous System, vol. II: Motor Control, part I, pp. 423–507. Baltimore: Williams and Wilkins.

Holstege JC and Kuypers HGJM (1987) Brainstem projections to spinal motoneurons: an update. Neuroscience 23: 809–821.

Hyngstrom AS, Johnson MD, Miller JF and Heckman CJ (2007) Intrinsic electrical properties of spinal motoneurons vary with joint angle. Nature Neuroscience 10: 363–369.

Jacobs BL and Fornal CA (1997) Serotonin and motor activity. Current Opinion in Neurobiology 7: 820–825.

Jankowska E (1992) Interneuronal relay in spinal pathways from proprioceptors. Progress in Neurobiology 38: 335–378.

Kernell D (2006) The Motoneurone and Its Muscle Fibres. New York: Oxford University Press.

Krawitz S, Fedirchuk B, Dai Y, Jordan LM and McCrea DA (2001) State‐dependent hyperpolarization of voltage threshold enhances motoneurone excitability during fictive locomotion in the cat. Journal of Physiology 532: 271–281.

Kuypers HGJM (1981) Anatomy of the descending pathways. In: Brooks VB (ed.) Handbook of Physiology, sect. I: The Nervous System, vol. II: Motor Control, part I, pp. 597–666. Baltimore: Williams and Wilkins.

Lee RG and Tatton WG (1978) Long loop reflexes in man: clinical applications. In: Desmedt JE (ed.) Cerebral Motor Control in Man: Long Loop Mechanisms, pp. 320–333. Basel: Karger.

Lee RH and Heckman CJ (1999) Enhancement of bistability in spinal motoneurons in vivo by the noradrenergic alpha1 agonist methoxamine. Journal of Neurophysiology 81: 2164–2174.

Lesage F (2003) Pharmacology of neuronal background potassium channels. Neuropharmacology 44: 1–7.

Monster AW and Chan H (1977) Isometric force production by motor units of extensor digitorum communis muscle in man. Journal of Neurophysiology 40: 1432–1443.

Pearson K (1976) The control of walking. Scientific American 235: 72–86.

Perrier JF and Hounsgaard J (2003) 5‐HT2 receptors promote plateau potentials in turtle spinal motoneurons by facilitating an L‐type calcium current. Journal of Neurophysiology 89: 954–959.

Perrier JF and Tresch MC (2005) Recruitment of motor neuronal persistent inward currents shapes withdrawal reflexes in the frog. Journal of Physiology 562: 507–520.

Powers RK and Binder MD (2001) Input‐output functions of mammalian motoneurons. Reviews of Physiology, Biochemistry and Pharmacology 143: 137–263.

Rekling JC, Funk GD, Bayliss DA, Dong XW and Feldman JL (2000) Synaptic control of motoneuronal excitability. Physiological Reviews 80: 767–852.

Svirskis G and Hounsgaard J (1998) Transmitter regulation of plateau properties in turtle motoneurons. Journal of Neurophysiology 79: 45–50.

Van de Crommert HWAA, Mulder T and Duysens J (1998) Neural control of locomotion – sensory control of the central pattern generator and its relation to treadmill training. Gait and Posture 7: 251–263.

Zagoraiou L, Akay T, Martin JF et al. (2009) A cluster of cholinergic premotor interneurons modulates mouse locomotor activity. Neuron 64: 645–662.

Further Reading

Brooks VB (1981) Handbook of Physiology, sect. I: The Nervous System, vol. II: Motor Control, part I. Baltimore: Williams and Wilkins.

Brown AG (1981) Organization in the Spinal Cord. Berlin: Springer.

Kandel ER, Schwartz JH and Jessell TM (1991) Principles of Neural Science. New York: Elsevier.

Rothwell J (1994) Control of Human Voluntary Movement. New York: Chapman and Hall.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Carp, Jonathan S, and Wolpaw, Jonathan R(Jun 2010) Motor Neurons and Spinal Control of Movement. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000156.pub2]