|Robert E. Burke (2008), Scholarpedia, 3(4):1925.||doi:10.4249/scholarpedia.1925||revision #87911 [link to/cite this article]|
All vertebrate animals have spinal cords. Phylogenetically, it is the oldest part of the central nervous system (CNS). In contrast to the more recently evolved cerebral and cerebellar hemispheres of the brain, the cell bodies and dendrites of spinal neurons (gray matter) lie inside the cord while the nerve fibers (axons) that interconnect them (white matter) run along the outside. As these axons ascend and descend along the body, the white matter occupies more space as the cord approaches the head. All movements of the body below the head are controlled by the spinal cord and injuries to it produce devastating losses of function. The spinal cord has been the object of systematic study for over two centuries. Accordingly, this brief introduction covers only a few topics from a vast literature.
The spinal cord begins at the brain stem near its exit from the skull (at the foramen magnum) and runs down the body within the bony spinal column (Fig. 1; see Brodal, 1969; Burke, 2003). The cord is divided into segments along its length, each with a separate pair of dorsal and ventral nerve roots, numbered according to the vertebral bodies between which they exit. The dorsal roots contain the incoming (afferent) sensory nerve fibers that carry information from the body below the head into the CNS. The ventral roots carry the outgoing (efferent) nerve fibers that control the muscles that produce movement, as well as “autonomic” functions such as the control of blood pressure, sweating, and micturition and defecation.
The white matter contains nerve fibers (axons) that are either myelinated (coated by the insulating material myelin) or without such coating (unmyelinated). In the white matter there exist three kinds of axons: 1) descending ones that carry signals from neurons located in supraspinal CNS structures within the skull: 2) ascending ones that relay sensory information from afferents, or from circuits within the spinal cord, to supraspinal regions; and 3) so-called “propriospinal” axons that originate from interneurons located within the spinal cord itself and project to other spinal neurons, either locally ("short") or to more distant spinal segments ("long"), to coordinate their activity. Axons with the same or related functional roles usually travel together in “tracts” that are located in particular regions of the white matter (Fig. 2).
The left half depicts the location of sensory tracts that project upward toward the brain. Some subserve conscious sensation, including pain and other sensory modalities (the dorsal columns and the spinothalamic tract (STT). Other ascending tracts are concerned more specifically with control of movement, including the dorsal columns and the dorsal (DSCT) and ventral (VSCT) spinocerebellar tracts. The right half shows the positions of descending tracts that are involved in the control of movement, including the lateral (LCST) and medial corticospinal (MCST), rubrospinal (RST), vestibulospinal (VST), and reticulospinal (RetST) tracts. The blue stippled regions next to the gray matter are occupied by the propriospinal axons, linking neurons along its length. The double arrows above and below the central canal denote commissural axons that interconnect the two sides of the cord. The sizes and exact locations of these tracts are approximations. They differ between animal species and with segmental distance along the cord.
The inner part of the cord, or gray matter, contains the cell bodies and dendrites of the spinal neurons. There are three basic kinds of spinal neurons: 1.) those with axons that leave the cord via the ventral roots (motoneurons and autonomic preganglionic neurons); 2.) tract cells that project mainly to supraspinal regions such as the cerebellum and thalamus, although some of these also have intraspinal corrections via axon collaterals; and 3.) spinal interneurons with axons that project entirely within the cord (Burke and Rudomin, 1977). Classically, the gray matter is divided into two major parts, called the dorsal (DH) and ventral horns (VH). The dorsal horn contains most of the tract cells that process incoming sensory information and project upward via the corresponding white matter tracts. The ventral horn contains the motoneurons, grouped together in the motor nuclei, and the autonomic preganglionic neurons that control functions such as control of blood pressure and gastrointestinal activity. Motoneurons have axons that leave the cord via ventral roots to innervate the muscles. The axons of preganglionic neurons also leave via the ventral roots to innervate secondary neurons in the autonomic ganglia along the spinal column. The locations of some identified types of tract cells are indicated on the left half of Fig. 3. The right half shows the approximate locations of two groups of well-identified interneurons (Group Ia inhibitory cells and Renshaw interneurons). A wide variety of other interneuron groups are scattered throughout the gray matter, especially in the large intermediate region, that are being studied intensively (e.g., Kiehn, 2006; Jankowska et al., 2007). As with the white matter tracts discussed above, the sizes and locations of these groupings with species and segmental position.
Some interneurons in the dorsal horn (DH) receive direct synaptic input from a variety of sensory afferent axons that enter through the dorsal roots (first-order interneurons). The most superficial DH layers receive information from unmyelinated and fine myelinated afferents that are activated by noxious (painful) stimuli. Deeper layers receive input from larger diameter afferents that are activated by non-noxious stimuli like light touch. Some first-order interneurons have axons that project into ascending tracts to higher (i.e., supraspinal) centers in the brainstem and in the brain itself. However, most sensory interneurons also project to other interneurons circuits within the spinal cord, where their activity is modified before relay into the ascending tracts described above. The anatomy and physiology of these information-processing circuits have been studied extensively (Bloedel and Courville, 1981; Brown, 1981; Willis and Westlund, 1997; Willis and Coggeshall, 1991) and will not be reviewed here.
Spinal reflexes are more-or-less stereotyped responses of a muscle or group of muscles that follow particular kinds of sensory input (Sherrington, 1906). Such responses are produced by neuronal circuits entirely within the spinal cord. There are two basic types of reflexes: 1) Simple reflexes such as muscle contraction after sudden stretch or withdrawal of an entire limb after a painful stimulus, which are produced by neuronal circuits located within the cord and can occur when the cord is isolated from the brain; and 2) Complex, coordinated action of many muscles in the limbs and trunk, such as those that produce postural adjustments, and rhythmic movements of the limbs, such as the scratching response, that are linked to postural actions. The following discussion simplifies a complex story of reflexes and the control of movement (see Windhorst, 2007).
A simple spinal reflex arc
Sudden muscle elongation (stretch) by an external force causes the motoneurons that innervate that muscle and allied (synergistic) muscles to fire more or less synchronously, resulting in sudden muscle contraction (the familiar knee jerk reflex). Sustained stretch of an extensor muscle, as for example by the action of gravity on the skeleton, can also cause sustained activation of this muscle, the “tonic stretch reflex”, which is an important factor in the control of posture. Both responses are mainly due to activation of sensory fibers coming from the muscle spindle stretch receptors. The sensitivity of these receptors is under CNS control through a set of so-called “gamma” motoneurons that innervate specialized muscle fibers within the spindle (Matthews, 1981).
Activation of the largest and fastest-conducting spindle afferents, called Group Ia, make direct, or monosynaptic, contacts on the alpha motoneurons that innervate the main muscle fibers in the host muscle and its synergists (Eccles, 1964). These synapses generate large depolarizing (excitatory) synaptic potentials (EPSPs; see below) in the motoneurons. This is the simplest spinal reflex circuit (left side of Fig. 4).
However, there is an interesting complication to this simple picture, as depicted on the right side of Fig. 4. It is now known that Group I afferents also project to the same motoneurons via a set of interposed interneurons, which also excite them. This is true for both extensor and flexor motoneuron groups (Angel et al., 1996; Degtyarenko et al., 1998; Quevedo et al., 2000). In this circuit there are two synapses between the afferents and the motoneurons, so that it is called a “disynaptic” reflex arc.
Modulation of reflex arcs
Why should there be a disynaptic arc, such as in Fig. 4, when its end product - excitation of the motoneurons - is similar to that produced by the monosynaptic arc? The most likely explanation is that the disynaptic arc can act to amplify the depolarization produced by the monosynaptic circuit, at least when the set of interposed excitatory interneurons are caused to fire outgoing action potentials by the incoming volley of action potentials in Group I afferents. Obviously, if they do not fire, transmission through the disynaptic link is interrupted and there is no amplification. By regulating the number of firing interneurons, as denoted by the arrow labeled “Control systems”, the CNS can modulate the amplification from zero to some maximum. Reflex arcs that include one or more interposed interneurons (disynaptic or polysynaptic, respectively) thus provide the CNS with the ability to change the strength of reflex arcs. This type of reflex modulation depends on particular arrangements of spinal interneuron circuits and therefore might be called "circuit-based" reflex control.
A second form of reflex modulation is referred to as “presynaptic inhibition” (Rudomin and Schmidt, 1999). It involves synapses that end directly on the afferent synapses themselves. Activation of such “axo-axonic synapses” reduces the amount of synaptic transmitter released by the recipient Ia synapses. This mechanism, which also depends on specific spinal circuits, can be activated by sensory inputs as well as supraspinal control, also operates on other types of primary afferent systems.
Both of the above mechanisms depend on "ionotropic" synaptic contacts in which transmitters open postsynaptic ionic channels to cause membrane potential changes that develop and decay relatively rapidly. A quite different type of spinal reflex modulation involves synapses that activate "metabotropic" receptors, which do not themselves produce postsynaptic potential changes but rather alter the responses of the postsynaptic neurons to other types of inputs (e.g., Heckman et al., 2005). In contrast to rapidly-decaying ionotropic synaptic actions, metabotropic or G protein-coupled receptors can evoke slowly-developing and long-lasting effects that involve intracellular second-messenger systems (Hille, 2001). The major sources of such transmitters that activate metabotropic receptors are nuclear groups in the brain stem that give rise to descending spinobulbar pathways that liberate serotonin (5-hydroxytryptamine, or 5-HT) or noradrenaline (NE), as well as other substances, that project widely to neurons in all parts of the spinal cord (Hökfelt et al., 2000). Spinal motoneurons are richly innervated by 5-HT synapses (Alvarez et al., 1998), which when activated greatly increase their excitability to ionotropic depolarization produced by other inputs. The same appears true of other spinal interneuronal circuits. These diffuse descending systems are likely to be critical in regulating the level of excitability in the entire spinal machinery and they are particularly relevant to the operation of segmental pattern generators to be discussed below.
The Group Ia stretch reflex discussed above also provides an example of how reflex arcs are linked together to support a specific function. At the end of the 19th Century, Sir Charles Sherrington demonstrated that certain types of stimulation can produce simultaneous excitation of one group of muscle (the "agonists") and inhibition of muscles that oppose their action (the "antagonists"; Sherrington, 1906). Later work by many others, using modern methods, showed that the excitation produced by Group Ia afferents in one set of motoneurons (the agonists) is changed to inhibition of their antagonists by inserting a set of spinal interneurons that hyperpolarize the latter, thus inhibiting them (Fig. 5; Baldissera et al., 1981; Burke and Rudomin, 1977). This reciprocal inhibition linkage is found in both extensor and flexor motoneuron groups. There are many other examples of linkages between reflex arcs, virtually all of which are subject to CNS modulation as described above (e.g., Balidessera et al., 1981; Jankowska, 1992).
The obvious function of Group Ia reciprocal inhibition is to reduce the probability that stretch-evoked action in one muscle group (the agonists that shorten) is disrupted by the resulting elongation of their antagonists (see Windhorst, 2007). However, some movements or postures may require co-activation of both agonist and antagonist muscles. This interruption of reciprocal inhibition if possible because transmission through both sets of inhibitory interneurons can be modulated by the CNS. There are other more complex linked reflexes that involve polysynaptic chains of spinal interneurons that also receive convergent control systems.
Centrally patterned movements
The spinal cord also contains neuronal circuits, sometimes referred to as Central Pattern Generators (CPGs), that under certain laboratory conditions can generate coordinated rhythmic flexion and extension of the limbs, as well as associated postural adjustments, that closely resemble those seen in intact animals. The scratching response that is triggered by light touch to the ear or neck in cats and dogs involves such a CPG (Shik and Orlovsky, 1976). The isolated spinal cord of vertebrates from fish to mammals also has a CPG that can generate coordinated action of the trunk and limbs that result in walking and running movements. Activation of this “locomotor” CPG usually requires sustained presence of pharmacological agents or stimulation of specific areas in the CNS and can occur in decerebrate or spinal animals (Edgerton et al., 2004), or even in spinal cord segments isolated ‘’in vitro’’ (Kiehn, 2006). The scratching and locomotor CPGs probably share common elements but there is some evidence that they are not identical (Degtyarenko et al., 1998; Deliagina et al., 1981). In mammals, it is clear that functionally complete walking and running movements require participation of supraspinal centers to control balance and direction, although these centers appear to act through CPG circuits in the spinal cord.
Extensive research in primitive fish has disclosed the details of neuronal organization of the spinal circuits that generate and control swimming movements (Grillner, 2003; see also Kiehn, 2006). Over the past several decades there has been intensive study of the locomotor CPG in animals from fish to higher mammals (Grillner, 1981; Hultborn et al., 1998; Jordan, 1991; Kiehn, 2006; Rossignol, 1996; Sillar, 1991; Whelan, 1996). Despite considerable progress many details remain to be uncovered (Kiehn, 2006). There is in fact still no agreement about the basic structure of spinal CPGs in adult mammals (Burke et al., 2001; Kiehn, 2006; Lafreniere-Roula and McCrea, 2005). However, comparison between the results in different species makes it clear that nervous systems in various animals have found different organizations to produce functionally similar results (Getting, 1989).
Control of reflex arcs by CPGs
The diagram in Fig. 6 uses the reciprocal Group Ia reflex system to illustrate how the locomotor CPG not only drives the motoneurons but also modulates the transmission of information through reflex interneurons in functionally meaningful ways. During the extension phase of locomotion, the extension half of the CPG excites extensor motoneurons as well as the excitatory and inhibitory interneurons in the disynaptic Group Ia arcs (Angel et al., 1996; Pratt and Jordan, 1987; Degtyarenko et al., 1998). A similar and complementary organization exists to control flexor motoneurons and their Group Ia reflex arcs during the flexion phase of locomotion by the flexor half of the CPG. Other types of reflex arcs, including those of cutaneous reflexes, also show such modulation during different phases of locomotion (see Burke, 1999; Burke et al., 2001; Degtyarenko et al., 1998).
The kind of experimental evidence from which we can deduce this types of circuit diagram is illustrated in Fig. 7. The records show computer-averaged excitatory postsynaptic potentials (EPSPs) recorded intracellularly from a cat hindlimb extensor motoneuron produced by stimulating extensor Group I afferents during “fictive locomotion” (Angel et al., 1996; Degtyarenko et al., 1998). The brief central latency (about 0.6 ms; solid arrow) between the entry of the Group I volley and the onset of the large EPSP shows that this potential is monosynaptic. During the flexion phases of locomotion, when the extensor motoneurons were silent, this monosynaptic potential decayed with a simple exponential shape. However, during the extension phases, a second EPSP with longer latency (about 1.4 ms) appeared, superimposed on the falling phase of the first. A corresponding enhancement of inhibitory postsynaptic potentials has been found in flexor motoneurons during the extension phase (Degtyarenko et al., 1998; Quevedo et al., 2000).
With appropriate controls, this kind of data is best explained by postulating that the sets of excitatory and inhibitory interneurons as in the preceding diagrams receive converging excitatory synaptic drive not only from Group I afferents but also from that part of the locomotor CPG that drive extensor motoneurons into action. The disynaptic excitatory interneurons evidently were completely silent during the flexion phase even though they must have received monosynaptic excitation from the Group I afferents. Adding convergent excitation from the CPG was enough to push at least some of the interneurons to fire action potentials, thus generating the disynaptic EPSP. This highly non-linear amplification is an example of what is called “spatial facilitation”. The use of the spatial facilitation approach has been instrumental in elucidating a variety of spinal cord circuits, including reflex pathways from other muscle and cutaneous afferent pathways (see Baldissera et al., 1981; Burke, 1999; Lundberg, 1969, 1979).
Convergent control of voluntary movements
The examples discussed above represent only a small fraction of the spinal reflex pathways that are composed of spinal interneurons that receive convergent control from local interneurons (including spinal CPGs), from axons originating in distant spinal segments and the supraspinal brain, or from both sources (Baldissera et al., 1981; Lundberg, 1979). Spinal motoneurons in carnivores receive relatively little direct connections from motor center in the brainstem and none at all from the cerebral cortex (Brodal, 1969; Burke and Rudomin, 1977). It is only in higher primates, including man, that the motor cortex makes direct, monosynaptic connections with some motoneurons, especially those that control muscles in the arm and hand (Porter and Lemon, 1993). The picture that has emerged from much recent research on the spinal cord suggests that most of what we term “voluntary” movements are actually mediated by spinal interneurons, many of which are parts of reflex pathways, that receive descending command signals from the brain, as well as spinal interneuron circuits such as those discussed above (Alstermark and Lundberg, 1992; Baldissera et al., 1981; Lundberg, 1975).
One likely interpretation of this organization is that motor commands from the brain must take account of the immediate “state-of-affairs” in the motor machinery. For example, in order to move an arm from one position to another, as in grasping an object or throwing a ball, the CNS needs information not only about the current position of the arm in relation to the rest of the body but also about the current patterns of activity in all of the relevant muscles, including those that maintain posture. The afferent systems from muscle, deep tissue, and cutaneous afferents supply this information. However, it is also critical to know the internal state of the spinal pathways that are interconnected and continuously modulated by afferent information as well by descending command systems. There are ascending pathways, such as the ventral spinocerebellar tract (VSCT), which are organized to deliver this internal state information to the cerebellar cortex (Lundberg, 1971) so as to allow computation of descending commands to take it into account. However, it is clear that the spinal machinery has immediate access to information about the initial conditions before a specific motor act as well as its ongoing progress . For reasons of timing and simplicity, it seems sensible to postulate that the spinal circuitry itself might “filter” descending motor commands so as to produce an appropriate final result .
The spinal cord is a highly evolved and complex part of the CNS that has considerable computational ability. A major reason why the spinal cord has been extensively studied is because the functional roles of the sensory systems that project to it, and of the motoneurons that leave it to control the musculature, are clearly identified. Thus the functions of interneuronal systems that mediate between specific inputs and outputs can, in principle, also be defined. These systems operate in elaborate feedback and feed-forward loops with the supraspinal CNS to produce the finely-tuned and sophisticated movements that we take for granted until they are disrupted by degenerative diseases like amyotrophic lateral sclerosis or mechanical injury to the cord. Even with such devastating disorders, there is evidence that the cord has some degree of “plasticity” that can compensate, at least in part, for interruption of its normal function (Edgerton et al., 2004; Wolpow and Tennissen, 2001).
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Motoneurons, Interneurons, Reflexes, Central pattern generators, Brainstem, Models of the Spinal Cord