Long descending motor tract axons and their control of neck and axial muscles

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Abstract

It has been tacitly assumed that a long descending motor tract axon consists of a private line connecting the cell of origin to a single muscle, as a motoneuron innervates a single muscle. However, this notion of a long descending motor tract referred to as a private line is no longer tenable, since recent studies have showed that axons of all major long descending motor tracts send their axon collaterals to multiple spinal segments, suggesting that they may exert simultaneous influences on different groups of spinal interneurons and motoneurons of multiple muscles. The long descending motor systems are divided into two groups, the medial and the lateral systems including interneurons and motoneurons. In this chapter, we focus mainly on the medial system (vestibulospinal, reticulospinal and tectospinal systems) in relation to movement control of the neck, describe the intraspinal morphologies of single long descending motor tract axons that are stained with intracellular injection of horseradish peroxidase, and provide evidence that single long motor-tract neurons are implicated in the neural implementation of functional synergies for head movements.

Introduction

The motor cortex is considered to be a higher center for voluntary movements. Corticofugal neurons from the motor cortex to the spinal cord pass through the medullary pyramid, so that this pathway is called the pyramidal tract. It was generally believed that the output from the motor cortex was conveyed only through the pyramidal tract to the spinal cord. Therefore, this system has been called the pyramidal tract system, and this pathway was considered to be the only pathway that mediates control signals for voluntary movements, since lesions of the pyramidal system produced impairment of voluntary movements such as paralysis of limb muscles, decreased or increased stretch reflex, and appearance of abnormal reflex (Babinski sign). On the other hand, the other long descending motor tract systems other than the pyramidal tract including the cerebellum and the basal ganglia were called the extrapyramidal system, and this system was considered to be mainly involved in control of posture rather than limb movements. This dichotomy between the pyramidal tract system and the extrapyramidal system has not been tenable any more, since movements of limbs are still possible after the sectioning of the bilateral pyramids (Lawrence & Kuypers (1968a), Lawrence & Kuypers (1968b)). Figure 1A summarizes the present view of the long descending motor tract systems. After the sectioning of the pyramidal tract, long descending tracts that receive inputs from the cerebral cortex still exist in the brainstem and they convey signals for voluntary movements of limbs to the spinal cord. Among them, there are two pathways; one that receives input via collaterals of pyramidal tract neurons and the other that receives input from corticofugal neurons of the cerebral cortex other than pyramidal tract neurons. The former is called the parapyramidal tract system, which includes the cortico-rubrospinal and cortico-reticulospinal connections, and the latter is called cortically originating extrapyramidal system. Except these long descending motor tract systems that are related to the cerebral cortex, the long descending motor tract system that does not receive cerebral input exists and is called the extrapyramidal system in a narrow sense. Readers interested in the changing views of the motor cortex and the pyramidal tract should consult excellent monographs by Phillips and Porter (1977) and Porter and Lemon (1995).

The final targets of these long descending motor tracts, either directly or indirectly, are motoneurons of muscles in different parts of the body. Somatic motoneurons which extend their axons through the ventral root to a given axial or limb muscle are arranged in a longitudinal, column-like fashion in the ventral horn (Romanes, 1951; Sprague, 1951; Burke et al., 1977). The longitudinal columns innervating individual muscles are grouped into the medial and lateral longitudinal aggregates. The medial aggregate is made up of motoneuronal columns of vertebral muscles innervated by the dorsal and the ventral rami of the ventral root and exists throughout the spinal cord, whereas the lateral aggregate of motoneuronal columns for other appendicular (limb) muscles innervated by the ventral rami exists only in the cervical and the lumbar enlargements due to the additional longitudinal columns for the muscles intrinsic to the extremities, and fuses to the medial aggregate in the upper cervical and the upper thoracic cord, and the lower thoracic cord.

Figure 1B (left) summarizes the general arrangement of the motor nuclei in the spinal ventral horn (lamina IX of Rexed) for muscles in different parts of the body. In general, the motor nuclei for distal muscles are located more laterally and those for proximal muscles are located more medially in the ventral horn. More specifically, the motor nuclei for axial muscles are located most medially, those for limb muscles (appendicular muscles) are most laterally, and those for girdle muscles are located between the above two. Among the limb muscles, extensors are located more medially than flexors, so that limb flexors, especially intrinsic muscles, are located in the most lateral part of the ventral horn where corticospinal axons most extensively terminate directly on motoneurons in both monkeys and humans (Lawrence and Kuypers, 1968a).

As motoneurons innervating axial and limb muscles are located in different areas of the ventral horn (musculotopic organization), interneurons terminating upon motoneurons of these two groups of muscles are also arranged in different portions of the spinal intermediate zone (laminae V–VIII) (Rexed, 1954; Kuypers, 1981). The spinal gray matter is divided into subdivisions dorsoventrally from lamina I to lamina X, based on the cytoarchitecture (Fig. 1B, left) (Rexed, 1954). Laminae I–IV belong to the dorsal horn, which is mainly related to sensory relays. The most ventral part, lamina IX, belongs to the ventral horn, which only includes motoneurons. Laminae V–VIII, which are located between the dorsal and ventral horns, are called the intermediate zone. This intermediate zone is responsible for motor integration, since it receives inputs from the spinal afferents such as Groups Ia and Ib and also inputs from the long descending motor tract systems, and send its outputs to motoneurons.

Spinal interneurons have been classified into segmental and propriospinal interneurons. Interneurons that project only to the same segment are called segmental interneurons, whereas interneurons that project to the other segments are called propriospinal interneurons. However, recent intracellular staining revealed that most “segmental” interneurons extend their axons once outside the gray matter into the white matter, and again enter the gray matter at different segments. Therefore, this dichotomous division of the spinal interneurons is no longer clear.

Interneurons in the intermediate zone may be divided into two groups; interneurons located in the medioventral part of the intermediate zone (lamina VIII and its adjacent lamina VII) and interneurons in the dorsal and lateral parts of the intermediate zone (laminae V–VII). These interneurons in different parts of the intermediate zone (different interneuron groups a–d in Fig. 1B, right) distribute their fibers to specific parts of the lateral and ventral funiculi in the white matter and terminate on specific motoneuronal groups in the ventral horn (see the details in the legend of Fig. 1B).

When considering the functions of the long descending motor tract pathways, it should be realized that their functions are not only determined by (1) inputs to cells of their origin, but also by (2) their terminations on target cells in the spinal cord. Various long descending motor tracts of supraspinal origin are known to terminate in different areas of the spinal gray matter (Brodal, 1981; Holstege, 1988), so that they influence differentially motoneurons of different groups of muscles and interneurons innervating them. The brainstem pathways terminating in the spinal intermediate zone as well as the motoneuronal cell groups probably subserve mainly motor functions. The subcorticospinal pathways, i.e., pathways from the subcortical structures to the spinal cord (Fig. 1A), have been grouped into the medial and lateral systems based upon the location of such pathways in the spinal white matter and their terminal distribution in the spinal cord (Kuypers et al., 1962). The medial system terminates in the ventromedial part of the intermediate zone, whereas the lateral system terminates in the dorsal and lateral parts of the intermediate zone of the spinal gray matter. Extending this classification to the entire long descending motor tract systems including both the corticospinal and subcorticospinal system, the long descending motor tract system is subdivided into two major systems (see Fig. 5A), although the terminal distribution of corticospinal tract (CST) fibers overlaps that of either of the two subcorticospinal systems: (1) the medial system originates in the brainstem (the medial subcorticospinal system), runs in the ventral funiculus, and terminates in the mediodorsal part of the ventral horn and its adjacent part of the intermediate zone; and (2) the lateral system consists of the corticospinal system and the lateral subcorticospinal system, runs in the dorsal lateral funiculus, and terminates in the lateral and dorsal parts of the intermediate zone (Kuypers, 1964). The lateral system consists of the CST and the rubrospinal tract (RBST), whereas the medial system consists of the reticulospinal tract (RST), the vestibulospinal tract (VST), the tectospinal tract (TST), and the interstitiospinal tract (IST). For spinal termination fields of different long descending motor tracts, see Holstege (1988).

It has been tacitly assumed that the pyramidal tract, which is the main output pathway from the motor cortex to the spinal cord for conveying control signals of voluntary movement, consists of private lines connecting a point in the motor cortex to a single muscle, as a motoneuron innervates a single muscle. Accordingly, CST neurons, often called as pyramidal tract neurons, have been referred to as upper motoneurons, and spinal and brainstem motoneurons as lower motoneurons. Other long descending motor tracts also have been considered to be similar to the pyramidal tract in this aspect. However, the above notion of a long descending motor tract referred to as a private line is no longer tenable, since recent studies showed that axons of all major long descending motor tracts send axon collaterals to multiple spinal segments. This situation was first described by Abzug et al. (1974), who found that 50% of lateral vestibulospinal tract (LVST) neurons, which sent axon branches to C6-Tl segments, were also antidromically driven by stimulation of the lumbar spinal cord. A similar percentage of RST neurons sent branches to the cervical gray matter as well as to the first lumbar segment (Peterson et al., 1975). More surprisingly, 6% of CST neurons activated from the cervical gray matter (C4–C8) projected to the first lumbar segment and 24% of CST neurons activated from the cervical gray matter projected to the thoracic cord (Shinoda et al., 1976). Similarly, 45% and 5% of RBST neurons projecting to the cervical gray matter sent axon branches to the thoracic cord and below, and to the first lumbar level, respectively (Shinoda et al., 1977). Furthermore, it turned out that virtually all CST neurons examined in the forelimb area of the motor cortex had three to seven axon collaterals at widely separated segments of the cervical and the higher thoracic cord (Shinoda, Arnold, & Asanuma (1976), Shinoda, Yamaguchi, & Futami (1986b)). In addition, multiple axon collaterals of RBST neurons were also demonstrated at different spinal segments (Shinoda et al., 1977). These results have indicated that single motor tract axons are not a simple private line connecting the cells of origin and motoneurons for a single muscle, but instead they may exert simultaneous influences on different groups of spinal interneurons and motoneurons of multiple muscles at widely separated spinal segments. In fact, single corticospinal axons terminated on motoneurons of multiple muscles in the monkey (Shinoda et al., 1981).

The purpose of this chapter is to briefly review the basic organizations of axial and neck muscles and their motor nuclei, and the general characteristics of the lateral and medial long descending motor tract systems, and to finally describe the intraspinal trajectories of single long descending motor tract axons in the medial descending motor tract system controlling head movements. Readers interested in the classical anatomy of descending motor pathways should consult excellent reviews by Kuypers (1981) and Holstege (1988).

Section snippets

General arrangements of the epaxial musculature

In comparative anatomy of the somatic musculature system, axial muscles are divided by the horizontal (longitudinal) myoseptum into dorsal and ventral muscle groups. Muscles dorsal to the horizontal septum and innervated by the dorsal rami of the ventral root are called epaxial muscles (Mm. dorsi proprii, Mm. tranci dorsales), whereas those ventral to it and innervated by the ventral rami of the ventral root are called hypaxial muscles (Mm. tranci ventrales) (Fig. 2). Based on the investigation

Lateral vs. medial long descending motor tract systems

As mentioned in the “Introduction,” long descending motor tracts of supraspinal origin are classified into the lateral and medial descending groups based on anatomical and behavioral observations after lesions of these two long descending motor tract groups (Lawrence & Kuypers (1968a), Lawrence & Kuypers (1968b)), although they are not completely separated. The general characteristics of these two descending systems are briefly summarized below (see a diagram in Fig. 5 for the summary of this

Morphologies of single neurons in the medial long descending motor tract system

As summarized above in a generalized form, long descending motor tracts, their target motor nuclei and interneurons may be principally segregated into the medial and lateral motor systems. Degeneration staining methods such as the Nauta method combined with lesion experiments were used for identifying the location of descending tracts in the brainstem and spinal cord and their terminal distribution in the spinal cord (Brodal et al., 1962; Verhaart, 1964). More recently, the autoradiographic

Functional connections of medial long descending motor tracts with neck motoneurons

Figure 19 summarizes electrophysiological properties of medial long descending motor tract neurons on neck motoneurons. VST influences on neck motoneurons are excluded from this diagram, since they were described in the previous section. When an interesting object appears in the visual field, animals quickly move both eyes and a head to that interesting object. This behavior is called an orienting response, and the SC is a primary center for orienting (Hess, 1956; Sprague and Meikel, 1965). The

Functional roles of multiple axon collaterals of single long descending motor tract axons

Head position control is an ideal paradigm for studying how the CNS controls a multidimensional motor system (Richmond and Vidal, 1988; Graf et al., 1997). Head-movement signals detected by the semicircular canals are mediated through vestibulocollic pathways that link each of the three semicircular canals to a set of neck muscles. For tasks necessitating compensatory head movements, the CNS programs muscle-activation patterns in a synergy, i.e., in a specific spatial and temporal combination

Acknowledgments

This study was supported by the 21st century COE Program from the Ministry of Education, Science and Culture of Japan to Y.S., Y.S., and Y.I.

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