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Functional synergies among neck muscles revealed by branching patterns of single long descending motor-tract axons
Progress in Brain Research, Vol. 143 ISSN 0079-6123 Copyright ß 2004 Elsevier BV. All rights reserved
CHAPTER 39
Functional synergies among neck muscles revealed by branching patterns of single long descending motor-tract axons Yuriko Sugiuchi, Shinji Kakei, Yoshiko Izawa and Yoshikazu Shinoda* Department of Systems Neurophysiology, Graduate School of Medicine, Tokyo Medical and Dental University, Tokyo 113-8519, Japan
Abstract: In this chapter, we describe our recent work on the divergent properties of single, long descending motor-tract neurons in the spinal cord, using the method of intra-axonal staining with horseradish peroxidase, and serial-section, three-dimensional reconstruction of their axonal trajectories. This work provides evidence that single motor-tract neurons are implicated in the neural implementation of functional synergies for head movements. Our results further show that single medial vestibulospinal tract (MVST) neurons innervate a functional set of multiple neck muscles, and thereby implement a canal-dependent, head-movement synergy. Additionally, both single MVST and reticulospinal axons may have similar innervation patterns for neck muscles, and thereby control the same functional sets of neck muscles. In order to stabilize redundant control systems in which many muscles generate force across several joints, the CNS routinely uses a combination of a control hierarchy and sensory feedback. In addition, in the head-movement system, the elaboration of functional synergies among neck muscles is another strategy, because it helps to decrease the degrees of freedom in this particularly complicated control system.
Introduction
Abzug et al. (1974), who used electrophysiological techniques to show that 50% of the lateral vestibulospinal tract (LVST) neurons which supply axon branches to C6-Th1 segments, are also antidromically driven by stimulation of the lumbar spinal cord. A similar percentage of reticulospinal tract (RTST) neurons were then shown to send branches to the cervical gray matter, as well as to the first lumbar segment (Peterson et al., 1975). Even more unexpectedly, similar electrophysiological experiments have shown that both CST (Shinoda et al., 1986b) and rubrospinal tract (RBST; Shinoda et al., 1977) neurons project to both the cervical gray matter (C4–8) and the thoracic or lumbar spinal cord. Furthermore, virtually all CST neurons examined in the forelimb area of the motor cortex have 3–7 axon collaterals at widely separated segments of the cervical and upper thoracic cord (Shinoda et al., 1976). In addition, multiple axon collaterals of single
It had been tacitly assumed, and emphasized in most textbooks, that the pyramidal tract consists of ‘private lines’, which connect a discrete site in the motor cortex to a single muscle, just as a spinal motor nucleus usually innervates a single muscle. Similarly, corticospinal tract (CST) neurons have long been referred to as ‘upper motoneurons’ and motoneurons as ‘lower motoneurons’. Other long descending motor tracts have generally been considered to be similarly arranged. These assumptions are no longer tenable, however, because recent studies have shown that axons of all the major long descending motor tracts send axon collaterals to multiple spinal segments. This organization was first described by *Corresponding author: Tel.: þ 81-3-5803-5152; Fax: þ 81-3-5803-5155; E-mail: [email protected]
411 DOI: 10.1016/S0079-6123(03)43039-2
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RBST neurons have been found at different spinal segments (Shinoda et al., 1977). These electrophysiological findings all emphasize that single, motor-tract axons are not simple private lines for connecting the cells of cortical origin to the motoneurons of a single muscle, but, rather, such descending axons concurrently exert multiple influences on different groups of spinal interneurons and motoneurons at widely separated spinal segments. The above findings clearly have important implications for the descending control of posture and movement. It was not possible until recently, however, to reinforce these electrophysiological findings with relevant morphology, due to the inability to trace long axons from their cell bodies when using classical anatomical techniques. For visualization of the entire axonal morphology of a single neuron, especially one with a relatively long axon, new methods had to be developed, particularly ones which would bring into view the entire morphology of single, functionally identified neurons in the central nervous system (CNS). The enzyme, horseradish peroxidase (HRP), was shown to be particularly valuable for this purpose (Jankowska et al., 1976; Kitai et al., 1976; Snow et al., 1976). Admittedly, all of the processes of a single neuron labeled with HRP may not be visualized in a single section. Reconstruction of the axonal trajectory using serial sections, however, reveals the entire axonal trajectory of a single-labeled neuron for a distance of 10–30 mm in the mammalian CNS (for review, see Shinoda, 1999). In this chapter, we summarize our HRP-reconstruction studies on the intraspinal morphology of single axons of various long descending motor tracts in the cat and monkey. We show that the branching patterns of single vestibulocollic and tecto-reticulospinal axons may reveal the functional synergies among neck muscles that the CNS uses for the control of head movements.
Morphology of single CST and other long descending motor-tract axons Our initial study in this area was undertaken on the cat (Futami et al., 1979). First, we identified CST axons in the lateral funiculus of the cervical spinal
cord, by their direct responses to electrical stimulation of the contralateral motor cortex. Next, such an axon was injected iontophoretically with HRP. The trajectory of each single, stained axon was then reconstructed in serial sections of the spinal cord. The stem axon in the lateral funiculus gave rise to multiple axon collaterals at different spinal segments. Primary collaterals ran ventromedially and entered the gray matter. There, they ramified successively to form a delta-like branching pattern in the transverse plane, with terminations in Rexed’s laminae V–VII. In the horizontal plane, the axons bifurcated successively, gradually turning their orientation in parallel to the long axis of the spinal cord. Finally, they spread in both ascending and descending directions over a distance of l.3–3.0 mm. Similar branching patterns were subsequently found for the RBST axons of the cat (Shinoda et al., 1982). It was long known that in the cat spinal cord, both CST and RBST tracts terminate on interneurons, but not motoneurons (Lloyd, 1941). Therefore, in spite of our above-described demonstration of the existence of multiple axon collaterals at different spinal segments, it did not necessarily indicate that single axons in these tracts participate in the concurrent control of multiple muscles. On the other hand, Preston and Whitlock (1961) had shown that the CST of the monkey does indeed have direct projections onto spinal motoneurons. We took advantage of this morphological connection in an electrophysiological study, which showed that single monkey CST neurons were activated antidromically by stimulation of different motor nuclei in the cervical cord (Shinoda et al., 1979). In a subsequent study (Shinoda et al., 1981), we injected HRP into single CST axons in the lateral funiculus at the level of the cervical cord. These axons originated in the forelimb area of the monkey motor cortex. The stained CST axons had multiple axon collaterals in the cervical cord, and, importantly, such single axons projected to several motor nuclei supplying different forelimb muscles. Terminal boutons of these axons had close (presumed) contacts with dendrites of some of the motoneurons, which we also labeled with HRP, in multiple motor nuclei supplying the forelimb. This latter finding therefore showed that at least some CST neurons of the forelimb area of the motor cortex participate in the simultaneous control of multiple
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muscles of the forelimb. The question then arose as to which group of muscles is innervated by single, long descending motor-tract axons, i.e., what functional synergies among neck muscles are thereby implemented? The CST system in the monkey is not suitable to address this issue, because the abovementioned experiment is so technically difficult that its experimental yield is too low. Fortunately, it was known (Wilson and Melvill Jones, 1979) that vestibulospinal (VS) neurons have strong monosynaptic connections with neck motoneurons in the cat. Using this vestibulocollic system, we were indeed able to test for the implementation of a functional synergy by even a single, long descending motor-tract neuron.
The axonal trajectories of single vestibulospinal axons Head position control is an ideal paradigm for studying how the CNS controls a multidimensional motor system (Richmond and Vidal, 1988). Headmovement 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., a specific spatial and temporal combination rather than in an infinite variety of patterns. Stimulation of individual semicircular canals produces canal-specific head movements (Suzuki and Cohen, 1964). The plane of the head movement produced by canal stimulation parallels that of the stimulated canal, i.e., they are almost coplanar. Therefore, a signal from each semicircular canal must be distributed to an appropriate set of neck muscles in order to induce compensatory head movement in the same plane as the plane of the stimulated canal. Obviously, this process is more economical when a given descending motor command signal is distributed by a single neuron with divergent branches to multiple target motoneurons that participate in cocontraction of muscles to produce the required movement. The convergence of different canal nerve inputs onto single motoneurons has been extensively analyzed in the vestibulocollic system (Wilson and Melvill Jones,
1979), but its converse, divergent properties of VS axons, have not attracted attention until recently. To address the latter issue, we first analyzed the morphology of single physiologically identified lateral and medial VS tract (LVST and MVST) axons in the cat, by resort to intracellular HRP staining and subsequent three-dimensional reconstruction of axonal trajectories (Shinoda et al., 1986a, 1992a). An example of our approach is shown in Fig. 1. Axons were penetrated in the cervical cord at C1–8 with an HRP-filled microelectrode. These axons were identified as VS axons by their monosynaptic responses to stimulation of the vestibular nerve, and further classified as either LVST or MVST axons by their responses to stimulation of the LVST and MVST. Figure 1 shows that when stained, these axons could be traced for a rostrocaudal distance of 3–16 mm. Within this length, both LVST and MVST axons were found to have multiple axon collaterals at different segments in the cervical cord. Up to seven collaterals were given off from the stems of both LVST and MVST axons. The LVST axons included neurons that terminated both at the cervical cord level and further caudally in the thoracic or lumbar cord. Each collateral of these LVST axons, after entering the gray matter, ramified successively in a delta-like fashion to terminate mainly in lamina VIII and the medial part of lamina VII. Many boutons of both terminal and en passant type made contact with cell bodies and proximal dendrites of neurons in the ventromedial nucleus (VM). Each collateral had a narrow rostrocaudal extension (0.2–1.6 mm; average, 0.8 mm) in the gray matter in contrast to a much wider intercollateral interval (average, 1.5 mm). This meant that there were gaps, which were free of terminal boutons, between adjacent collateral arborizations. The morphology of the axon collaterals of MVST axons was very similar to that of the LVST axons. The rostrocaudal extent of their single axon collaterals was very restricted (0.3–2.1 mm) in contrast to the wider spread in the mediolateral and dorsoventral directions (0.9–2.6 mm). MVST axons had dense projections, with multiple axon collaterals, to the upper cervical cord. At the C1–3 levels, 1–7 collaterals of single MVST axons were identified. Their terminals were distributed in laminae VII–IX, including the VM, the nucleus of the spinal accessory
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Fig. 1. Spinal distribution of an uncrossed MVST axon. Projection patterns are shown at the C2 and C3 levels in the transverse (left-side) and horizontal (right-side) plane. The overall reconstruction was made from 90 serial sections. The stem axon was traced further rostrally (to 2.8 mm above B1). This axon has terminals in both the ventromedial (VM) and spinal accessory (A) nucleus. Note that these terminals are distributed in Rexed’s laminae IV–IX. Note further that many of the terminals of this axon made apparent contact with motoneurons supplying multiple neck muscles. (Reproduced from Shinoda et al., 1992a with permission from Wiley-Liss.)
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nerve (A) and the commissural nucleus. Many terminals made contact with retrogradely HRPlabeled motoneurons supplying neck muscles. Both axosomatic and axodendritic contacts were observed on motoneurons of various size. Some collaterals gave rise to terminal arborizations in both the VM and the A. These results suggest that single LVST and MVST axons may help control the excitability of motoneurons to multiple axial muscles concurrent with their control of limb muscles at multisegmental levels.
Convergent patterns of input from the semicircular canals to neck motoneurons The pattern of connections between different semicircular canals and motoneurons supplying dorsal neck muscles was first investigated by Wilson and Maeda (1974). Since then, the study of VS connections has been dominated by reports describing connections to a specific group of motoneurons that supply large dorsal neck muscles such as the biventer cervicis, complexus and splenius muscles (eg., Uchino and Isu, 1992). It has become increasingly apparent, however, that the large dorsal neck muscles involved in head movement represent a highly specialized group. More than 30 neck muscles must be controlled in an appropriate spatial and temporal pattern to induce a compensatory head movement in the same plane as the stimulated semicircular canal. Hence, it is more likely that there is more than one pattern of input from the six semicircular canals to motoneurons supplying different neck muscles. To address the above issue, we investigated the patterns of input and the pathways from the six semicircular canals to motoneurons supplying 16 different neck muscles in the anesthetized cat. Intracellularly recorded PSPs from neck motoneurons were obtained during electrical stimulation of the six individual canal nerves (Sugiuchi et al., 1992b; Shinoda et al., 1994, 1997). Their separate stimulation evoked either excitatory (EPSP) or inhibitory (IPSP) postsynaptic potentials in all the tested neck motoneurons. Furthermore, virtually all such motoneurons received convergent inputs from the six canal nerves. All the motoneurons supplying a single neck muscle had one of four homogeneous patterns of
input from the six semicircular canals. Figure 2 shows that the first of these four patterns was observed in motoneurons to the rectus capitis posterior (RCP) muscle. In Fig. 2A–C, note that both ipsi- and contralateral stimulation of the anterior canal nerve (ACN) produced an EPSP in the shown (exemplary) RCP motoneuron, whereas analogous stimulation of the posterior canal nerve (PCN) produced an IPSP. Stimulation of the ipsi- and contralateral lateral canal nerve (LCN) produced an IPSP and EPSP, respectively. To determine the central pathways that link the six semicircular canals to neck motoneurons, the effects of canal nerve stimulation were compared before and after a lesion of the medial longitudinal fasciculus (MLF), ipsilateral to the recorded motoneuron. After the cut, which was at the level of the obex, the EPSP evoked from the contralateral ACN and LCN disappeared, as did the IPSP from the contralateral PCN and the ipsilateral LCN and PCN. In contrast, the EPSP evoked by ipsilateral ACN stimulation remained unchanged. In other experiments, which are not shown in Fig. 2, a lesion was also made in the MLF contralateral to the recording site. In this case, however, no effect of sectioning was observed for bilateral canal inputs to RCP motoneurons. Most of the EPSPs evoked by stimulation of the bilateral ACNs and contralateral LCN, and the IPSPs evoked by stimulation of the ipsilateral PCN and LCN, had latencies <1.6 ms, and were therefore considered to be disynaptic. This input and connection pattern was seen in all the tested RCP motoneurons. The second pattern of input from the six semicircular canals was observed in motoneurons of the obliquus capitis inferior (OCI) muscle. Their EPSPs were evoked by stimulation of the ipsilateral ACN and PCN and the contralateral LCN, whereas IPSPs were evoked by stimulation of the contralateral ACN and PCN, and the ipsilateral LCN. The latency of most of these responses was 0.9–1.6 ms, so they, too, could be classed as disynaptic. In contrast, stimulation of the contralateral ACN induced IPSPs at a latency 1.8 ms, i.e., 1.0 ms longer than the disynaptic PSPs evoked by stimulation of the other canal nerves (Sugiuchi et al., 1995). These IPSPs were
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Fig. 2. Postsynaptic responses of an RCP motoneuron to stimulation of semicircular canal nerves before and after ipsilateral section of the MLF. (A–C) Control PSP responses with the MLF intact. (E–F) Analogous test responses after the complete MLF section. (A and D) Antidromic spikes (at two amplification levels) before (A) and after (D) the section. In A, the two smaller responses show monosynaptic EPSPs evoked by stimulation of neck muscle afferents. The upper voltage and the time calibration in A apply to the B–F traces. (B and C) Control PSPs evoked by stimulation of the three ipsilateral (B) and contralateral (C) canal nerves (Ant, anterior; Lat, lateral; Post, posterior). (E and F) Test PSPs recorded after the MLF section. In all cases, the strength of the stimulus pulse was 100 mA. During intracellular recording from this motoneuron, MLF sectioning at the level of the obex was performed in progressive mediolateral steps ipsilateral to the RCP motoneuron. The final (complete) lesion (hatched area) was reconstructed in a montage serial section (top middle sketch). This figure emphasizes that the lesion was well localized in the MLF and its immediate surroundings in the brainstem. Other abbreviations: NXII, hypoglossal nucleus; XII, hypoglossal nerve; IO, inferior olive; PT, pyramidal tract. (Reproduced from Shinoda et al., 1994 with permission from The American Physiological Society.)
classed as trisynaptic from primary vestibular afferents (Sugiuchi et al., 1992a). The third pattern of semicircular canal input was observed in motoneurons of the muscles innervated by the A. In these motoneurons, stimulation of the three contralateral canal nerves evoked disynaptic EPSPs, whereas stimulation of their three ipsilateral counterparts evoked disynaptic IPSPs. These EPSPs and IPSPs were completely abolished by sectioning the MLF ipsilateral to the recorded motoneurons.
The fourth pattern was observed in motoneurons of the longus capitis (LC) muscle. These motoneurons received EPSPs from the bilateral PCNs and the contralateral LCN, and IPSPs from the bilateral ACNs and the ipsilateral LCN. The latencies of these PSPs were mainly <1.8 ms and therefore considered to be disynaptic. The single exception was the IPSPs evoked by stimulation of the contralateral ACN, which had a latency >1.8 ms. Therefore, these IPSPs were most likely trisynaptic from primary vestibular afferents. In this pattern,
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section of the ipsilateral MLF eliminated the PSPs evoked by individual canal nerves except those produced by stimulation of the contralateral ACN. In contrast, section of the contralateral LVST eliminated the IPSPs evoked from the contralateral ACN, but left unaffected the PSPs from the other five canal nerves. Each of the examined 16 neck muscles was supplied by motoneurons with one of the above four patterns of input from the six canal nerves. Input patterns to the motoneurons of six of these muscles are exemplified in Fig. 3. The patterns shown emphasize the convergent nature of input from the six semicircular canals to motoneurons of individual neck muscles. Note that the same type of data exemplified in Fig. 3 also revealed the divergent output patterns from a particular semicircular canal to motoneurons supplying the 16 selected muscles. For example, an inhibitory output from the LCN is distributed to the six neck muscles shown in Fig. 3, whereas an inhibitory output from the PCN is distributed to five of the same six (i.e., the OCI motoneurons received no such input). By this means, we were able to delineate the divergent output patterns of the six individual semicircular canals to the motoneurons supplying 16 different neck muscles. To induce a compensatory head movement in the same plane as a stimulated semicircular canal, a signal from the latter must be distributed to an appropriate set of neck muscles. Two models seem possible for explaining the neural mechanisms underlying this spatial transformation in the vestibulocollic pathway. In one model: (1) each single MVST neuron innervates only one motor nucleus supplying a single neck muscle; and (2) primary afferents from a semicircular canal have a divergent projection pattern onto multiple MVST neurons. In the other model: (1) each single MVST neuron has a divergent projection pattern to a specific group of multiple motor nuclei; and (2) primary afferents originating from a semicircular canal innervate those MVST neurons that project to that particular group of multiple motor nuclei. The results presented above exclude the former model and provide indirect support for the latter one, because virtually all our sample of well-stained MVST axons were shown to project to more than one motor nucleus.
Innervation patterns of single MVST axons The important question arises as to whether the branching pattern of an individual MVST axon reveals if it innervates different motor nuclei randomly or selectively. The assumption is that the latter would involve a combination of motor nuclei to a specific set of functionally relevant neck muscles. To address this issue, we undertook experiments in which we first labeled motoneurons of different neck muscles retrogradely with either HRP or a fluorescent dye, and constructed a map of motor nuclei at the C1 and C2 levels that supplied different neck muscles (Sugiuchi and Shinoda, 1992). Next, MVST axons were impaled by a microelectrode inserted into the ipsilateral or contralateral MLF. They were identified as VS axons by their monosynaptic responses to stimulation of primary vestibular afferents. Each axon was then classified in terms of the semicircular canal input it received, i.e., from the lateral, anterior or posterior canal. This involved determining the axon’s maximal response to head rotations on a three-dimensional turntable (Shinoda et al., 1988, 1992b). As an example of the above experimental approach, we discuss below the properties of MVST axons receiving input from the ipsilateral posterior canal and projecting to ipsilateral neck motor nuclei. After the above-mentioned physiological identification, such axons were injected with HRP in the upper cervical cord where 2–3 motor nuclei were retrogradely labeled with HRP. These axons ran in the ipsilateral MLF, and they commonly exhibited a stereotypic innervation of the motor nuclei of (1) the sternomastoid–cleidomastoid muscles, (2) the semispinalis group (i.e., the biventer, complexus and multifidus cervicis muscles) and (3) the RCP muscle. Each single collateral of these axons did not necessarily terminate within all of these motor nuclei. Other collaterals arising from the same stem axon, however, terminated in one or more of these nuclei. In other words, single MVST axons innervated the above group of the motor nuclei by way of multiple collaterals. This spatial innervation pattern was found in almost all of the tested posterior canalrelated, uncrossed MVST axons. Figure 3 shows that posterior canal-related VS neurons include both excitatory and inhibitory neurons. The excitatory
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Fig. 3. Convergent input patterns and pathways from the six semicircular canals to motoneurons supplying six different neck muscles. Open and closed circles represent neurons that are excitatory and inhibitory, respectively. The key feature of this figure is that all the motoneurons supplying each neck muscle had a homogeneous pattern of input from the six semicircular canals. Abbreviations: A, H, and P, anterior, horizontal and posterior semicircular canal nerves, respectively; MN, neck motoneuron; MLF, medial longitudinal fasciculus.
neurons projected either contralaterally into the MLF or ipsilaterally in the LVST. Therefore, posterior canal-related VS axons passing in the ipsilateral MLF were most likely inhibitory to their target motoneurons, because posterior canal-related excitatory VS axons that projected ipsilaterally should be LVST axons and innervate motoneurons of the OCI muscle (viz. Fig. 3). Indeed, electron microscopic analysis of some HRP-labeled axon terminals of these VS axons demonstrated that their terminals had morphological characteristics of inhibitory synapses with OCI motoneurons (not illustrated). We further tried to specify functional synergies among neck muscles that were innervated by single MVST axons, which responded to input from other
semicircular canals. The posterior canal on one side is coplanar to the anterior canal on the opposite side. The above-mentioned posterior canal-related MVST axons on the ipsilateral side were inhibitory to the above-mentioned group of muscles. We also found that excitatory MVST axons on the contralateral side receiving input from the anterior semicircular canal terminated in the same group of neck motor nuclei. In other words, this result indicated that single MVST axons receiving input from either one of these coplanar canals exerted their influence on the same functional set of neck muscles, but with opposite effects. In summary, it was possible to show that single MVST axons receiving input from a particular
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semicircular canal had a common projection onto the motoneurons of a set of neck motor nuclei that were appropriate for that same semicircular canal. Furthermore, the MVST axons’ innervation patterns clearly explained the electrophysiologically determined output patterns from individual semicircular canals to motoneurons supplying functionally related sets of neck muscles.
Role of the tecto-reticulospinal system in the control of neck movements The superior colliculus (SC) is known to be an important center for the control of coordinated eye–head (orienting) movements. Electrical stimulation of the SC elicits coordinated eye and head movements toward a target, with the orientation direction dependent on the specific site of intra-SC stimulation. Thus, the output signals of the SC should contain specific information on which neck muscles should be coactivated. Collicular influences onto neck motoneurons are conveyed mainly by tectospinal axons (Muto et al., 1996) and more indirect pathways via the brainstem’s RTSTs. A key question is whether a single reticulospinal (RS) neuron may implement the same functional synergy among neck muscles as do vestibulocollic axons. To address this issue in the cat, we searched for RS axons in the upper cervical spinal cord of the cat. This involved their monosynaptic activation by stimulation of the contralateral SC, and their subsequent staining with HRP (Kakei et al., 1994). The stem axons of these RS neurons were shown to give rise to multiple axon collaterals which entered laminae VII– IX over a few cervical segments. They made contact with retrogradely HRP-labeled motoneurons supplying different neck muscles. We interpreted these results as meaning that RS axons simultaneously mediate output from the SC to motoneurons supplying functionally different groups of neck muscles. Furthermore, we showed that many RS axons innervate the same group of neck motor nuclei as do the posterior canal-related MVST axons. This finding strongly suggests that branching patterns of single RS axons are similar to those of single MVST axons, and that both single MVST and RS axons may have similar innervation patterns for neck
muscles, and thereby control the same functional sets of these muscles.
Summary In this chapter, we described our recent work on the divergent properties of single, long descending motor-tract neurons in the spinal cord, using the method of intra-axonal staining with HRP, and serial-section, three-dimensional reconstruction of their axonal trajectories. This work provides evidence that single motor-tract neurons are implicated in the neural implementation of functional synergies for head movements. Our results further show that single MVST neurons innervate a functional set of multiple neck muscles, and thereby implement a canaldependent, head-movement synergy. Additionally, both single MVST and RS axons may have similar innervation patterns for neck muscles, and thereby control the same functional sets of neck muscles. In order to stabilize redundant control systems in which many muscles generate force across several joints, the CNS routinely uses a combination of a control hierarchy and sensory feedback. In addition, in the head-movement system, the elaboration of functional synergies among neck muscles is another strategy, because it helps to decrease the degrees of freedom in this particularly complicated control system.
Acknowledgments This research was supported by Grants-in-Aid for Scientific Research from the Ministry of Education, Science and Culture of Japan to Y. Shinoda, Y. Sugiuchi and Y. Izawa.
Abbreviations ACN CNS CST EPSP HRP IPSP LC LCN
anterior canal nerve central nervous system corticospinal tract excitatory postsynaptic potential horseradish peroxidase inhibitory postsynaptic potential longus capitis lateral canal nerve
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LVST MLF MVST A OCI PCN PSP RBST RCP RS RTST SC Th VM VS
lateral vestibulospinal tract medial longitudinal fasciculus medial vestibulospinal tract nucleus of the spinal accessory nerve obliquus capitis inferior posterior canal nerve postsynaptic potential rubrospinal tract rectus capitis posterior reticulospinal reticulospinal tract superior colliculus thoracic ventromedial nucleus vestibulospinal
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421 Sensory Motor System. Oxford University Press, Oxford, pp. 235–240. Sugiuchi, Y., Kakei, S. and Shinoda, Y. (1992a). Spinal commissural neurons mediating vestibular input to neck motoneurons in the cat cervical spinal cord. Neurosci. Lett., 145: 221–225. Sugiuchi, Y., Futami, T., Ando, N., Kawasaki, T., Yagi, Y. and Shinoda, Y. (1992b). Patterns of connections between six semicircular canals and neck motoneurons. Ann. N.Y. Acad. Sci., 656: 957–959. Sugiuchi, Y., Izawa, Y. and Shinoda, Y. (1995). Trisynaptic inhibition from the contralateral vertical semicircular canal nerves to neck motoneurons mediated by spinal commissural neurons. J. Neurophysiol., 73: 1973–1987.
Suzuki, J.-I. and Cohen, B. (1964). Head eye, body and limb movements from semicircular canal nerves. Exp. Neurol., 10: 393–405. Uchino, Y. and Isu, N. (1992). Properties of vestibulo-ocular and/or vestibulo-collic neurons in the cat. In: Berthoz A., Vidal P.P. and Graf W. (Eds.), Head-Neck SensoryMotor System. Oxford University Press, New York, pp. 266–272. Wilson, V.J. and Maeda, M. (1974). Connections between semicircular canals and neck motoneurons in the cat. J. Neurophysiol., 37: 346–357. Wilson, V.J. and Melvill Jones, G. (1979). Mammalian Vestibular Physiology. Plenum Press, New York.
CHAPTER 39
Functional synergies among neck muscles revealed by branching patterns of single long descending motor-tract axons Yuriko Sugiuchi, Shinji Kakei, Yoshiko Izawa and Yoshikazu Shinoda* Department of Systems Neurophysiology, Graduate School of Medicine, Tokyo Medical and Dental University, Tokyo 113-8519, Japan
Abstract: In this chapter, we describe our recent work on the divergent properties of single, long descending motor-tract neurons in the spinal cord, using the method of intra-axonal staining with horseradish peroxidase, and serial-section, three-dimensional reconstruction of their axonal trajectories. This work provides evidence that single motor-tract neurons are implicated in the neural implementation of functional synergies for head movements. Our results further show that single medial vestibulospinal tract (MVST) neurons innervate a functional set of multiple neck muscles, and thereby implement a canal-dependent, head-movement synergy. Additionally, both single MVST and reticulospinal axons may have similar innervation patterns for neck muscles, and thereby control the same functional sets of neck muscles. In order to stabilize redundant control systems in which many muscles generate force across several joints, the CNS routinely uses a combination of a control hierarchy and sensory feedback. In addition, in the head-movement system, the elaboration of functional synergies among neck muscles is another strategy, because it helps to decrease the degrees of freedom in this particularly complicated control system.
Introduction
Abzug et al. (1974), who used electrophysiological techniques to show that 50% of the lateral vestibulospinal tract (LVST) neurons which supply axon branches to C6-Th1 segments, are also antidromically driven by stimulation of the lumbar spinal cord. A similar percentage of reticulospinal tract (RTST) neurons were then shown to send branches to the cervical gray matter, as well as to the first lumbar segment (Peterson et al., 1975). Even more unexpectedly, similar electrophysiological experiments have shown that both CST (Shinoda et al., 1986b) and rubrospinal tract (RBST; Shinoda et al., 1977) neurons project to both the cervical gray matter (C4–8) and the thoracic or lumbar spinal cord. Furthermore, virtually all CST neurons examined in the forelimb area of the motor cortex have 3–7 axon collaterals at widely separated segments of the cervical and upper thoracic cord (Shinoda et al., 1976). In addition, multiple axon collaterals of single
It had been tacitly assumed, and emphasized in most textbooks, that the pyramidal tract consists of ‘private lines’, which connect a discrete site in the motor cortex to a single muscle, just as a spinal motor nucleus usually innervates a single muscle. Similarly, corticospinal tract (CST) neurons have long been referred to as ‘upper motoneurons’ and motoneurons as ‘lower motoneurons’. Other long descending motor tracts have generally been considered to be similarly arranged. These assumptions are no longer tenable, however, because recent studies have shown that axons of all the major long descending motor tracts send axon collaterals to multiple spinal segments. This organization was first described by *Corresponding author: Tel.: þ 81-3-5803-5152; Fax: þ 81-3-5803-5155; E-mail: [email protected]
411 DOI: 10.1016/S0079-6123(03)43039-2
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RBST neurons have been found at different spinal segments (Shinoda et al., 1977). These electrophysiological findings all emphasize that single, motor-tract axons are not simple private lines for connecting the cells of cortical origin to the motoneurons of a single muscle, but, rather, such descending axons concurrently exert multiple influences on different groups of spinal interneurons and motoneurons at widely separated spinal segments. The above findings clearly have important implications for the descending control of posture and movement. It was not possible until recently, however, to reinforce these electrophysiological findings with relevant morphology, due to the inability to trace long axons from their cell bodies when using classical anatomical techniques. For visualization of the entire axonal morphology of a single neuron, especially one with a relatively long axon, new methods had to be developed, particularly ones which would bring into view the entire morphology of single, functionally identified neurons in the central nervous system (CNS). The enzyme, horseradish peroxidase (HRP), was shown to be particularly valuable for this purpose (Jankowska et al., 1976; Kitai et al., 1976; Snow et al., 1976). Admittedly, all of the processes of a single neuron labeled with HRP may not be visualized in a single section. Reconstruction of the axonal trajectory using serial sections, however, reveals the entire axonal trajectory of a single-labeled neuron for a distance of 10–30 mm in the mammalian CNS (for review, see Shinoda, 1999). In this chapter, we summarize our HRP-reconstruction studies on the intraspinal morphology of single axons of various long descending motor tracts in the cat and monkey. We show that the branching patterns of single vestibulocollic and tecto-reticulospinal axons may reveal the functional synergies among neck muscles that the CNS uses for the control of head movements.
Morphology of single CST and other long descending motor-tract axons Our initial study in this area was undertaken on the cat (Futami et al., 1979). First, we identified CST axons in the lateral funiculus of the cervical spinal
cord, by their direct responses to electrical stimulation of the contralateral motor cortex. Next, such an axon was injected iontophoretically with HRP. The trajectory of each single, stained axon was then reconstructed in serial sections of the spinal cord. The stem axon in the lateral funiculus gave rise to multiple axon collaterals at different spinal segments. Primary collaterals ran ventromedially and entered the gray matter. There, they ramified successively to form a delta-like branching pattern in the transverse plane, with terminations in Rexed’s laminae V–VII. In the horizontal plane, the axons bifurcated successively, gradually turning their orientation in parallel to the long axis of the spinal cord. Finally, they spread in both ascending and descending directions over a distance of l.3–3.0 mm. Similar branching patterns were subsequently found for the RBST axons of the cat (Shinoda et al., 1982). It was long known that in the cat spinal cord, both CST and RBST tracts terminate on interneurons, but not motoneurons (Lloyd, 1941). Therefore, in spite of our above-described demonstration of the existence of multiple axon collaterals at different spinal segments, it did not necessarily indicate that single axons in these tracts participate in the concurrent control of multiple muscles. On the other hand, Preston and Whitlock (1961) had shown that the CST of the monkey does indeed have direct projections onto spinal motoneurons. We took advantage of this morphological connection in an electrophysiological study, which showed that single monkey CST neurons were activated antidromically by stimulation of different motor nuclei in the cervical cord (Shinoda et al., 1979). In a subsequent study (Shinoda et al., 1981), we injected HRP into single CST axons in the lateral funiculus at the level of the cervical cord. These axons originated in the forelimb area of the monkey motor cortex. The stained CST axons had multiple axon collaterals in the cervical cord, and, importantly, such single axons projected to several motor nuclei supplying different forelimb muscles. Terminal boutons of these axons had close (presumed) contacts with dendrites of some of the motoneurons, which we also labeled with HRP, in multiple motor nuclei supplying the forelimb. This latter finding therefore showed that at least some CST neurons of the forelimb area of the motor cortex participate in the simultaneous control of multiple
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muscles of the forelimb. The question then arose as to which group of muscles is innervated by single, long descending motor-tract axons, i.e., what functional synergies among neck muscles are thereby implemented? The CST system in the monkey is not suitable to address this issue, because the abovementioned experiment is so technically difficult that its experimental yield is too low. Fortunately, it was known (Wilson and Melvill Jones, 1979) that vestibulospinal (VS) neurons have strong monosynaptic connections with neck motoneurons in the cat. Using this vestibulocollic system, we were indeed able to test for the implementation of a functional synergy by even a single, long descending motor-tract neuron.
The axonal trajectories of single vestibulospinal axons Head position control is an ideal paradigm for studying how the CNS controls a multidimensional motor system (Richmond and Vidal, 1988). Headmovement 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., a specific spatial and temporal combination rather than in an infinite variety of patterns. Stimulation of individual semicircular canals produces canal-specific head movements (Suzuki and Cohen, 1964). The plane of the head movement produced by canal stimulation parallels that of the stimulated canal, i.e., they are almost coplanar. Therefore, a signal from each semicircular canal must be distributed to an appropriate set of neck muscles in order to induce compensatory head movement in the same plane as the plane of the stimulated canal. Obviously, this process is more economical when a given descending motor command signal is distributed by a single neuron with divergent branches to multiple target motoneurons that participate in cocontraction of muscles to produce the required movement. The convergence of different canal nerve inputs onto single motoneurons has been extensively analyzed in the vestibulocollic system (Wilson and Melvill Jones,
1979), but its converse, divergent properties of VS axons, have not attracted attention until recently. To address the latter issue, we first analyzed the morphology of single physiologically identified lateral and medial VS tract (LVST and MVST) axons in the cat, by resort to intracellular HRP staining and subsequent three-dimensional reconstruction of axonal trajectories (Shinoda et al., 1986a, 1992a). An example of our approach is shown in Fig. 1. Axons were penetrated in the cervical cord at C1–8 with an HRP-filled microelectrode. These axons were identified as VS axons by their monosynaptic responses to stimulation of the vestibular nerve, and further classified as either LVST or MVST axons by their responses to stimulation of the LVST and MVST. Figure 1 shows that when stained, these axons could be traced for a rostrocaudal distance of 3–16 mm. Within this length, both LVST and MVST axons were found to have multiple axon collaterals at different segments in the cervical cord. Up to seven collaterals were given off from the stems of both LVST and MVST axons. The LVST axons included neurons that terminated both at the cervical cord level and further caudally in the thoracic or lumbar cord. Each collateral of these LVST axons, after entering the gray matter, ramified successively in a delta-like fashion to terminate mainly in lamina VIII and the medial part of lamina VII. Many boutons of both terminal and en passant type made contact with cell bodies and proximal dendrites of neurons in the ventromedial nucleus (VM). Each collateral had a narrow rostrocaudal extension (0.2–1.6 mm; average, 0.8 mm) in the gray matter in contrast to a much wider intercollateral interval (average, 1.5 mm). This meant that there were gaps, which were free of terminal boutons, between adjacent collateral arborizations. The morphology of the axon collaterals of MVST axons was very similar to that of the LVST axons. The rostrocaudal extent of their single axon collaterals was very restricted (0.3–2.1 mm) in contrast to the wider spread in the mediolateral and dorsoventral directions (0.9–2.6 mm). MVST axons had dense projections, with multiple axon collaterals, to the upper cervical cord. At the C1–3 levels, 1–7 collaterals of single MVST axons were identified. Their terminals were distributed in laminae VII–IX, including the VM, the nucleus of the spinal accessory
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Fig. 1. Spinal distribution of an uncrossed MVST axon. Projection patterns are shown at the C2 and C3 levels in the transverse (left-side) and horizontal (right-side) plane. The overall reconstruction was made from 90 serial sections. The stem axon was traced further rostrally (to 2.8 mm above B1). This axon has terminals in both the ventromedial (VM) and spinal accessory (A) nucleus. Note that these terminals are distributed in Rexed’s laminae IV–IX. Note further that many of the terminals of this axon made apparent contact with motoneurons supplying multiple neck muscles. (Reproduced from Shinoda et al., 1992a with permission from Wiley-Liss.)
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nerve (A) and the commissural nucleus. Many terminals made contact with retrogradely HRPlabeled motoneurons supplying neck muscles. Both axosomatic and axodendritic contacts were observed on motoneurons of various size. Some collaterals gave rise to terminal arborizations in both the VM and the A. These results suggest that single LVST and MVST axons may help control the excitability of motoneurons to multiple axial muscles concurrent with their control of limb muscles at multisegmental levels.
Convergent patterns of input from the semicircular canals to neck motoneurons The pattern of connections between different semicircular canals and motoneurons supplying dorsal neck muscles was first investigated by Wilson and Maeda (1974). Since then, the study of VS connections has been dominated by reports describing connections to a specific group of motoneurons that supply large dorsal neck muscles such as the biventer cervicis, complexus and splenius muscles (eg., Uchino and Isu, 1992). It has become increasingly apparent, however, that the large dorsal neck muscles involved in head movement represent a highly specialized group. More than 30 neck muscles must be controlled in an appropriate spatial and temporal pattern to induce a compensatory head movement in the same plane as the stimulated semicircular canal. Hence, it is more likely that there is more than one pattern of input from the six semicircular canals to motoneurons supplying different neck muscles. To address the above issue, we investigated the patterns of input and the pathways from the six semicircular canals to motoneurons supplying 16 different neck muscles in the anesthetized cat. Intracellularly recorded PSPs from neck motoneurons were obtained during electrical stimulation of the six individual canal nerves (Sugiuchi et al., 1992b; Shinoda et al., 1994, 1997). Their separate stimulation evoked either excitatory (EPSP) or inhibitory (IPSP) postsynaptic potentials in all the tested neck motoneurons. Furthermore, virtually all such motoneurons received convergent inputs from the six canal nerves. All the motoneurons supplying a single neck muscle had one of four homogeneous patterns of
input from the six semicircular canals. Figure 2 shows that the first of these four patterns was observed in motoneurons to the rectus capitis posterior (RCP) muscle. In Fig. 2A–C, note that both ipsi- and contralateral stimulation of the anterior canal nerve (ACN) produced an EPSP in the shown (exemplary) RCP motoneuron, whereas analogous stimulation of the posterior canal nerve (PCN) produced an IPSP. Stimulation of the ipsi- and contralateral lateral canal nerve (LCN) produced an IPSP and EPSP, respectively. To determine the central pathways that link the six semicircular canals to neck motoneurons, the effects of canal nerve stimulation were compared before and after a lesion of the medial longitudinal fasciculus (MLF), ipsilateral to the recorded motoneuron. After the cut, which was at the level of the obex, the EPSP evoked from the contralateral ACN and LCN disappeared, as did the IPSP from the contralateral PCN and the ipsilateral LCN and PCN. In contrast, the EPSP evoked by ipsilateral ACN stimulation remained unchanged. In other experiments, which are not shown in Fig. 2, a lesion was also made in the MLF contralateral to the recording site. In this case, however, no effect of sectioning was observed for bilateral canal inputs to RCP motoneurons. Most of the EPSPs evoked by stimulation of the bilateral ACNs and contralateral LCN, and the IPSPs evoked by stimulation of the ipsilateral PCN and LCN, had latencies <1.6 ms, and were therefore considered to be disynaptic. This input and connection pattern was seen in all the tested RCP motoneurons. The second pattern of input from the six semicircular canals was observed in motoneurons of the obliquus capitis inferior (OCI) muscle. Their EPSPs were evoked by stimulation of the ipsilateral ACN and PCN and the contralateral LCN, whereas IPSPs were evoked by stimulation of the contralateral ACN and PCN, and the ipsilateral LCN. The latency of most of these responses was 0.9–1.6 ms, so they, too, could be classed as disynaptic. In contrast, stimulation of the contralateral ACN induced IPSPs at a latency 1.8 ms, i.e., 1.0 ms longer than the disynaptic PSPs evoked by stimulation of the other canal nerves (Sugiuchi et al., 1995). These IPSPs were
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Fig. 2. Postsynaptic responses of an RCP motoneuron to stimulation of semicircular canal nerves before and after ipsilateral section of the MLF. (A–C) Control PSP responses with the MLF intact. (E–F) Analogous test responses after the complete MLF section. (A and D) Antidromic spikes (at two amplification levels) before (A) and after (D) the section. In A, the two smaller responses show monosynaptic EPSPs evoked by stimulation of neck muscle afferents. The upper voltage and the time calibration in A apply to the B–F traces. (B and C) Control PSPs evoked by stimulation of the three ipsilateral (B) and contralateral (C) canal nerves (Ant, anterior; Lat, lateral; Post, posterior). (E and F) Test PSPs recorded after the MLF section. In all cases, the strength of the stimulus pulse was 100 mA. During intracellular recording from this motoneuron, MLF sectioning at the level of the obex was performed in progressive mediolateral steps ipsilateral to the RCP motoneuron. The final (complete) lesion (hatched area) was reconstructed in a montage serial section (top middle sketch). This figure emphasizes that the lesion was well localized in the MLF and its immediate surroundings in the brainstem. Other abbreviations: NXII, hypoglossal nucleus; XII, hypoglossal nerve; IO, inferior olive; PT, pyramidal tract. (Reproduced from Shinoda et al., 1994 with permission from The American Physiological Society.)
classed as trisynaptic from primary vestibular afferents (Sugiuchi et al., 1992a). The third pattern of semicircular canal input was observed in motoneurons of the muscles innervated by the A. In these motoneurons, stimulation of the three contralateral canal nerves evoked disynaptic EPSPs, whereas stimulation of their three ipsilateral counterparts evoked disynaptic IPSPs. These EPSPs and IPSPs were completely abolished by sectioning the MLF ipsilateral to the recorded motoneurons.
The fourth pattern was observed in motoneurons of the longus capitis (LC) muscle. These motoneurons received EPSPs from the bilateral PCNs and the contralateral LCN, and IPSPs from the bilateral ACNs and the ipsilateral LCN. The latencies of these PSPs were mainly <1.8 ms and therefore considered to be disynaptic. The single exception was the IPSPs evoked by stimulation of the contralateral ACN, which had a latency >1.8 ms. Therefore, these IPSPs were most likely trisynaptic from primary vestibular afferents. In this pattern,
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section of the ipsilateral MLF eliminated the PSPs evoked by individual canal nerves except those produced by stimulation of the contralateral ACN. In contrast, section of the contralateral LVST eliminated the IPSPs evoked from the contralateral ACN, but left unaffected the PSPs from the other five canal nerves. Each of the examined 16 neck muscles was supplied by motoneurons with one of the above four patterns of input from the six canal nerves. Input patterns to the motoneurons of six of these muscles are exemplified in Fig. 3. The patterns shown emphasize the convergent nature of input from the six semicircular canals to motoneurons of individual neck muscles. Note that the same type of data exemplified in Fig. 3 also revealed the divergent output patterns from a particular semicircular canal to motoneurons supplying the 16 selected muscles. For example, an inhibitory output from the LCN is distributed to the six neck muscles shown in Fig. 3, whereas an inhibitory output from the PCN is distributed to five of the same six (i.e., the OCI motoneurons received no such input). By this means, we were able to delineate the divergent output patterns of the six individual semicircular canals to the motoneurons supplying 16 different neck muscles. To induce a compensatory head movement in the same plane as a stimulated semicircular canal, a signal from the latter must be distributed to an appropriate set of neck muscles. Two models seem possible for explaining the neural mechanisms underlying this spatial transformation in the vestibulocollic pathway. In one model: (1) each single MVST neuron innervates only one motor nucleus supplying a single neck muscle; and (2) primary afferents from a semicircular canal have a divergent projection pattern onto multiple MVST neurons. In the other model: (1) each single MVST neuron has a divergent projection pattern to a specific group of multiple motor nuclei; and (2) primary afferents originating from a semicircular canal innervate those MVST neurons that project to that particular group of multiple motor nuclei. The results presented above exclude the former model and provide indirect support for the latter one, because virtually all our sample of well-stained MVST axons were shown to project to more than one motor nucleus.
Innervation patterns of single MVST axons The important question arises as to whether the branching pattern of an individual MVST axon reveals if it innervates different motor nuclei randomly or selectively. The assumption is that the latter would involve a combination of motor nuclei to a specific set of functionally relevant neck muscles. To address this issue, we undertook experiments in which we first labeled motoneurons of different neck muscles retrogradely with either HRP or a fluorescent dye, and constructed a map of motor nuclei at the C1 and C2 levels that supplied different neck muscles (Sugiuchi and Shinoda, 1992). Next, MVST axons were impaled by a microelectrode inserted into the ipsilateral or contralateral MLF. They were identified as VS axons by their monosynaptic responses to stimulation of primary vestibular afferents. Each axon was then classified in terms of the semicircular canal input it received, i.e., from the lateral, anterior or posterior canal. This involved determining the axon’s maximal response to head rotations on a three-dimensional turntable (Shinoda et al., 1988, 1992b). As an example of the above experimental approach, we discuss below the properties of MVST axons receiving input from the ipsilateral posterior canal and projecting to ipsilateral neck motor nuclei. After the above-mentioned physiological identification, such axons were injected with HRP in the upper cervical cord where 2–3 motor nuclei were retrogradely labeled with HRP. These axons ran in the ipsilateral MLF, and they commonly exhibited a stereotypic innervation of the motor nuclei of (1) the sternomastoid–cleidomastoid muscles, (2) the semispinalis group (i.e., the biventer, complexus and multifidus cervicis muscles) and (3) the RCP muscle. Each single collateral of these axons did not necessarily terminate within all of these motor nuclei. Other collaterals arising from the same stem axon, however, terminated in one or more of these nuclei. In other words, single MVST axons innervated the above group of the motor nuclei by way of multiple collaterals. This spatial innervation pattern was found in almost all of the tested posterior canalrelated, uncrossed MVST axons. Figure 3 shows that posterior canal-related VS neurons include both excitatory and inhibitory neurons. The excitatory
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Fig. 3. Convergent input patterns and pathways from the six semicircular canals to motoneurons supplying six different neck muscles. Open and closed circles represent neurons that are excitatory and inhibitory, respectively. The key feature of this figure is that all the motoneurons supplying each neck muscle had a homogeneous pattern of input from the six semicircular canals. Abbreviations: A, H, and P, anterior, horizontal and posterior semicircular canal nerves, respectively; MN, neck motoneuron; MLF, medial longitudinal fasciculus.
neurons projected either contralaterally into the MLF or ipsilaterally in the LVST. Therefore, posterior canal-related VS axons passing in the ipsilateral MLF were most likely inhibitory to their target motoneurons, because posterior canal-related excitatory VS axons that projected ipsilaterally should be LVST axons and innervate motoneurons of the OCI muscle (viz. Fig. 3). Indeed, electron microscopic analysis of some HRP-labeled axon terminals of these VS axons demonstrated that their terminals had morphological characteristics of inhibitory synapses with OCI motoneurons (not illustrated). We further tried to specify functional synergies among neck muscles that were innervated by single MVST axons, which responded to input from other
semicircular canals. The posterior canal on one side is coplanar to the anterior canal on the opposite side. The above-mentioned posterior canal-related MVST axons on the ipsilateral side were inhibitory to the above-mentioned group of muscles. We also found that excitatory MVST axons on the contralateral side receiving input from the anterior semicircular canal terminated in the same group of neck motor nuclei. In other words, this result indicated that single MVST axons receiving input from either one of these coplanar canals exerted their influence on the same functional set of neck muscles, but with opposite effects. In summary, it was possible to show that single MVST axons receiving input from a particular
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semicircular canal had a common projection onto the motoneurons of a set of neck motor nuclei that were appropriate for that same semicircular canal. Furthermore, the MVST axons’ innervation patterns clearly explained the electrophysiologically determined output patterns from individual semicircular canals to motoneurons supplying functionally related sets of neck muscles.
Role of the tecto-reticulospinal system in the control of neck movements The superior colliculus (SC) is known to be an important center for the control of coordinated eye–head (orienting) movements. Electrical stimulation of the SC elicits coordinated eye and head movements toward a target, with the orientation direction dependent on the specific site of intra-SC stimulation. Thus, the output signals of the SC should contain specific information on which neck muscles should be coactivated. Collicular influences onto neck motoneurons are conveyed mainly by tectospinal axons (Muto et al., 1996) and more indirect pathways via the brainstem’s RTSTs. A key question is whether a single reticulospinal (RS) neuron may implement the same functional synergy among neck muscles as do vestibulocollic axons. To address this issue in the cat, we searched for RS axons in the upper cervical spinal cord of the cat. This involved their monosynaptic activation by stimulation of the contralateral SC, and their subsequent staining with HRP (Kakei et al., 1994). The stem axons of these RS neurons were shown to give rise to multiple axon collaterals which entered laminae VII– IX over a few cervical segments. They made contact with retrogradely HRP-labeled motoneurons supplying different neck muscles. We interpreted these results as meaning that RS axons simultaneously mediate output from the SC to motoneurons supplying functionally different groups of neck muscles. Furthermore, we showed that many RS axons innervate the same group of neck motor nuclei as do the posterior canal-related MVST axons. This finding strongly suggests that branching patterns of single RS axons are similar to those of single MVST axons, and that both single MVST and RS axons may have similar innervation patterns for neck
muscles, and thereby control the same functional sets of these muscles.
Summary In this chapter, we described our recent work on the divergent properties of single, long descending motor-tract neurons in the spinal cord, using the method of intra-axonal staining with HRP, and serial-section, three-dimensional reconstruction of their axonal trajectories. This work provides evidence that single motor-tract neurons are implicated in the neural implementation of functional synergies for head movements. Our results further show that single MVST neurons innervate a functional set of multiple neck muscles, and thereby implement a canaldependent, head-movement synergy. Additionally, both single MVST and RS axons may have similar innervation patterns for neck muscles, and thereby control the same functional sets of neck muscles. In order to stabilize redundant control systems in which many muscles generate force across several joints, the CNS routinely uses a combination of a control hierarchy and sensory feedback. In addition, in the head-movement system, the elaboration of functional synergies among neck muscles is another strategy, because it helps to decrease the degrees of freedom in this particularly complicated control system.
Acknowledgments This research was supported by Grants-in-Aid for Scientific Research from the Ministry of Education, Science and Culture of Japan to Y. Shinoda, Y. Sugiuchi and Y. Izawa.
Abbreviations ACN CNS CST EPSP HRP IPSP LC LCN
anterior canal nerve central nervous system corticospinal tract excitatory postsynaptic potential horseradish peroxidase inhibitory postsynaptic potential longus capitis lateral canal nerve
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LVST MLF MVST A OCI PCN PSP RBST RCP RS RTST SC Th VM VS
lateral vestibulospinal tract medial longitudinal fasciculus medial vestibulospinal tract nucleus of the spinal accessory nerve obliquus capitis inferior posterior canal nerve postsynaptic potential rubrospinal tract rectus capitis posterior reticulospinal reticulospinal tract superior colliculus thoracic ventromedial nucleus vestibulospinal
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