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Addressing the spinal cord
Brain Research, 78 (1974) 3543
35
© Elsevier ScientificPublishingCompany, Amsterdam - Printed in The Netherlands
ADDRESSING THE SPINAL CORD
STEPHEN BLOMFIELD Division of Cell Biology, Medical Research Council, Laboratory of Molecular Biology, Cambridge CB2 2QH (Great Britain) (Accepted May 10th, 1974)
SUMMARY
It is suggested that the long fibres, descending to the spinal cord, address columns of motoneurones, such as have been described by Romanes. Anatomical and physiological evidence is adduced in support of this suggestion. The consequences of such a projection rule are examined for several descending tracts. It is shown that the organization of the motor cortical map may simply reflect the arrangement of the motoneurone columns within the spinal cord. That is, the mapping from motor cortex to spinal cord is continuous if one adopts the correct topology and 'tolerance' for the motoneurone pools. Finally, some developmental mechanisms that may account for this projection rule are briefly mentioned.
The descending tracts
The white matter of the mammalian spinal cord contains several long descending tracts. Prominent amongst them are the corticospinal, rubrospinal and lateral vestibulospinal tracts and the sulcomarginal zone, often termed the medial longitudinal fasciculus ~9 (see Fig. 1). Beside these fairly well-demarcated tracts are less well-defined pathways, from the reticular formation of the brain stem, which pass in the swathe of white matter enveloping the ventral horn 19. Collaterals are given off by the long fibres at various points along their descent. These collaterals pass to the neighbouring grey matter, where they may impinge directly onto motoneurones. But generally they act on interneurones, which may in turn form connections over several segmental levels28. The net result is that descending fibres do not have a restricted level of termination. This poses certain problems for the functions of these descending tracts. In particular, how is it that well-localised movements can be commanded by such apparently diffuse projections? We make the following hypothesis. Each descending fibre is constrained, during its development, to form contacts with members of a class of target neurones whose
36
S. BLOMFIELD
Cor ticospinal tract Rubrospinal tract Vestibulospinal tract Sulcomarginal zone
Fig. 1. Highly schematic diagram showing (on the left) the positions of some long descending tracts within the white matter and (on the right) the locations of motoneurone columns within the ventral horn. Motoneurones are grouped as they supply the body axis (A), the girdle and proximal limb muscles (B), and the distal limb muscles (C). The main influence of each descending tract falls on its neighbouring motoneurones columns. transverse location within the cord is accurately determined, but whose longitudinal position is only loosely specified. This has the following simple consequence. Those fibres, whose potential target neurones lie over many segments, will have a wide longitudinal distribution of collaterals, whilst those fibres, with target neurones confined to a few segments, will have a narrow collateral distribution.
Motoneurone columns To understand the significance of this observation, it is necessary to consider the arrangements of the motoneurones within the spinal cord. Several studies have shown that motoneurones tend to lie within longitudinal columns z~,27. Moreover, motoneurone columns concerned with given regions of the body tend to lie within restricted segmental zones of the cord (e.g. motoneurones to the distal limb muscles or to the girdle musculature). Generally the motoneurones within a column supply muscles that are coactive. For example, in the lumbosacral cord, the motoneurones to the extensors (anti-gravity muscles) lie in the most lateral part o f the ventrolateral cell columns; whereas the motoneurones supplying the morphological flexors lie ventromedially to the extensor group 27 (see Fig. 2). It is therefore possible to separately address these two classes of motoneurones. Perhaps most striking of all is the disposition of the motoneurones that supply the axial and neck musculature. These form a distinctive medial group, which runs unbroken for much of the length of the cord and is well separated from the ventrolateral motoneurone pools 25. Inputs to this column will
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Fig. 2. Arrangement of the ventrolateral motoneurone columns in cat. Certain features are apparent. One is that columns consist of largely synergistic motoneurones. Another is the fairly close spacing of antagonistic motoneurone pools. Lastly, as one passes round the border of the ventral horn, from its ventral aspect to its dorsolateral aspect, one comes across motoneurones that supply progressively more distal portions of the limb musculature. (Taken from Romanes 27, Fig. 18. Copywright, Wistar Institute.)
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consequently be spread over many segments. In contrast, the motoneurones that supply the extremities occupy the most dorsal portion of the ventrolateral cell group, and they are confined to very few segments 27. They can, therefore, receive the most intimate descending connections of all. Their position also permits them to be contacted directly by the long descending tracts of the lateral funiculus z4. This is presumably of importance in the fine control of movement of the digits.
Implication for the non-pyramidal tracts As a general rule, the descending tracts send collaterals to the zones of grey matter that they abut. This has been demonstrated both anatomically L9 22 and physiologically1°,24,3x. Thus, the main influence of the sulcomarginal zone falls on the ventromedial motoneurone column, which supplies the axial musculature. The individual fibres will send collaterals to widely distributed segments, yet with no drawback since the axial musculature contracts en bloc: control of individual segments is unlikely to be possible, especially in view of the fact that many back muscles bridge across several vertebrae s. Further, the actions of the sulcomarginal fibres will tend to be bilateral, since their endings are largely on the commissural neurones of the ventral horn. The lateral vestibulospinal tract, passing in the boundary region between the ventral and ventrolateral funiculi, is closely related to the motoneurones supplying the proximal limb muscles, particularly the extensors. Since these motoneurone groups only appear in the enlargements, the action of the lateral vestibulospinal tract will be confined to these muscle groups. The descending respiratory fibres constitute a sub-class of the reticulospinal fibres, and their influence falls mainly on the non-axial trunk musculature. Their action is the same over many segments 3°. Now the abdominal walt musculature is in effect a continuation of the intercostal musculature: it shows the same division into 3 main layers and these have the corresponding orientations 9. Respiratory influences can fall on the abdominal muscles, especially during deep breathing 3,4. This is in line with the view that descending fibres do not have a restricted longitudinal distribution but do have a restricted transverse distribution. The rubrospinal tract constitutes a major outflow for the cerebellum. Its position is well within the lateral funiculus. It does not appear to have direct access to motoneurones (with the possible exception of the most dorsally placed cell groups) but plays upon the interneurones of the intermediate grey matter. The lateral portions of the grey matter, which come most of all under its influence, are mainly concerned with flexor functions and control of distal musculature 14. Implications for the motor cortical map In the present context, only that portion of the corticospinal tract that arises from the precentral motor area (i.e. Brodman's areas 4 and 6) will be considered. The motor pyramidal tract projection has been investigated in several ways. By using electrical stimulation, Griinbaum and Sherrington showed the existence of a somatotopic representation of body movements on the exposed precentral cortex of
ADDRESSING THE SPINAL CORD
39
the ape11,lZ; in particular, they found separate leg, arm and face areas arranged along the mediolateral axis. Later studies by Woolsey and his colleagues on the 'motor' and 'premotor' areas of monkey cortex have confirmed these findings32,a3. Further, they have shown that the more rostral regions of agranular cortex are concerned with proximal limb, trunk and axial musculature. There seems no good reason to distinguish areas 4 and 6; functionally and structurally they appear similar; both receive projections from the ventrolateral thalamic nucleus 26. However, the notion that area 6 is premotor, long held sway and this is of some interest. The apparent reason for distinguishing these two regions was that the movements elicited by stimulation of area 6, are much more complex than those elicited by stimulation of area 4; moreover their threshold is considerably higher a4. Now this is not surprising. The spatial distributions of motor pyramidal cells, that project to the distal limb or to face musculature, are tight; the reason for this is that the motoneurones taking over their projections only exist in restricted regions of the brain stem of spinal cord (i.e. motor V and VII cranial nuclei and spinal motoneurone pools supplying the extremities). The threshold for producing movement is low, since the population ofpyramidals has a largely common destination. For the same reason, these movements are precisely localised and simple. However, the spatial distribution or motor pyramidals that project to parts of the axial and trunk musculature is much more diffuse; this time the motoneurones that receive their projections are widely spaced along the spinal cord. The threshold for evoking movement will be high, owing to the need to activate widely distributed pyramidals. And, in this case, the movements will be widespread, since the pyramidal population activated by a large stimulus will impinge on motoneurones in many different parts of the cord; they may even include movements of the extremities, since the stimulus need not spread far caudally in the cortex in order to reach their more tightly organised upper motoneurones. The use of repeated stimulation should permit one to pick out smaller populations of motor pyramidals, since their synaptic actions are greatly enhanced by repetition 24. The 'dissolution' of the simple pattern of representation 16, obtained on increasing the stimulus frequency, probably reflects the ability to excite spinal motoneurones, without much convergence, from the motor pyramidals. As such, it gives a more realistic picture of the motor cortical organisation, since the pyramidal neurones do fire at moderately high frequencies during voluntary movementsS, 6. Direct evidence for the organisation of the pyramidal cells in baboon motor cortex comes from the experiments of Phillips and otherslS, 24, as they have plotted the size of the monosynaptic response of a spinal motoneurone against the strength of cortical stimulation. Their results clearly demonstrate the tightness of the upper motoneurones related to distal musculature and the looser arrangement of the upper motoneurones related to more proximal musculature (see Fig. 3). Relevance to Jendrassik's manoeuvre
It is possible for a long descending fibre to form connections with the motoneurones to both fore- and hind-limbs, without forming any connections with the intervening trunk motoneurones 1. This is because the relevant class of target neurones
40
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Fig. 3. Dimensions of upper motoneurone colonies. Each curve plots the size of the monosynaptic EPSP in a motoneurone against the strength of a short stimulating pulse delivered to the motor cortex. The minimum current strength at which the EPSP saturates gives an indication of the dimension of the motor pyramidal colony that projects to the motoneurone concerned. These are (from the left) an ulnar, a radial and a musculocutaneous motoneurone. The first two have connections with small colonies whilst the third has a large associated colony. Small colonies are densely packed, large colonies are diffuse. (Taken from Phillips2a, Fig. 7. Copywright, American Medical Association.)
is missing at t h o r a c i c levels. The i m p l i c a t i o n s for l o c o m o t o r mechanisms are o b v i o u s ; the l i m b m o t o n e u r o n e s m a y receive instructions f r o m o v e r l a p p i n g sets o f u p p e r m o t o neurones. The existence o f long fibres t h a t p r o j e c t to b o t h fore-limb a n d h i n d - l i m b m o t o n e u r o n e s - - or, m o r e accurately, to interneurones which in t u r n act o n the m o t o n e u r o n e s - - c o u l d a c c o u n t for J e n d r a s s i k ' s m a n o e u v r e (i.e. the increase in size o f the knee j e r k reflex t h a t is p r o d u c e d by b r a c i n g the arms one against the other). Some o f the fibres t h a t are used to c o m m a n d e l b o w extension m a y also be used to c o m m a n d knee extension. This w o u l d be o f use in w a l k i n g a n d w o u l d n o t cause confusion in n o r m a l circumstances. W h e n i n d i v i d u a l l i m b m o v e m e n t s are required, those fibres activated, which are connected to b o t h groups o f l i m b m o t o n e u r o n e s , are by themselves insuflicient to cause irrelevant m o t o n e u r o n e firing - - they constitute an unrecognised input. But, t h o u g h subliminal, their effect will enhance the G r o u p l a reflex action o n these m o t o n e u r o n e s (see Fig. 4).
Developmental considerations The connections f o r m e d b y a given d e s c e n d i n g fibre may, to a large extent, be specified by the intrinsic genetic p r o g r a m o f t h a t fibre. H o w e v e r they m a y also be d e t e r m i n e d , in p a r t , by o t h e r factors such as (i) the time o f arrival o f the fibre in the cord, (ii) the availability o f susceptible target neurones 1~ a n d (iii) the actual l o c a t i o n o f the fibre in the white matter. The l a t t e r a p p e a r s to be an i m p o r t a n t factor. F o r instance, the s u l c o m a r g i n a l zone contains several phylogenetically o l d tracts, which
41
ADDRESSING THE SPINAL CORD Zone of active pyramidels
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colony overlaps the knee extensor colony. The members that they hold in common give fibre collaterals to both elbow and knee extensor motoneurones. Some of the activated pyramidals fall within this common intersect, but they are too few to cause knee extension. Nevertheless, their subliminal effect will enhance the tendon jerk reflex. 1, active 'elbow' fibre; 2, active 'elbow and knee' fibre; 3, inactive 'knee' fibre; A, body axis column; B, proximal limb columns; C, distal limb columns. have maintained their positions is, and presumably their functions, within the cord despite many other changes of form. However, a simple model o f development based solely on geometric constraints appears inadequate since, for example, the fibres of the corticospinal tract have lost all semblance o f somatotopic order at the level of the pyramidsL Some specification intrinsic to the long fibres therefore seems required. The rough level o f termination of a fibre could be determined by timing factors and the previous occupancy of potential sites by other fibres 17. If so, it may be that later arriving fibres are forced to seek lower levels of the cord or, alternatively, later appearing classes o f neurones - - this could be of particular relevance if, as seems plausible, the motoneurones supplying the limbs appear later than those supplying the body axis 7. It nevertheless remains true that the long fibres have a predominantly longitudinal zone of influence, whose extent is largely determined by factors intrinsic to the
42
s. BLOMFIELI)
spinal cord, to whit: the arrangement of the motoneurone pools and their associated interneuronal structures. ACKNOWLEDGEMENTS
I wish to thank Dr. Clarke Slater for helpful criticism of the manuscript. 1 am grateful to Professor Romanes and the Wistar Institute for permission to reproduce Fig. 2, and to Professor Phillips and the American Medical Association for permission to reproduce Fig. 3. This work was supported by a research fellowship from Christ's College, Cambridge.
REFERENCES 1 ABZUG, C., MAEDA, M., PETERSON, B. W., AND WILSON, V. J., Branching of individual lateral vestibulospinal axons at different spinal cord levels, Brain Research, 56 (1973) 327-330. 2 BARNARD, J. W., AND WOOLSEY, C. N., A study of localization in the corticospinal tracts of monkey and rat, J. comp. NeuroL, 105 (1956) 25-50. 3 CAMPBELL,E. J. M., An electromyographic study of the role of the abdominal muscles in breathing, J. Physiol. (Lond.), 117 (1952) 222-233. 4 CAMPBELL,E. J. M., AND GREEN, J. H., The expiratory function of the abdominal muscles in man. An electromyographic study, J. Physiol. (Lond.), 120 (1953) 409M.18. 5 EVARTS, E. V., Relation of pyramidal tract activity to force exerted during voluntary movement, J. Neurophysiol., 31 (1968) 14-27. 6 EVARTS, E. V., Activity of pyramidal tract neurons during postural fixation, J. Neurophysiol., 32 (1969) 375-385. 7 FUJITA, S., Analysis of neuron differentiation in the central nervous system by tritiated thymidine autoradiography, J. comp. Neurol., 122 (1964) 311-327. 8 GRAY'S ANATOMY(32nd edition), Longmans, Green, London, 1958, pp. 575-582. 9 GRAV'S ANATOMY (32nd edition), Longmans, Green, London, 1958, pp. 582-602. 10 GRILLNER, S., HONGO, T., AND LUND, S., Vestibulospinal tract. Effects on a-motoneurons in lumbo-sacral spinal cord in cat, Exp. Brain Res., 10 (1970) 94-120. 11 GRONBAUM,A. S., AND SI~RRINGTON, C. S., Observations on the physiology of the cerebral cortex of some of the higher apes, Proe. roy. Soe. B, 69 (1901) 206-209. 12 GRONBAUM,A. S., AND SHERRINGTON, C. S., Observations on the physiology of the cerebral cortex of the anthropoid apes, Proc. roy. Soc. B, 72 (1903) 152-155. 13 HAMORI, J., Development of synaptic organization in the partially agranular and in the transneuronally atrophid cerebellar cortex. In R. LLINAS (Ed.), Neurobiology of Cerebellar Evolution and Development, American Medical Association, Chicago, I11., 1969, pp. 845-858. 14 KUYPERS, H. G. J. M., The descending pathways to the spinal cord, their anatomy and function. In J. C. ECCLES AND J. P. SCHAD~ (Eds.), Organization of the Spinal Cord, Progr. Brain Res., Vol. 11, Elsevier, Amsterdam, 1964, pp. 178-202. 15 LANDGREN, S., PHILLIPS, C. G., AND PORTER, R., Cortical fields of origin of the monosynaptic pyramidal pathways to some motoneurones of the baboon's hand and forearm, J. Physiol. (Lond.), 161 (1962)91-111. 16 L1DELL, E. G. T., AND PHILLIPS, C. G., 'Overlapping areas in motor cortex of baboon, J. Physiol. (Lond.), 112 (1951) 392-399. 17 MUGNAINI, E., Neurones as synaptic targets. In P. ANDERSEN AND J. K. S. JANSEN (Eds.), Excitatory Synaptic Mechanisms, Universitetsforlaget, Oslo, 1970. 18 NIEUWENHUYS, R., Comparative anatomy of the spinal cord. In J. C. ECCLES AND J. P. SCHADE (Eds.), Organization of the Spinal Cord, Progr. Brain Res., Vol. 11, Elsevier, Amsterdam, 1964, pp. 1-57.
ADDRESSING THE SPINAL CORD
43
19 NYBERG-HANSEN,R., Sites and mode of termination of reticulospinal fibres in the cat, J. comp. NeuroL, 124 (1965) 71-100. 20 NYBERG-HANSEN,R., AND BRODAL, A., Sites of termination of corticospinal fibres in the cat, J. comp. Neurol., 120 (1963) 369-391. 21 NYBERG-HANSEN,R., AND BRODAL,A., Sites and mode of termination of rubrospinal fibres in the cat, J. Anat. (Lond.), 98 (1964) 235-253. 22 NYBERG-HANSEN,R., AND MASCETTI,T. A., Sites and mode of termination of fibres of the vestibulospinal tract in the cat, J. comp. Neurol., 122 (1964) 369-387. 23 PHILLIPS, C. G., Corticomotoneuronal organization, Arch. Neurol. (Chic.), 17 (1967) 188-195. 24 PHILLIPS, C. G., AND PORTER, R., The pyramidal projection to motoneurones of some muscle groups of the baboon's forelimb. In J. C. ECCLESAND J. P. SCHADI~(Eds.), Physiology of Spinal Neurons, Progr. Brain Res., Vol. 12, Elsevier, Amsterdam, 1964, pp. 222-245. 25 REXED, B., A cytoarchitectonic atlas of the spinal cord in the cat, J. comp. Neurol., 100 (1954) 297-351. 26 RISPAL-PADEL,L., AND MASSION,J., Relations between the ventrolateral nucleus and the motor cortex in the cat, Exp. Brain Res., 10 (1970) 331-339. 27 ROMANES,G. J., The motor cell columns of the lumbo-sacral spinal cord of the cat, J. comp. Neurol., 94 (1954) 313-358. 28 SCHEIBEL, M. E., AND SCHEIBEL,A. B., Terminal axonal patterns in the cat spinal cord I. The lateral corticospinal tract, Brain Research, 2 0966) 333-350. 29 SCttOEN, J. H. R., Comparative aspects of the descending fibre systems in the spinal cord. In J. C. ECCLES AND J. P. SCHADI~(Eds.), Organization of the Spinal Cord, Progr. Brain Res., Vol. 11, Elsevier, Amsterdam, 1964, pp. 203-222. 30 SEARS,T. A., Pathways of supra-spinal origin regulating the activity of respiratory motoneurones. In R. GRANIT (Ed.), Muscular Afferents and Motor Control, First Nobel Symposium, Almquist and Wiksell, Stockholm, 1965, pp. 187-196. 31 WILSON,V. J., YOSHIDA,M., AND SCHOR, R. H., Supraspinal monosynaptic excitation and inhibition of thoracic back motoneurons, Exp. Brain Res., l l (1970) 282-295. 32 WOOLSEY,C. N., Organization of somatic sensory and motor areas of the cerebral cortex. In H. F. HARLOW AND C. N. WOOLSEY(Eds.), Biological and Biochemical Bases of Behaviour, University of Wisconsin Press, Madison, Wise., 1958, pp. 63-81. 33 WOOLSEY,C. N., AND SETTLAGE, P. H., The pattern of localization in the precentral motor cortex of Macaca mulatta, Fed. Proc., 9 (1950) 140. 34 WOOLSEY,C. N., SETTLAGE,P. H., MEYER,D. R., SPENCER,W., HAMY, T. P., AND TRAVIS,A. M., Patterns of localization in precentral and 'supplementary' motor areas and their relation to the concept of a premotor area, Res. Publ. Ass. nerv. ment. Dis., 30 0952) 238-264.
35
© Elsevier ScientificPublishingCompany, Amsterdam - Printed in The Netherlands
ADDRESSING THE SPINAL CORD
STEPHEN BLOMFIELD Division of Cell Biology, Medical Research Council, Laboratory of Molecular Biology, Cambridge CB2 2QH (Great Britain) (Accepted May 10th, 1974)
SUMMARY
It is suggested that the long fibres, descending to the spinal cord, address columns of motoneurones, such as have been described by Romanes. Anatomical and physiological evidence is adduced in support of this suggestion. The consequences of such a projection rule are examined for several descending tracts. It is shown that the organization of the motor cortical map may simply reflect the arrangement of the motoneurone columns within the spinal cord. That is, the mapping from motor cortex to spinal cord is continuous if one adopts the correct topology and 'tolerance' for the motoneurone pools. Finally, some developmental mechanisms that may account for this projection rule are briefly mentioned.
The descending tracts
The white matter of the mammalian spinal cord contains several long descending tracts. Prominent amongst them are the corticospinal, rubrospinal and lateral vestibulospinal tracts and the sulcomarginal zone, often termed the medial longitudinal fasciculus ~9 (see Fig. 1). Beside these fairly well-demarcated tracts are less well-defined pathways, from the reticular formation of the brain stem, which pass in the swathe of white matter enveloping the ventral horn 19. Collaterals are given off by the long fibres at various points along their descent. These collaterals pass to the neighbouring grey matter, where they may impinge directly onto motoneurones. But generally they act on interneurones, which may in turn form connections over several segmental levels28. The net result is that descending fibres do not have a restricted level of termination. This poses certain problems for the functions of these descending tracts. In particular, how is it that well-localised movements can be commanded by such apparently diffuse projections? We make the following hypothesis. Each descending fibre is constrained, during its development, to form contacts with members of a class of target neurones whose
36
S. BLOMFIELD
Cor ticospinal tract Rubrospinal tract Vestibulospinal tract Sulcomarginal zone
Fig. 1. Highly schematic diagram showing (on the left) the positions of some long descending tracts within the white matter and (on the right) the locations of motoneurone columns within the ventral horn. Motoneurones are grouped as they supply the body axis (A), the girdle and proximal limb muscles (B), and the distal limb muscles (C). The main influence of each descending tract falls on its neighbouring motoneurones columns. transverse location within the cord is accurately determined, but whose longitudinal position is only loosely specified. This has the following simple consequence. Those fibres, whose potential target neurones lie over many segments, will have a wide longitudinal distribution of collaterals, whilst those fibres, with target neurones confined to a few segments, will have a narrow collateral distribution.
Motoneurone columns To understand the significance of this observation, it is necessary to consider the arrangements of the motoneurones within the spinal cord. Several studies have shown that motoneurones tend to lie within longitudinal columns z~,27. Moreover, motoneurone columns concerned with given regions of the body tend to lie within restricted segmental zones of the cord (e.g. motoneurones to the distal limb muscles or to the girdle musculature). Generally the motoneurones within a column supply muscles that are coactive. For example, in the lumbosacral cord, the motoneurones to the extensors (anti-gravity muscles) lie in the most lateral part o f the ventrolateral cell columns; whereas the motoneurones supplying the morphological flexors lie ventromedially to the extensor group 27 (see Fig. 2). It is therefore possible to separately address these two classes of motoneurones. Perhaps most striking of all is the disposition of the motoneurones that supply the axial and neck musculature. These form a distinctive medial group, which runs unbroken for much of the length of the cord and is well separated from the ventrolateral motoneurone pools 25. Inputs to this column will
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Fig. 2. Arrangement of the ventrolateral motoneurone columns in cat. Certain features are apparent. One is that columns consist of largely synergistic motoneurones. Another is the fairly close spacing of antagonistic motoneurone pools. Lastly, as one passes round the border of the ventral horn, from its ventral aspect to its dorsolateral aspect, one comes across motoneurones that supply progressively more distal portions of the limb musculature. (Taken from Romanes 27, Fig. 18. Copywright, Wistar Institute.)
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s. BLOMFIELD
consequently be spread over many segments. In contrast, the motoneurones that supply the extremities occupy the most dorsal portion of the ventrolateral cell group, and they are confined to very few segments 27. They can, therefore, receive the most intimate descending connections of all. Their position also permits them to be contacted directly by the long descending tracts of the lateral funiculus z4. This is presumably of importance in the fine control of movement of the digits.
Implication for the non-pyramidal tracts As a general rule, the descending tracts send collaterals to the zones of grey matter that they abut. This has been demonstrated both anatomically L9 22 and physiologically1°,24,3x. Thus, the main influence of the sulcomarginal zone falls on the ventromedial motoneurone column, which supplies the axial musculature. The individual fibres will send collaterals to widely distributed segments, yet with no drawback since the axial musculature contracts en bloc: control of individual segments is unlikely to be possible, especially in view of the fact that many back muscles bridge across several vertebrae s. Further, the actions of the sulcomarginal fibres will tend to be bilateral, since their endings are largely on the commissural neurones of the ventral horn. The lateral vestibulospinal tract, passing in the boundary region between the ventral and ventrolateral funiculi, is closely related to the motoneurones supplying the proximal limb muscles, particularly the extensors. Since these motoneurone groups only appear in the enlargements, the action of the lateral vestibulospinal tract will be confined to these muscle groups. The descending respiratory fibres constitute a sub-class of the reticulospinal fibres, and their influence falls mainly on the non-axial trunk musculature. Their action is the same over many segments 3°. Now the abdominal walt musculature is in effect a continuation of the intercostal musculature: it shows the same division into 3 main layers and these have the corresponding orientations 9. Respiratory influences can fall on the abdominal muscles, especially during deep breathing 3,4. This is in line with the view that descending fibres do not have a restricted longitudinal distribution but do have a restricted transverse distribution. The rubrospinal tract constitutes a major outflow for the cerebellum. Its position is well within the lateral funiculus. It does not appear to have direct access to motoneurones (with the possible exception of the most dorsally placed cell groups) but plays upon the interneurones of the intermediate grey matter. The lateral portions of the grey matter, which come most of all under its influence, are mainly concerned with flexor functions and control of distal musculature 14. Implications for the motor cortical map In the present context, only that portion of the corticospinal tract that arises from the precentral motor area (i.e. Brodman's areas 4 and 6) will be considered. The motor pyramidal tract projection has been investigated in several ways. By using electrical stimulation, Griinbaum and Sherrington showed the existence of a somatotopic representation of body movements on the exposed precentral cortex of
ADDRESSING THE SPINAL CORD
39
the ape11,lZ; in particular, they found separate leg, arm and face areas arranged along the mediolateral axis. Later studies by Woolsey and his colleagues on the 'motor' and 'premotor' areas of monkey cortex have confirmed these findings32,a3. Further, they have shown that the more rostral regions of agranular cortex are concerned with proximal limb, trunk and axial musculature. There seems no good reason to distinguish areas 4 and 6; functionally and structurally they appear similar; both receive projections from the ventrolateral thalamic nucleus 26. However, the notion that area 6 is premotor, long held sway and this is of some interest. The apparent reason for distinguishing these two regions was that the movements elicited by stimulation of area 6, are much more complex than those elicited by stimulation of area 4; moreover their threshold is considerably higher a4. Now this is not surprising. The spatial distributions of motor pyramidal cells, that project to the distal limb or to face musculature, are tight; the reason for this is that the motoneurones taking over their projections only exist in restricted regions of the brain stem of spinal cord (i.e. motor V and VII cranial nuclei and spinal motoneurone pools supplying the extremities). The threshold for producing movement is low, since the population ofpyramidals has a largely common destination. For the same reason, these movements are precisely localised and simple. However, the spatial distribution or motor pyramidals that project to parts of the axial and trunk musculature is much more diffuse; this time the motoneurones that receive their projections are widely spaced along the spinal cord. The threshold for evoking movement will be high, owing to the need to activate widely distributed pyramidals. And, in this case, the movements will be widespread, since the pyramidal population activated by a large stimulus will impinge on motoneurones in many different parts of the cord; they may even include movements of the extremities, since the stimulus need not spread far caudally in the cortex in order to reach their more tightly organised upper motoneurones. The use of repeated stimulation should permit one to pick out smaller populations of motor pyramidals, since their synaptic actions are greatly enhanced by repetition 24. The 'dissolution' of the simple pattern of representation 16, obtained on increasing the stimulus frequency, probably reflects the ability to excite spinal motoneurones, without much convergence, from the motor pyramidals. As such, it gives a more realistic picture of the motor cortical organisation, since the pyramidal neurones do fire at moderately high frequencies during voluntary movementsS, 6. Direct evidence for the organisation of the pyramidal cells in baboon motor cortex comes from the experiments of Phillips and otherslS, 24, as they have plotted the size of the monosynaptic response of a spinal motoneurone against the strength of cortical stimulation. Their results clearly demonstrate the tightness of the upper motoneurones related to distal musculature and the looser arrangement of the upper motoneurones related to more proximal musculature (see Fig. 3). Relevance to Jendrassik's manoeuvre
It is possible for a long descending fibre to form connections with the motoneurones to both fore- and hind-limbs, without forming any connections with the intervening trunk motoneurones 1. This is because the relevant class of target neurones
40
S. BLOMFIELD o
/
o
>
l"
2~
/ 2
/4
,
4 mA
Fig. 3. Dimensions of upper motoneurone colonies. Each curve plots the size of the monosynaptic EPSP in a motoneurone against the strength of a short stimulating pulse delivered to the motor cortex. The minimum current strength at which the EPSP saturates gives an indication of the dimension of the motor pyramidal colony that projects to the motoneurone concerned. These are (from the left) an ulnar, a radial and a musculocutaneous motoneurone. The first two have connections with small colonies whilst the third has a large associated colony. Small colonies are densely packed, large colonies are diffuse. (Taken from Phillips2a, Fig. 7. Copywright, American Medical Association.)
is missing at t h o r a c i c levels. The i m p l i c a t i o n s for l o c o m o t o r mechanisms are o b v i o u s ; the l i m b m o t o n e u r o n e s m a y receive instructions f r o m o v e r l a p p i n g sets o f u p p e r m o t o neurones. The existence o f long fibres t h a t p r o j e c t to b o t h fore-limb a n d h i n d - l i m b m o t o n e u r o n e s - - or, m o r e accurately, to interneurones which in t u r n act o n the m o t o n e u r o n e s - - c o u l d a c c o u n t for J e n d r a s s i k ' s m a n o e u v r e (i.e. the increase in size o f the knee j e r k reflex t h a t is p r o d u c e d by b r a c i n g the arms one against the other). Some o f the fibres t h a t are used to c o m m a n d e l b o w extension m a y also be used to c o m m a n d knee extension. This w o u l d be o f use in w a l k i n g a n d w o u l d n o t cause confusion in n o r m a l circumstances. W h e n i n d i v i d u a l l i m b m o v e m e n t s are required, those fibres activated, which are connected to b o t h groups o f l i m b m o t o n e u r o n e s , are by themselves insuflicient to cause irrelevant m o t o n e u r o n e firing - - they constitute an unrecognised input. But, t h o u g h subliminal, their effect will enhance the G r o u p l a reflex action o n these m o t o n e u r o n e s (see Fig. 4).
Developmental considerations The connections f o r m e d b y a given d e s c e n d i n g fibre may, to a large extent, be specified by the intrinsic genetic p r o g r a m o f t h a t fibre. H o w e v e r they m a y also be d e t e r m i n e d , in p a r t , by o t h e r factors such as (i) the time o f arrival o f the fibre in the cord, (ii) the availability o f susceptible target neurones 1~ a n d (iii) the actual l o c a t i o n o f the fibre in the white matter. The l a t t e r a p p e a r s to be an i m p o r t a n t factor. F o r instance, the s u l c o m a r g i n a l zone contains several phylogenetically o l d tracts, which
41
ADDRESSING THE SPINAL CORD Zone of active pyramidels
~,'~
Z~Z~
rye,,~ -
~ ~
.AA
Knee extensor colony
Elbow extensor colony
ed pyamidal tract
ABC Grey matter
White matter
Contralateral soinal cord Fig. 4. A possible explanation of Jendrassik's manoeuvre. In bracing the arms against each other, a population of pyramidal cells is activated which lies within the elbow extensor colony. Part of this
colony overlaps the knee extensor colony. The members that they hold in common give fibre collaterals to both elbow and knee extensor motoneurones. Some of the activated pyramidals fall within this common intersect, but they are too few to cause knee extension. Nevertheless, their subliminal effect will enhance the tendon jerk reflex. 1, active 'elbow' fibre; 2, active 'elbow and knee' fibre; 3, inactive 'knee' fibre; A, body axis column; B, proximal limb columns; C, distal limb columns. have maintained their positions is, and presumably their functions, within the cord despite many other changes of form. However, a simple model o f development based solely on geometric constraints appears inadequate since, for example, the fibres of the corticospinal tract have lost all semblance o f somatotopic order at the level of the pyramidsL Some specification intrinsic to the long fibres therefore seems required. The rough level o f termination of a fibre could be determined by timing factors and the previous occupancy of potential sites by other fibres 17. If so, it may be that later arriving fibres are forced to seek lower levels of the cord or, alternatively, later appearing classes o f neurones - - this could be of particular relevance if, as seems plausible, the motoneurones supplying the limbs appear later than those supplying the body axis 7. It nevertheless remains true that the long fibres have a predominantly longitudinal zone of influence, whose extent is largely determined by factors intrinsic to the
42
s. BLOMFIELI)
spinal cord, to whit: the arrangement of the motoneurone pools and their associated interneuronal structures. ACKNOWLEDGEMENTS
I wish to thank Dr. Clarke Slater for helpful criticism of the manuscript. 1 am grateful to Professor Romanes and the Wistar Institute for permission to reproduce Fig. 2, and to Professor Phillips and the American Medical Association for permission to reproduce Fig. 3. This work was supported by a research fellowship from Christ's College, Cambridge.
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19 NYBERG-HANSEN,R., Sites and mode of termination of reticulospinal fibres in the cat, J. comp. NeuroL, 124 (1965) 71-100. 20 NYBERG-HANSEN,R., AND BRODAL, A., Sites of termination of corticospinal fibres in the cat, J. comp. Neurol., 120 (1963) 369-391. 21 NYBERG-HANSEN,R., AND BRODAL,A., Sites and mode of termination of rubrospinal fibres in the cat, J. Anat. (Lond.), 98 (1964) 235-253. 22 NYBERG-HANSEN,R., AND MASCETTI,T. A., Sites and mode of termination of fibres of the vestibulospinal tract in the cat, J. comp. Neurol., 122 (1964) 369-387. 23 PHILLIPS, C. G., Corticomotoneuronal organization, Arch. Neurol. (Chic.), 17 (1967) 188-195. 24 PHILLIPS, C. G., AND PORTER, R., The pyramidal projection to motoneurones of some muscle groups of the baboon's forelimb. In J. C. ECCLESAND J. P. SCHADI~(Eds.), Physiology of Spinal Neurons, Progr. Brain Res., Vol. 12, Elsevier, Amsterdam, 1964, pp. 222-245. 25 REXED, B., A cytoarchitectonic atlas of the spinal cord in the cat, J. comp. Neurol., 100 (1954) 297-351. 26 RISPAL-PADEL,L., AND MASSION,J., Relations between the ventrolateral nucleus and the motor cortex in the cat, Exp. Brain Res., 10 (1970) 331-339. 27 ROMANES,G. J., The motor cell columns of the lumbo-sacral spinal cord of the cat, J. comp. Neurol., 94 (1954) 313-358. 28 SCHEIBEL, M. E., AND SCHEIBEL,A. B., Terminal axonal patterns in the cat spinal cord I. The lateral corticospinal tract, Brain Research, 2 0966) 333-350. 29 SCttOEN, J. H. R., Comparative aspects of the descending fibre systems in the spinal cord. In J. C. ECCLES AND J. P. SCHADI~(Eds.), Organization of the Spinal Cord, Progr. Brain Res., Vol. 11, Elsevier, Amsterdam, 1964, pp. 203-222. 30 SEARS,T. A., Pathways of supra-spinal origin regulating the activity of respiratory motoneurones. In R. GRANIT (Ed.), Muscular Afferents and Motor Control, First Nobel Symposium, Almquist and Wiksell, Stockholm, 1965, pp. 187-196. 31 WILSON,V. J., YOSHIDA,M., AND SCHOR, R. H., Supraspinal monosynaptic excitation and inhibition of thoracic back motoneurons, Exp. Brain Res., l l (1970) 282-295. 32 WOOLSEY,C. N., Organization of somatic sensory and motor areas of the cerebral cortex. In H. F. HARLOW AND C. N. WOOLSEY(Eds.), Biological and Biochemical Bases of Behaviour, University of Wisconsin Press, Madison, Wise., 1958, pp. 63-81. 33 WOOLSEY,C. N., AND SETTLAGE, P. H., The pattern of localization in the precentral motor cortex of Macaca mulatta, Fed. Proc., 9 (1950) 140. 34 WOOLSEY,C. N., SETTLAGE,P. H., MEYER,D. R., SPENCER,W., HAMY, T. P., AND TRAVIS,A. M., Patterns of localization in precentral and 'supplementary' motor areas and their relation to the concept of a premotor area, Res. Publ. Ass. nerv. ment. Dis., 30 0952) 238-264.