Termination patterns of identified group II and III afferent fibres from deep tissues in the spinal cord of the cat

In chloralose-anaesthetized cats, the impulse activity of single afferent fibres supplying receptors in the deep tissues of the hindlimb (fasciae, muscles, ligaments, joint capsules) was recorded using micropipettes filled with a solution of horseradish peroxidase. Only myelinated fibres with conduction velocities up to 40 m/s (Group III and Group II units) were studied, i.e. fast conducting afferent fibres from muscle spindles and tendon organs were excluded. The fibres were functionally characterized with the use of mechanical stimuli such as local pressure and joint movements. The results show that a relationship exists between the functional properties of a given afferent unit and the location of its terminals in the spinal cord. Since the conduction velocity and hence the diameter of the fibres was similar in all the units studied, these factors appear not to be of importance for determining the pattern of spinal termination. Out of 84 units, 42 were classified as high-threshold mechanosensitive, 26 as low-threshold mechanosensitive, and 16 as secondary endings from muscle spindles. Following physiological identification the fibres were ionophoretically injected with horseradish peroxidase and their trajectory in the white and gray matter of the spinal cord visualized histologically with diaminobenzidine. High-threshold mechanosensitive units took a lateral course in the posterior funiculus and usually did not bifurcate. They exhibited two different patterns of spinal termination, one being characterized by terminal arborizations in both lamina I and deeper laminae (mostly IV/V), the other one by an exclusive projection to lamina I. Low-threshold mechanosensitive units often showed a bifurcation in the posterior funiculus and did not have a uniform termination pattern. The main areas of termination were lamina II and laminae IV-VI. The slowly conducting secondary endings from muscle spindles projected mainly to laminae VI and VII with additional collaterals entering the ventral horn. They thus had a termination pattern similar to that reported for fast conducting afferent fibres (above 50 m/s) from muscle spindle secondary endings. With the exception of one high-threshold mechanosensitive unit none of the stained fibres possessed terminal arborization and boutons in lamina III. It is concluded that different types of Group II and III primary afferent fibres from deep tissues exhibit different patterns of spinal termination.(ABSTRACT TRUNCATED AT 400 WORDS)

[1]  J. Arvidsson,et al.  An HRP study of the central projections of primary trigeminal neurons which innervate tooth pulps in the cat , 1981, Brain Research.

[2]  P. Matthews,et al.  Mammalian muscle receptors and their central actions , 1974 .

[3]  E. Perl,et al.  Synaptic complexes formed by functionally defined primary afferent units with fine myelinated fibers , 1982, The Journal of comparative neurology.

[4]  P J Snow,et al.  Tracing axons and axon collaterals of spinal neurons using intracellular injection of horseradish peroxidase. , 1976, Science.

[5]  J. Fleshman,et al.  Monosynaptic projections of individual spindle group II afferents to type-identified medial gastrocnemius motoneurons in the cat. , 1982, Journal of neurophysiology.

[6]  A. Blomqvist,et al.  The central projection of muscle afferent fibres to the lower medulla and upper spinal cord: An anatomical study in the cat with the transganglionic transport method , 1984, The Journal of comparative neurology.

[7]  B. Peterson,et al.  Cat spinoreticular neurons: Locations, responses and changes in responses during repetitive stimulation , 1978, Brain Research.

[8]  F. Richmond,et al.  Central projections from cat suboccipital muscles: A study using transganglionic transport of horseradish peroxidase , 1984, The Journal of comparative neurology.

[9]  H. Fields,et al.  Somatosensory properties of spinoreticular neurons in the cat , 1977, Brain Research.

[10]  A. Apkarian,et al.  A dorsolateral spinothalamic pathway in cat , 1985, Brain Research.

[11]  H. Ha,et al.  Cell origin of the ventral spinocerebellar tract , 1968, The Journal of comparative neurology.

[12]  P. Brown,et al.  Projections of two hindlimb cutaneous nerves to cat dorsal horn. , 1980, Journal of neurophysiology.

[13]  A. Craig,et al.  Spinal and supraspinal terminations of primary afferent fibers from the gastrocnemius-soleus muscle in the cat , 1988, Neuroscience.

[14]  C. Marfurt.  The central projections of trigeminal primary afferent neurons in the cat as determined by the tranganglionic transport of horseradish peroxidase , 1981, The Journal of comparative neurology.

[15]  E. Perl,et al.  Spinal termination of functionally identified primary afferent neurons with slowly conducting myelinated fibers , 1979, The Journal of comparative neurology.

[16]  S Mense,et al.  Different types of slowly conducting afferent units in cat skeletal muscle and tendon. , 1985, The Journal of physiology.

[17]  W. C. Groat,et al.  Horseradish peroxidase tracing of visceral efferent and primary afferent pathways in the cat's sacral spinal cord using benzidine processing , 1978, Neuroscience Letters.

[18]  H. Ralston,et al.  Morphology and synaptic relationships of physiologically identified low-threshold dorsal root axons stained with intra-axonal horseradish peroxidase in the cat and monkey. , 1984, Journal of neurophysiology.

[19]  W. D. de Groat,et al.  Primary afferent projections of the major splanchnic nerve to the spinal cord and gracile nucleus of the cat , 1985, The Journal of comparative neurology.

[20]  F. Cerveró,et al.  Fine afferent fibers from viscera do not terminate in the substantia gelatinosa of the thoracic spinal cord , 1984, Brain Research.

[21]  A. Craig.  Spinocervical tract cells in cat and dog, labeled by the retrograde transport of horseradish peroxidase , 1976, Neuroscience Letters.

[22]  D. Maxwell,et al.  Ultrastructure and synaptic connections of cutaneous afferent fibres in the spinal cord , 1987, Trends in Neurosciences.

[23]  T. Hongo,et al.  Trajectory of group Ia afferent fibers stained with horseradish peroxidase in the lumbosacral spinal cord of the cat: Three dimensional reconstructions from serial sections , 1979, The Journal of comparative neurology.

[24]  T. Sears,et al.  Monosynaptic excitation of motoneurones from secondary endings of muscle spindles , 1974, Nature.

[25]  M. Matsushita,et al.  Contralateral termination of primary afferent axons in the sacral and caudal segments of the cat, as studied by anterograde transport of horseradish peroxidase , 1983, The Journal of comparative neurology.

[26]  E. Perl,et al.  Central projections of identified, unmyelinated (C) afferent fibers innervating mammalian skin. , 1986, Science.

[27]  R. Dubner,et al.  The cells of origin of the dorsal column postsynaptic projection in the lumbosacral enlargements of cats and monkeys. , 1983, Somatosensory research.

[28]  H. Hayashi,et al.  Morphology of terminations of small and large myelinated trigeminal primary afferent fibers in the cat , 1985, The Journal of comparative neurology.

[29]  C. Marfurt,et al.  The central projections of tooth pulp afferent neurons in the rat as determined by the transganglionic transport of horseradish peroxidase , 1984, The Journal of comparative neurology.

[30]  D. E. Haines,et al.  Contralateral projection of primary afferent fibers to mammalian spinal cord , 1979, Experimental Neurology.

[31]  C. Hodge,et al.  The spinothalamic tract: An examination of the cells of origin of the dorsolateral and ventral spinothalamic pathways in cats , 1987, The Journal of comparative neurology.

[32]  A. G. Brown,et al.  The morphology of group Ia afferent fibre collaterals in the spinal cord of the cat. , 1979, The Journal of physiology.

[33]  F. Richmond,et al.  Projections from C2 and C3 nerves supplying muscles and skin of the cat neck: A study using transganglionic transport of horseradish peroxidase , 1984, The Journal of comparative neurology.

[34]  H. Ralston,et al.  The distribution of dorsal root axons to laminae IV, V, and VI of the macaque spinal cord: A quantitative electron microscopic study , 1979, The Journal of comparative neurology.

[35]  A. Lundberg,et al.  Three ascending spinal pathways in the dorsal part of the lateral funiculus. , 1961, Acta physiologica Scandinavica.

[36]  M. Karnovsky,et al.  THF EARLY STAGES OF ABSORPTION OF INJECTED HORSERADISH PEROXIDASE IN THE PROXIMAL TUBULES OF MOUSE KIDNEY: ULTRASTRUCTURAL CYTOCHEMISTRY BY A NEW TECHNIQUE , 1966, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[37]  M. Wiberg,et al.  The spinomesencephalic tract in the cat: Its cells of origin and termination pattern as demonstrated by the intraaxonal transport method , 1984, Brain Research.

[38]  A. Craig,et al.  Spinothalamic lumbosacral lamina I cells responsive to skin and muscle stimulation in the cat. , 1985, The Journal of physiology.

[39]  J. Eccles,et al.  Intracellular recording from cells of the ventral spinocerebellar tract , 1961, The Journal of physiology.

[40]  M. Yamashita,et al.  Trajectory of group Ia and Ib fibers from the hind‐limb muscles at the L3 and L4 segments of the spinal cord of the cat , 1987, The Journal of comparative neurology.

[41]  W. Willis,et al.  Location of cells of origin of the spinothalamic tract in the lumbar enlargement of cat. , 1972, Experimental neurology.

[42]  A. G. Brown,et al.  Form and function of dorsal horn neurones with axons ascending the dorsal columns in cat. , 1981, The Journal of physiology.

[43]  S. Mense,et al.  Descending influences on the responses of spinocervical tract neurones to chemical stimulation of fine muscle afferents , 1979 .

[44]  P J Snow,et al.  The morphology of hair follicle afferent fibre collaterals in the spinal cord of the cat , 1977, The Journal of physiology.

[45]  E. Carstens,et al.  Laminar origins of spinothalamic projections in the cat as determined by the retrograde transport of horseradish peroxidase , 1978, The Journal of comparative neurology.

[46]  A. Craig,et al.  The distribution of afferent fibers from the gastrocnemius-soleus muscle in the dorsal horn of the peroxidase cat, as revealed by the transport of horseradish peroxidase , 1983, Neuroscience Letters.

[47]  G. Grant,et al.  Spinal cord projections from hindlimb muscle nerves in the rat studied by transganglionic transport of horseradish peroxidase, wheat germ agglutinin conjugated horseradish peroxidase, or horseradish peroxidase with dimethylsulfoxide , 1987, The Journal of comparative neurology.

[48]  M. Jacquin,et al.  Structure-function relationships in rat medullary and cervical dorsal horns. I. Trigeminal primary afferents. , 1986, Journal of neurophysiology.

[49]  J. Adams,et al.  Technical considerations on the use of horseradish peroxidase as a neuronal marker , 1977, Neuroscience.

[50]  N. Prabhakar,et al.  Spinal termination of nociceptive afferent fibres from deep tissues in the cat , 1986, Neuroscience Letters.

[51]  B. Rexed.  The cytoarchitectonic organization of the spinal cord in the cat , 1952, The Journal of comparative neurology.

[52]  David P. C. Lloyd,et al.  NEURON PATTERNS CONTROLLING TRANSMISSION OF IPSILATERAL HIND LIMB REFLEXES IN CAT , 1943 .

[53]  M. Beattie,et al.  Ultrastructural identification of dorsal root primary afferent terminals after anterograde filling with horseradish peroxidase , 1978, Brain Research.