Development of sensory‐motor synapses in the spinal cord of the frog.

The development and specificity of monosynaptic sensory‐motor synapses were studied in the brachial spinal cord of bullfrog tadpoles. Intracellular and extracellular recordings were made from motoneurones innervating several different muscles of the forelimb. Excitatory synaptic potentials (e.p.s.p.s) were elicited by stimulation of various peripheral muscle nerves. Sensory and motor axons in the triceps brachii muscle nerves were electrically excitable at stage XIII, the earliest stage studied. Their conduction velocities were 0.2‐0.4 m/s. These velocities increased during subsequent development so that by stage XXII they were approximately 5 m/s. Before stage XVII, synaptic potentials evoked in motoneurones by stimulation of the triceps sensory fibres had a long central latency and fatigued easily. These potentials were probably mediated polysynaptically. At stage XVII, the first short‐latency triceps synaptic potentials appeared. They had central latencies of less than 3 ms and represented the direct, monosynaptic input from muscle sensory cells on to motoneurones. During subsequent development the percentage of triceps motoneurones innervated by triceps sensory fibres increased, while the number of long‐latency polysynaptic inputs decreased. Both the electrical and chemical components, characteristic of these monosynaptic e.p.s.p.s in adult frogs, were prominent from the time the e.p.s.p.s first appeared. The pattern of innervation of brachial motoneurones by triceps sensory afferents was specific from the beginning. Triceps sensory fibres innervated most triceps motoneurones but very few subscapular or pectoralis motoneurones, just as in adult frogs. At no time were there appreciable numbers of ‘aberrant’ connexions. The developmental time course of several different classes of sensory‐motor connexions was similar. Thus the synaptic specificity of this system cannot be explained by a differential timing of synaptogenesis.

[1]  J. Eccles,et al.  The convergence of monosynaptic excitatory afferents on to many different species of alpha motoneurones , 1957, The Journal of physiology.

[2]  E Henneman,et al.  Terminals of single Ia fibers: location, density, and distribution within a pool of 300 homonymous motoneurons. , 1971, Journal of neurophysiology.

[3]  S. Skoglund Activity of Muscle Receptors in the Kitten , 1960, Nature.

[4]  A. Mellström Recurrent and antidromic effects on the monosynaptic reflex during postnatal development in the cat. , 1971, Acta physiologica Scandinavica.

[5]  S. Skoglund Central Connections and Functions of Muscle Nerves in the Kitten , 1960 .

[6]  G. Fischbach,et al.  Synapse formation between dissociated nerve and muscle cells in low density cell cultures. , 1972, Developmental biology.

[7]  D. Purves,et al.  The elimination of redundant preganglionic innervation to hamster sympathetic ganglion cells in early post‐natal life. , 1980, The Journal of physiology.

[8]  W. Willis,et al.  Patterns of innervation of kitten motoneurones , 1963, The Journal of physiology.

[9]  M. Westerfield,et al.  The formation of appropriate central and peripheral connexions by foreign sensory neurones of the bullfrog , 1982, The Journal of physiology.

[10]  V. J. Wilson Reflex transmission in the kitten. , 1962, Journal of neurophysiology.

[11]  Unit activity in the isolated spinal cord of chick embryo, in situ. , 1970, Proceedings of the National Academy of Sciences of the United States of America.

[12]  K. Naka ELECTROPHYSIOLOGY OF THE FETAL SPINAL CORD. I. ACTION POTENTIALS OF THE MOTONEURON. , 1964 .

[13]  D. Purves,et al.  On the purpose of selective innervation of guinea‐pig superior cervical ganglion cells. , 1979, The Journal of physiology.

[14]  M. Jacobson,et al.  Development of reflexes from skin grafts in Rana pipiens: influence of size and position of grafts. , 1970, Developmental biology.

[15]  R. Miledi,et al.  Effects of some divalent cations on synaptic transmission in frog spinal neurones. , 1979, The Journal of physiology.

[16]  M. Letinsky The development of nerve-muscle junctions in Rana catesbeiana tadpoles. , 1974, Developmental biology.

[17]  A. I. Shapovalov,et al.  Mechanisms of post‐synaptic excitation in amphibian motoneurones. , 1978, The Journal of physiology.

[18]  R. Provine,et al.  Development of spinal cord bioelectric activity in spinal chick embryos and its behavioral implications. , 1977, Journal of neurobiology.

[19]  F. Ito Muscle spindle responses during contractions of extrafusal muscle fibers in the frog. , 1968, The Japanese journal of physiology.

[20]  A. I. Shapovalov,et al.  Dual mode of junctional transmission at synapses between single primary afferent fibres and motoneurones in the amphibian , 1980, The Journal of physiology.

[21]  K. Saito,et al.  Development of spinal reflexes in the rat fetus studied in vitro. , 1979, The Journal of physiology.

[22]  S. Skoglund,et al.  Postnatal excitability changes of kitten motoneurones. , 1971, Acta physiologica Scandinavica.

[23]  J. Eccles Electrophysiology of the Fetal Spinal Cord II . Interaction among peripheral inputs and recurrent inhibition , 2022 .

[24]  W. Willis,et al.  Presynaptic inhibition of the monosynaptic reflex pathway in kittens , 1963, The Journal of physiology.

[25]  A. C. Taylor,et al.  Stages in the normal development of Rana pipiens larvae , 1946, The Anatomical record.

[26]  A. Mellström Postnatal excitability changes of the ankle monosynaptic reflexes in the cat. , 1971, Acta physiologica Scandinavica.

[27]  R. Wyman Somatotopic Connectivity or Species Recognition Connectivity , 1973 .

[28]  Nancy Miner,et al.  Integumental specification of sensory fibers in the development of cutaneous local sign , 1956, The Journal of comparative neurology.

[29]  Specificity of electrical coupling among neurons innervating forelimb muscles of the adult bullfrog. , 1982, Journal of neurophysiology.

[30]  M. Westerfield,et al.  Synaptic organization of sensory and motor neurones innervating triceps brachii muscles in the bullfrog , 1982, The Journal of physiology.

[31]  R. Sperry CHEMOAFFINITY IN THE ORDERLY GROWTH OF NERVE FIBER PATTERNS AND CONNECTIONS. , 1963, Proceedings of the National Academy of Sciences of the United States of America.

[32]  E. Macagno,et al.  Mechanism for the formation of synaptic projections in the arthropod visual system , 1978, Nature.

[33]  W. Willis,et al.  The effect of repetitive stimulation upon monosynaptic transmission in kittens , 1965, The Journal of physiology.

[34]  V. Hamburger,et al.  Electrical activity in the spinal cord of the chick embryo, in situ. , 1970, Proceedings of the National Academy of Sciences of the United States of America.