Synaptic organization of sensory and motor neurones innervating triceps brachii muscles in the bullfrog

Frank, Eric; Westerfield, Monte

doi:10.1113/jphysiol.1982.sp014125

Cited by 58 publications

(49 citation statements)

References 18 publications

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“…2). Although we could not identify motoneurones antidromically at this stage (see Methods), one-third of the motoneurones in the triceps region of the spinal cord innervate triceps muscles (Frank & Westerfield, 1982a), so approximately six or seven of the twenty cells were probably triceps motoneurones. In the few cells that did receive triceps input, the synaptic latency varied from 25 to 45 ms, and fluctuated by several milliseconds from trial to trial.…”

Section: Appearance Of Monosynaptic Sensory-motor Connexionsmentioning

confidence: 96%

“…Thus, even below the threshold for antidromic activation ofthe cell being studied, the synaptic input from sensory cells is contaminated by electrical coupling potentials from the antidromic impulses in other motoneurones. These problems have been discussed in detail elsewhere (Frank & Westerfield, 1982a;Westerfield & Frank, 1982). Because of these difficulties, we have not included measurements of homonymous sensory-motor connexions.…”

Section: Methodsmentioning

confidence: 99%

“…Spinal cords were isolated using procedures similar to those described earlier (Frank & Westerfield, 1982a;Westerfield & Frank, 1982). In most preparations the spinal cord was hemisected longitudinally near the dorsal-ventral mid line.…”

Section: Methodsmentioning

confidence: 99%

“…The development of synaptic connexions has been studied in many areas of the nervous system including the spinal cord. In adults, synapses between muscle sensory neurones and spinal cord motoneurones are highly ordered (Eccles, 1957), and their precise organization has been demonstrated in both mammals (Eccles, Eccles & Lundberg, 1957) and amphibians (Frank & Westerfield, 1982a). In general, muscle afferent axons project strongly to motoneurones innervating their own muscles (homonymous connexions), but weakly or not at all to motoneurones innervating functionally unrelated muscles.…”

Section: Introductionmentioning

confidence: 99%

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

Frank¹,

Westerfield²

1983

The Journal of Physiology

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SUMMARY1. 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.2. Sensory and motor axons in the triceps brachii muscle nerves were electrically excitable at stage XIII, the earliest stage studied. Their conduction velocities were 02-0)4 in/s. These velocities increased during subsequent development so that by stage XXII they were approximately 5 m/s.3. 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.4. 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.5. Both the electrical and chemical components, characteristic ofthese monosynaptic e.p.s.p.s in adult frogs, were prominent from the time the e.p.s.p.s first appeared.6. 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.7. 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.

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Section: Appearance Of Monosynaptic Sensory-motor Connexionsmentioning

confidence: 96%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

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

Frank¹,

Westerfield²

1983

The Journal of Physiology

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“…If the synaptic input caused orthodromic activation, a lower stimulation intensity was used (see Mendelson and Frank, 1991). Homonymous synaptic potentials often were obscured by the antidromic spike (Frank and Westerfield, 1982), for which the threshold is similar to those of Ia afferents. In these cases the stimulus was reduced below this threshold.…”

Section: Methodsmentioning

confidence: 99%

Formation of Specific Monosynaptic Connections between Muscle Spindle Afferents and Motoneurons in the Mouse

1997

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In adult vertebrates, sensory neurons innervating stretchsensitive muscle spindles make monosynaptic excitatory connections with specific subsets of motoneurons in the spinal cord. Spindle afferents (Ia fibers) make the strongest connections with motoneurons supplying the same (homonymous) muscle but make few or no connections with motoneurons supplying antagonistic or functionally unrelated muscles. In lower vertebrates these connections are specific from the time they first are formed, but there is comparatively little information about how these reflex connections form in mammals. We therefore studied the pattern of these synaptic connections during postnatal development in mice. Intracellular recordings were made from identified hindlimb motoneurons in an isolated spinal cord preparation, and monosynaptic inputs from Ia fibers in identified hindlimb muscle nerves were measured at different times during the first postnatal week. The pattern of connections was specific throughout this period. Ia fibers made strong connections with homonymous motoneurons but only weak connections with antagonistic motoneurons at every time point examined, from P0 through P7. Even when muscle nerves were stimulated at only 0.1 Hz, the pattern of connections was still highly specific, arguing against a special subpopulation of labile inappropriate connections. The absence of appreciable rearrangements in the pattern of these connections during the first postnatal week is, therefore, analogous to the situation in lower vertebrates, suggesting that mechanisms responsible for establishing this specificity have been conserved during evolution. Key words: synaptogenesis; synaptic specificity; motoneurons; muscle spindle afferents; Ia fibers; spinal cord; stretch reflexFor the nervous system to function correctly, specific patterns of synaptic connections must be established between appropriate groups of neurons. A commonly accepted paradigm for achieving this specificity is that chemoaffinity mechanisms are used to establish the initial pattern of connections, and then these connections are remodeled during subsequent development to refine the connectivity further (Goodman and Shatz, 1993). Coordinated electrical activity between pre-and postsynaptic partners can play a critical role in the refinement process.An alternative strategy used in other developmental systems is that chemoaffinity mechanisms are sufficient to produce a highly precise pattern of connections. In these systems, which have received the most attention in lower vertebrates and invertebrates, synaptic rearrangements are not seen. One example is the set of connections between muscle spindle sensory axons (Ia fibers) and spinal motoneurons, the synaptic pathway that mediates the simple stretch reflex. Ia afferents from one muscle make strong monosynaptic excitatory synapses with motoneurons supplying the same and synergistic muscles, but Ia afferents make few if any direct connections with motoneurons supplying antagonistic muscles. Studies in the frog and chick have ...

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Specificity of identified central synapses in the embryonic cockroach: Appropriate connections form before the onset of spontaneous afferent activity

1996

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The mechanisms by which neurons recognize the appropriate postsynaptic cells remain largely unknown. A useful approach to this problem is to use a system with a few identifiable neurons that form highly specific synaptic connections. We studied the development of synapses between two identified cercal sensory afferents and two giant interneurons (GIs) in the embryonic cockroach Periplaneta americana. By 46% of embryonic development, the axons of the filiform hair sensory neurons have entered the terminal ganglionic neuropil and grow alongside the GI primary dendrites, although they do not form synapses. From 50% of development, the GI dendrites grow outward from the center of the neuropil to contact the presynaptic axons and their branches. The sensory neurons begin to spike at 52% of development, and, from 55% of development, these action potentials evoked excitatory postsynaptic potentials in the GIs. Synaptic contacts were first seen at this time. The pattern of synaptic connections was highly specific from the outset. G12 had strong input from the medial (M) afferent and had almost negligible input from the lateral (L) afferent, whereas G13 had input from both. This specificity was present before bursts of spontaneous activity began in the sensory neurons at 59% of development. G12 filopodia selectively formed synaptic contacts with the M axon rather than the L axon. The few contacts made by G12 with the L axon had a normal morphology but fewer presynaptic densities. Filopodial insertions were not involved in selective synapse formation. In this system, highly specific synaptic recognition appears to be activity independent.

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Synaptic organization of sensory and motor neurones innervating triceps brachii muscles in the bullfrog

Cited by 58 publications

References 18 publications

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

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

Formation of Specific Monosynaptic Connections between Muscle Spindle Afferents and Motoneurons in the Mouse

Specificity of identified central synapses in the embryonic cockroach: Appropriate connections form before the onset of spontaneous afferent activity

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