Analysis of muscle receptor connections by spike-triggered averaging. 1. Spindle primary and tendon organ afferents

Abstract

1. The synaptic connections of 44 single identified muscle spindle Ia afferents and of 21 Golgi tendon organ (Ib) afferents from medial gastrocnemius (MG) were studied in 46 cats by the spike-triggered averaging of synaptic noise in 803 motoneurons of various types. 2. The well-known monosynaptic Ia excitatory connections were confirmed and their characteristics examined in 113 cells. The method was used at greater sensitivity than before and revealed that, in addition to the larger EPSPs of the order of 300 muV, there were many below the previously reported lower 17-muV limit. 3. By studying the Ia disynaptic inhibitory pathway with quick stretch-evoked Ia volleys and by spike-triggered averaging (STA), it was shown that the latter method can reveal disynaptic and possibly trisynaptic excitatory connections. This is believed to depend on having continuous activity in the relevant interneurons. 4. Latencies of individual connections showed broad distributions and arguments are advanced for setting working limits to mono- and disynaptic paths for Ia excitation and inhibition. Monosynaptic EPSP latency from cord entry was 0.4-1.1 ms and disynaptic inhibition was 1.2-2.4 ms. It was recognized that the boundaries are not rigid and monosynaptic Ia EPSPs may have latencies up to 1.5 ms. 5. Rise times of disynaptic PSPs were, on average, significantly longer than monosynaptic, but individual disynaptic responses could have values within the monosynaptic range. 6. A small diphasic wave shortly preceding the monosynaptic EPSPs was interpreted as a presynaptic spike. Its timing was consistent with this and, as such, permitted estimates to be made of central conduction time. 7. An early negative wave (latency less than or equal 1.1 ms) of small emplitude was sometimes detected in antagonist motoneurons when triggering from Ia afferents. It was found tha extracellular fields could be detected due to single Ia afferent excitations and efforts were made to see if the early negative wave could be explained by this. In a few cases there was evidence that a very short-latency IPSP might be occuring. This evidence and its implications are discussed with attention to the new factors which have to be considered in using the spike-triggered averaging method at very high sensitivity. 8. Ib effect were di- or trisynaptic. They were excitatory to 18% of synergists and to 28% of antagonists. They were inhibitory to 41% of synergists and to 19% of antagonists. The Ib IPSPs were larger than the EPSPs.

Oligosynaptic excitation of motoneurones by impulses in group Ia muscle spindle afferents in the cat

“…(Schomberg & Behrends, 1978), supporting the conclusion that the latter are evoked oligosynaptically (see Introduction). Kirkwood & Sears' observations also strengthen the interpretation of Watt et al (1976) Hultborn & Wigstr6m (1975) the late long-lasting I a excitation is evoked primarily in homonymous motoneurones and in motoneurones of I a synergists (from ankle and toe extensors: soleus, gastrocnemius and plantaris, in soleus motoneurones), while the results presented in two previous papers (Fetz et al 1979;Jankowska et al 1981 b) show that the predominant Ia oligosynaptic effects to ankle and toe extensors are inhibitory. Other characteristic features of the Ia oligosynaptic excitation, i.e.…”

Excitatory post‐synaptic potentials from single muscle spindle afferents in external intercostal motoneurones of the cat.

“…297-298) nevertheless show that relatively large artifactual depolarizations could be created from this source in spiketriggered averaged recordings of unitary e.p.s.p.s. Interpretations of slowly rising components such as have been seen in a proportion of spike-triggered average e.p.s.p.s from most studies, particularly on the falling phases (Mendell & Henneman, 1971;Kirkwood & Sears, 1974Watt et al 1976;Munson & Sypert, 1979b;Munson et al 1980) Windhorst, 1977;Inbar, Madrid & Rudomin, 1979;Roscoe, Botterman, Reinking & Stuart, 1980), especially bearing in mind that the greater numbers of spindles present in these muscles means that an even weaker synchronization than we have shown in Fig. 5 would give significant artefacts.…”

The Transition from Development to Motor Control Function in the Corticospinal System

“…The number of spinal interneurons at the pipette tip receiving direct CS axon contacts and the amount of associated inward synaptic currents would be small compared with the capacity of the pipette to sample summed synaptic currents over several hundred micrometers. Unlike focal synaptic potentials, in which negative responses are localized to very discrete gray matter regions (Watt et al, 1976;Munson and Sypert, 1979), the distribution of the postsynaptic field potential we recorded was localized but broad (Fig. 4A).…”