Tests of the motor neuron model of the local pattern-generating circuits in the swimmeret system

Abstract

The motor pattern that drives each crayfish swimmeret consists of alternating bursts of impulses in power-stroke (PS) and return-stroke (RS) motor neurons. A model of the neural circuit that generates this pattern focused on connections between motor neurons themselves (Heitler, 1978, 1981). The model predicts that synergist motor neurons are electrically coupled, whereas antagonists make mostly inhibitory synapses. We tested this model by observing the responses of motor neurons to pressure ejection of GABA and glutamate, transmitters that crayfish motor neurons release at neuromuscular junctions, and by measuring the strengths and delays of synapses between pairs of motor neurons. Both GABA and glutamate inhibited motor neurons. This inhibition persisted when synaptic transmitter release was blocked by high Mg2+. The effects of GABA were mimicked by muscimol, but not by baclofen or the GABAc receptor agonist cis-4-aminocrotonic acid, and they were not blocked by bicuculline. The effects of glutamate were mimicked by ibotenic acid. Picrotoxin partially blocked glutamate's inhibition of the motor pattern, but did not affect GABA responses. Most (87%) pairs of synergist motor neurons tested made weak, noninverting connections. Approximately half of these had synaptic delays of <2 msec, consistent with direct electrical or chemical synapses. Individual motor neurons were dye-coupled to between one and three other motor neurons, and to interneurons. Less than half (44%) of the pairs of antagonist motor neurons tested made synaptic connections. These connections were weak, had long latencies (>4 msec), and therefore were probably polysynaptic. We conclude that direct synapses between swimmeret motor neurons cannot account for alternation of PS and RS bursts.

A Test of the Excitability-Gradient Hypothesis in the Swimmeret System of Crayfish

“…Since then, we have learned that each swimmeret has its own pattern-generating module of motor neurons and nonspiking local interneurons, and that these modules are coordinated by a separate circuit of coordinating interneurons (for review, see Mulloney et al, 1993). There is no evidence for "pacemaker cells" in these modules like those envisioned in the hypothesis; the cycle of PS-RS activity is best accounted for by the properties of a circuit of nonspiking local interneurons that drive the motor neurons (Perkel and Mulloney, 1974;Paul and Mulloney, 1986;Skinner et al, 1994;Sharp et al, 1996;Sherff and Mulloney, 1996). A contemporary restatement of the hypothesis would refer instead to a gradient of excitability of these modules in different segments.…”

“…Each swimmeret is innervated by its own set of motor neurons (Davis, 1968(Davis, , 1969Mulloney et al, 1990;Sherff and Mulloney, 1996) that are part of its pattern-generating module . These modules are located in individual segmental ganglia (see Fig.…”

“…1) that are separated spatially but linked together by interganglionic connectives in which thousands of axons run (Wiersma, 1958). The motor neurons themselves do not send axon collaterals to neighboring ganglia (Mulloney et al, 1990;Sherff and Mulloney, 1996), but coordinating interneurons do conduct information to neighboring modules about the activities of modules in each segment (Hughes and Wiersma, 1960;Stein, 1971Stein, , 1974Mulloney et al, 1993). The connections between neighboring ganglia are enough to permit a pair of ganglia to generate well coordinated swimmeret activity, with the same phase relations that they would exhibit in an intact animal (Paul and Mulloney, 1986).…”

Modulation of Force during Locomotion: Differential Action of Crustacean Cardioactive Peptide on Power-Stroke and Return- Stroke Motor Neurons

“…The normal saline solution contained (in mM) 195 NaC l, 5.36 KC l, 2.6 MgC l 2 , 13.5 C aC l 2 , and 10 Tris-maleate buffer at pH 7.4. Synaptic input to the motor neurons was blocked with a modified saline that contained 20ϫ normal Mg 2ϩ , 1:5 normal C a 2ϩ , and 3:5 normal Na ϩ (Sherff and Mulloney, 1996). The solution bathing the preparation was changed by switching it to a different source; the lag between switching the source and the new solution first reaching the bath was ϳ80 sec.…”

Mechanisms of Coordination in Distributed Neural Circuits: Decoding and Integration of Coordinating Information

“…Direct synaptic connections between crayfish neurons recorded at room temperature have brief synaptic delays, between 2.0 and 3.5 ms at chemical synapses (Sherff and Mulloney, 1996 (Fig. 1D), not with an IPS neuron.…”