Pyloric motor pattern modification by a newly identified projection neuron in the crab stomatogastric nervous system

J Neurophysiol. 1996 Jan;75(1):97-108. doi: 10.1152/jn.1996.75.1.97.

Abstract

1. We have used multiple, simultaneous intra- and extracellular recordings as well as Lucifer yellow dye-fills to identify modulatory commissural neuron 5 (MCN5) and characterize its effects in the stomatogastric nervous system (STNS) of the crab, Cancer borealis. MCN5 has a soma and neuropilar arborization in the commissural ganglion (CoG; Figs. 1 and 2), and it projects through the inferior esophageal nerve (ion) and stomatogastric nerve (stn) to the stomatogastric ganglion (STG; Figs. 1-3). 2. Within the CoGs, MCN5 receives esophageal rhythm-timed excitation and pyloric rhythm-timed inhibition (Fig. 4). Additionally, during the lateral teeth protractor phase of the gastric mill rhythm, the pyloric-timed inhibition of MCN5 is reduced or eliminated. 3. Intracellular stimulation of MCN5 excites the pyloric pacemaker ensemble, including the anterior burster (AB), pyloric dilator (PD), and lateral posterior gastric (LPG) neurons. This produces a faster pyloric rhythm. MCN5 stimulation also inhibits all nonpacemaker pyloric neurons, reducing or eliminating their activity (Figs. 5 and 6A; Tables 1 and 2). After MCN5 stimulation, bursting is enhanced for several cycles in some pyloric neurons when compared with their prestimulus activity (Figs. 5 and 6A; Tables 1 and 2). 4. MCN5 evokes distinct responses from each pyloric pacemaker neuron (Figs. 6-8). The AB and LPG neurons respond with increased activity. The AB response includes the presence of large amplitude excitatory postsynaptic potentials (EPSPs) that contribute to a depolarization of the trough of its rhythmic oscillations (Fig. 6). LPG responds by exhibiting increased activity that prolongs the duration of its burst beyond that of AB and PD (Fig. 7). In contrast, MCN5 stimulation initially produces decreased PD neuron activity, followed by a slight enhancement of each PD burst (Figs. 7 and 8). PD activity is further enhanced after MCN5 stimulation (Figs. 7 and 8). 5. MCN5-elicited action potentials evoke discrete, constant latency inhibitory postsynaptic potentials (IPSPs) in all nonpacemaker pyloric neurons, including the inferior cardiac (IC), lateral pyloric (LP), pyloric (PY), and ventricular dilator (VD) neurons (Fig. 9). MCN5 activity also inhibits these neurons indirectly, via its excitation of the pacemaker neurons. The pyloric pacemaker neurons synaptically inhibit all four nonpacemaker neurons. 6. The increased activity in the VD neuron, after MCN5 stimulation, is not mimicked by either direct hyperpolarization or by synaptically inhibiting VD via another pathway (Fig. 10). The poststimulation increase in IC neuron activity is stronger than that after hyperpolarizing current injection but is comparable with that resulting from stimulation of another inhibitory pathway (Fig. 10). The enhanced PY neuron activity is comparable with that resulting from either direct current injection or synaptic inhibition from another pathway (Fig. 10). 7. MCN5 activity increases the pyloric cycle frequency of both slow (< 1 Hz) and fast (1-2 Hz) rhythms (Fig. 11), and it significantly alters the phase relationships that define this motor pattern (Fig. 12). These phase relationships change again after MCN5 stimulation (Fig. 12). 8. MCN5 acts in concert with the pyloric pacemaker ensemble to elicit a pyloric rhythm that exhibits enhanced pacemaker neuron activity and reduced activity in all nonpacemaker neurons. Additionally, despite their electrical coupling, the three types of pacemaker neurons exhibit distinct responses to MCN5 stimulation. This partially uncouples their normally coactive bursts. The resulting motor pattern is distinct from all previously characterized pyloric rhythms.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Brachyura / physiology*
  • Ganglia, Invertebrate / physiology*
  • Gastric Emptying / physiology
  • Membrane Potentials / physiology
  • Motor Neurons / physiology*
  • Nerve Net / physiology*
  • Pylorus / innervation*
  • Synaptic Transmission / physiology