Abstract

The crustacean stomatogastric ganglion (STG) receives descending neuromodulatory inputs from three anterior ganglia, the paired commissural ganglia (CoGs) and the single esophageal ganglion (OG). In this paper we provide the first detailed and quantitative analyses of the short- and long-term effects of removal of these descending inputs (decentralization) on the pyloric rhythm of the STG. Thirty minutes after decentralization, the mean frequency of the pyloric rhythm dropped from 1.20 Hz in control to 0.52 Hz. Whereas the relative phase of pyloric neuron activity was approximately constant across frequency in the controls, after decentralization this changed markedly. Nine control preparations kept for 5-6 days in vitro maintained pyloric rhythm frequencies close to their control values. Nineteen decentralized preparations kept for 5-6 days dropped slightly in frequency from those seen at 30 minutes after decentralization, but then displayed stable activity over 6 days. Bouts of higher frequency activity were intermittently seen in both control and decentralized preparations, but the bouts began earlier and were more frequent in the decentralized preparations. Although the bouts may indicate that the removal of the modulatory inputs triggered changes in neuronal excitability, these changes did not produce obvious long-lasting changes in the frequency of the decentralized preparations.

Highlights

  • A fundamental but unresolved issue in neuroscience is how neurons and networks respond to the reduction or total loss of neuromodulatory inputs

  • We find that removal of neuromodulatory inputs from the stomatogastric ganglion of wild-caught Cancer borealis decreases frequency and alters phase relationships of the pyloric rhythm within 30 min, and that these changes persist across time

  • The first component includes two pyloric dilator (PD) neurons and a single anterior burster neuron (AB), which are electrically coupled and fire together, forming the pacemaker kernel of the network. Rhythmic inhibition from these neurons drives bursting activity in follower neurons: a single lateral pyloric (LP) neuron, which fires a burst of action potentials following the PD/AB burst; and a set of several pyloric constrictor (PY) neurons, which fire as the third component of the rhythm

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Summary

Introduction

A fundamental but unresolved issue in neuroscience is how neurons and networks respond to the reduction or total loss of neuromodulatory inputs. Panulirus interruptus, the importance of descending inputs from the paired commissural ganglia (CoGs) to the single stomatogastric ganglion (STG) for the generation of robust gastric mill and pyloric rhythms was first highlighted by reversible block of the stomatogastric nerve (stn) (Russell, 1976, 1979) This resulted in loss of gastric mill activity and decreases in the cycle frequency (subsequently referred to as frequency) of the pyloric rhythm, within minutes. Because the effects of excitatory neuromodulators are more seen when the pyloric rhythm is either very slow or stopped, the specific examples used as figures demonstrating the effects of neuromodulators in the literature have been inadvertently biased towards preparations with less robust pyloric rhythms after decentralization This has fostered the perception that decentralization in C. borealis routinely results in the loss of all pyloric rhythm activity, there have been no large data sets that address this issue. This has prompted us, in the first section of this paper, to provide data from more than a hundred preparations showing, for the first time, a quantitative analysis of the effects of short-term removal of the descending

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