Literature DB >> 11976370

Mechanisms underlying fictive feeding in aplysia: coupling between a large neuron with plateau potentials activity and a spiking neuron.

Abraham J Susswein1, Itay Hurwitz, Richard Thorne, John H Byrne, Douglas A Baxter.   

Abstract

The buccal ganglia of Aplysia contain a central pattern generator (CPG) that organizes the rhythmic movements of the radula and buccal mass during feeding. Many of the cellular and synaptic elements of this CPG have been identified and characterized. However, the roles that specific cellular and synaptic properties play in generating patterns of activity are not well understood. To examine these issues, the present study developed computational models of a portion of this CPG and used simulations to investigate processes underlying the initiation of patterned activity. Simulations were done with the SNNAP software package. The simulated network contained two neurons, B31/B32 and B63. The development of the model was guided and constrained by the available current-clamp data that describe the properties of these two protraction-phase interneurons B31/B32 and B63, which are coupled via electrical and chemical synapses. Several configurations of the model were examined. In one configuration, a fast excitatory postsynaptic potential (EPSP) from B63 to B31/B32 was implemented in combination with an endogenous plateau-like potential in B31/B32. In a second configuration, the excitatory synaptic connection from B63 to B31/B32 produced both fast and slow EPSPs in B31/B32 and the plateau-like potential was removed from B31/B32. Simulations indicated that the former configuration (i.e., electrical and fast chemical coupling in combination with a plateau-like potential) gave rise to a circuit that was robust to changes in parameter values and stochastic fluctuations, that closely mimicked empirical observations, and that was extremely sensitive to inputs controlling the onset of a burst. The coupling between the two simulated neurons served to amplify exogenous depolarizations via a positive feedback loop and the subthreshold activation of the plateau-like potential. Once a burst was initiated, the circuit produced the program in an all-or-none fashion. The slow kinetics of the simulated plateau-like potential played important roles in both initiating and maintaining the burst activity. Thus the present study identified cellular and network properties that contribute to the ability of the simulated network to integrate information over an extended period before a decision is made to initiate a burst of activity and suggests that similar mechanisms may operate in the buccal ganglia in initiating feeding movements.

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Year:  2002        PMID: 11976370     DOI: 10.1152/jn.2002.87.5.2307

Source DB:  PubMed          Journal:  J Neurophysiol        ISSN: 0022-3077            Impact factor:   2.714


  14 in total

1.  Autaptic muscarinic self-excitation and nitrergic self-inhibition in neurons initiating Aplysia feeding are revealed when the neurons are cultured in isolation.

Authors:  Ravit Saada-Madar; Nimrod Miller; Abraham J Susswein
Journal:  J Mol Histol       Date:  2012-05-10       Impact factor: 2.611

Review 2.  Phylogenetic and individual variation in gastropod central pattern generators.

Authors:  Akira Sakurai; Paul S Katz
Journal:  J Comp Physiol A Neuroethol Sens Neural Behav Physiol       Date:  2015-04-03       Impact factor: 1.836

3.  Inferring neuronal network functional connectivity with directed information.

Authors:  Zhiting Cai; Curtis L Neveu; Douglas A Baxter; John H Byrne; Behnaam Aazhang
Journal:  J Neurophysiol       Date:  2017-05-03       Impact factor: 2.714

4.  A quantitative model of conserved macroscopic dynamics predicts future motor commands.

Authors:  Connor Brennan; Alexander Proekt
Journal:  Elife       Date:  2019-07-11       Impact factor: 8.140

5.  In vitro analog of classical conditioning of feeding behavior in aplysia.

Authors:  Riccardo Mozzachiodi; Hilde A Lechner; Douglas A Baxter; John H Byrne
Journal:  Learn Mem       Date:  2003 Nov-Dec       Impact factor: 2.460

6.  The central pattern generator underlying swimming in Dendronotus iris: a simple half-center network oscillator with a twist.

Authors:  Akira Sakurai; Paul S Katz
Journal:  J Neurophysiol       Date:  2016-07-20       Impact factor: 2.714

7.  Functional differentiation of a population of electrically coupled heterogeneous elements in a microcircuit.

Authors:  Kosei Sasaki; Kosai Sasaki; Elizabeth C Cropper; Klaudiusz R Weiss; Jian Jing
Journal:  J Neurosci       Date:  2013-01-02       Impact factor: 6.167

8.  A specific synaptic pathway activates a conditional plateau potential underlying protraction phase in the Aplysia feeding central pattern generator.

Authors:  Nikolai C Dembrow; Jian Jing; Vladimir Brezina; Klaudiusz R Weiss
Journal:  J Neurosci       Date:  2004-06-02       Impact factor: 6.167

9.  The quest for action potentials in C. elegans neurons hits a plateau.

Authors:  Shawn R Lockery; Miriam B Goodman
Journal:  Nat Neurosci       Date:  2009-04       Impact factor: 24.884

10.  Organelle calcium-derived voltage oscillations in pacemaker neurons drive the motor program for food-seeking behavior in Aplysia.

Authors:  Alexis Bédécarrats; Laura Puygrenier; John Castro O'Byrne; Quentin Lade; John Simmers; Romuald Nargeot
Journal:  Elife       Date:  2021-06-30       Impact factor: 8.140

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