Literature DB >> 31548235

Network Degeneracy and the Dynamics of Task Switching in the Feeding Circuit in Aplysia.

Yanqing Wang1, Klaudiusz R Weiss1, Elizabeth C Cropper2.   

Abstract

The characteristics of a network are determined by parameters that describe the intrinsic properties of the component neurons and their synapses. Degeneracy occurs when more than one set of parameters produces the same (or very similar) output. It is not clear whether network degeneracy impacts network function or is simply a reflection of the fact that, although it is important for a network to be able to generate a particular output, it is not important how this is achieved. We address this issue in the feeding network of the mollusc Aplysia In this system, there are two stimulation paradigms that generate egestive motor programs: repetition priming and positive biasing. We demonstrate that circuit parameters differ in the 2 cases (e.g., egestive repetition priming requires activity in an interneuron, B20, which is not essential for positive biasing). We show that degeneracy has consequences for task switching. If egestive repetition priming is immediately followed by stimulation of an ingestive input to the feeding central pattern generator, the first few cycles of activity are egestive (not ingestive). In this situation, there is a task switch cost. This "cost" is in part due to the potentiating effect of egestive repetition priming on B20. In contrast, there is no switch cost after positive biasing. Stimulation of the ingestive central pattern generator input immediately triggers ingestive activity. Our results indicate that the mechanisms used to pattern activity can impact network function in that they can determine how readily a network can switch from one configuration to another.SIGNIFICANCE STATEMENT A particular pattern of neural activity can be generated by more than one set of circuit parameters. How or whether this impacts network function is unclear. We address this issue in the feeding network of Aplysia and demonstrate that degeneracy in network function can have consequences for task switching. Namely, we show that, when egestive activity is generated via one set of circuit modifications, an immediate switch to ingestive activity is not possible. In contrast, rapid transitions to ingestive activity are possible if egestive activity is generated via a different set of circuit modifications.
Copyright © 2019 the authors.

Keywords:  central pattern generator; invertebrate; mollusc; motor program

Year:  2019        PMID: 31548235      PMCID: PMC6820203          DOI: 10.1523/JNEUROSCI.1454-19.2019

Source DB:  PubMed          Journal:  J Neurosci        ISSN: 0270-6474            Impact factor:   6.167


  38 in total

1.  The construction of movement with behavior-specific and behavior-independent modules.

Authors:  Jian Jing; Elizabeth C Cropper; Itay Hurwitz; Klaudiusz R Weiss
Journal:  J Neurosci       Date:  2004-07-14       Impact factor: 6.167

2.  Animal-to-animal variability of connection strength in the leech heartbeat central pattern generator.

Authors:  Rebecca C Roffman; Brian J Norris; Ronald L Calabrese
Journal:  J Neurophysiol       Date:  2011-12-21       Impact factor: 2.714

3.  Degeneracy and neuromodulation among thermosensory neurons contribute to robust thermosensory behaviors in Caenorhabditis elegans.

Authors:  Matthew Beverly; Sriram Anbil; Piali Sengupta
Journal:  J Neurosci       Date:  2011-08-10       Impact factor: 6.167

4.  Similar network activity from disparate circuit parameters.

Authors:  Astrid A Prinz; Dirk Bucher; Eve Marder
Journal:  Nat Neurosci       Date:  2004-11-21       Impact factor: 24.884

5.  Motor outputs in a multitasking network: relative contributions of inputs and experience-dependent network states.

Authors:  Allyson K Friedman; Yuriy Zhurov; Bjoern Ch Ludwar; Klaudiusz R Weiss
Journal:  J Neurophysiol       Date:  2009-10-21       Impact factor: 2.714

6.  Composite modulatory feedforward loop contributes to the establishment of a network state.

Authors:  Jin-Sheng Wu; Ferdinand S Vilim; Nathan G Hatcher; Michael R Due; Jonathan V Sweedler; Klaudiusz R Weiss; Jian Jing
Journal:  J Neurophysiol       Date:  2010-02-24       Impact factor: 2.714

7.  Cellular Effects of Repetition Priming in the Aplysia Feeding Network Are Suppressed during a Task-Switch But Persist and Facilitate a Return to the Primed State.

Authors:  Matthew H Perkins; Elizabeth C Cropper; Klaudiusz R Weiss
Journal:  J Neurosci       Date:  2018-06-22       Impact factor: 6.167

8.  Repetition priming of motor activity mediated by a central pattern generator: the importance of extrinsic vs. intrinsic program initiators.

Authors:  Michael J Siniscalchi; Elizabeth C Cropper; Jian Jing; Klaudiusz R Weiss
Journal:  J Neurophysiol       Date:  2016-07-27       Impact factor: 2.714

9.  Feeding behavior in Aplysia: a simple system for the study of motivation.

Authors:  I Kupfermann
Journal:  Behav Biol       Date:  1974-01

10.  Interneuronal and peptidergic control of motor pattern switching in Aplysia.

Authors:  Peter T Morgan; Jian Jing; Ferdinand S Vilim; Klaudiusz R Weiss
Journal:  J Neurophysiol       Date:  2002-01       Impact factor: 2.714

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  5 in total

1.  An Anticipatory Circuit Modification That Modifies Subsequent Task Switching.

Authors:  Yanqing Wang; Michael A Barry; Monica Cambi; Klaudiusz R Weiss; Elizabeth C Cropper
Journal:  J Neurosci       Date:  2021-01-26       Impact factor: 6.167

2.  Perturbation-specific responses by two neural circuits generating similar activity patterns.

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Journal:  Curr Biol       Date:  2021-09-09       Impact factor: 10.834

3.  Feeding state-dependent modulation of feeding-related motor patterns.

Authors:  Aaron P Cook; Michael P Nusbaum
Journal:  J Neurophysiol       Date:  2021-10-20       Impact factor: 2.974

4.  Feeding state functionally reconfigures a sensory circuit to drive thermosensory behavioral plasticity.

Authors:  Asuka Takeishi; Jihye Yeon; Nathan Harris; Wenxing Yang; Piali Sengupta
Journal:  Elife       Date:  2020-10-19       Impact factor: 8.140

5.  Chronic vs acute manipulations reveal degeneracy in a thermosensory neuron network.

Authors:  Jihye Yeon; Asuka Takeishi; Piali Sengupta
Journal:  MicroPubl Biol       Date:  2021-01-15
  5 in total

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