Literature DB >> 18782747

Different functions for homologous serotonergic interneurons and serotonin in species-specific rhythmic behaviours.

James M Newcomb1, Paul S Katz.   

Abstract

Closely related species can exhibit different behaviours despite homologous neural substrates. The nudibranch molluscs Tritonia diomedea and Melibe leonina swim differently, yet their nervous systems contain homologous serotonergic neurons. In Tritonia, the dorsal swim interneurons (DSIs) are members of the swim central pattern generator (CPG) and their neurotransmitter serotonin is both necessary and sufficient to elicit a swim motor pattern. Here it is shown that the DSI homologues in Melibe, the cerebral serotonergic posterior-A neurons (CeSP-As), are extrinsic to the swim CPG, and that neither the CeSP-As nor their neurotransmitter serotonin is necessary for swim motor pattern initiation, which occurred when the CeSP-As were inactive. Furthermore, the serotonin antagonist methysergide blocked the effects of both the serotonin and CeSP-As but did not prevent the production of a swim motor pattern. However, the CeSP-As and serotonin could influence the Melibe swim circuit; depolarization of a cerebral serotonergic posterior-A was sufficient to initiate a swim motor pattern and hyperpolarization of a CeSP-A temporarily halted an ongoing swim motor pattern. Serotonin itself was sufficient to initiate a swim motor pattern or make an ongoing swim motor pattern more regular. Thus, evolution of species-specific behaviour involved alterations in the functions of identified homologous neurons and their neurotransmitter.

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Year:  2009        PMID: 18782747      PMCID: PMC2614243          DOI: 10.1098/rspb.2008.0683

Source DB:  PubMed          Journal:  Proc Biol Sci        ISSN: 0962-8452            Impact factor:   5.349


  48 in total

1.  Swimming behavior of the nudibranch Melibe leonina.

Authors:  K A Lawrence; W H Watson
Journal:  Biol Bull       Date:  2002-10       Impact factor: 1.818

2.  Cycle period of a network oscillator is independent of membrane potential and spiking activity in individual central pattern generator neurons.

Authors:  Paul S Katz; Akira Sakurai; Stefan Clemens; Deron Davis
Journal:  J Neurophysiol       Date:  2004-04-28       Impact factor: 2.714

3.  Comparative mapping of serotonin-immunoreactive neurons in the central nervous systems of nudibranch molluscs.

Authors:  James M Newcomb; David J Fickbohm; Paul S Katz
Journal:  J Comp Neurol       Date:  2006-11-20       Impact factor: 3.215

Review 4.  Pedigrees of neurobehavioral circuits: tracing the evolution of novel behaviors by comparing motor patterns, muscles, and neurons in members of related taxa.

Authors:  D H Paul
Journal:  Brain Behav Evol       Date:  1991       Impact factor: 1.808

5.  Motor control of the jamming avoidance response of Apteronotus leptorhynchus: evolutionary changes of a behavior and its neuronal substrates.

Authors:  W Heiligenberg; W Metzner; C J Wong; C H Keller
Journal:  J Comp Physiol A       Date:  1996-11       Impact factor: 1.836

6.  Single neuron control over a complex motor program.

Authors:  W N Frost; P S Katz
Journal:  Proc Natl Acad Sci U S A       Date:  1996-01-09       Impact factor: 11.205

7.  Mechanisms of pattern generation underlying swimming in Tritonia. IV. Gating of central pattern generator.

Authors:  P A Getting; M S Dekin
Journal:  J Neurophysiol       Date:  1985-02       Impact factor: 2.714

8.  Transition to endogenous bursting after long-term decentralization requires De novo transcription in a critical time window.

Authors:  M Thoby-Brisson; J Simmers
Journal:  J Neurophysiol       Date:  2000-07       Impact factor: 2.714

9.  The engrailed-expressing secondary head spots in the embryonic crayfish brain: examples for a group of homologous neurons in Crustacea and Hexapoda?

Authors:  Silvia Sintoni; Kathia Fabritius-Vilpoux; Steffen Harzsch
Journal:  Dev Genes Evol       Date:  2007-10-25       Impact factor: 0.900

10.  Modulation of swimming in Tritonia: excitatory and inhibitory effects of serotonin.

Authors:  A D McClellan; G D Brown; P A Getting
Journal:  J Comp Physiol A       Date:  1994-02       Impact factor: 1.836

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  14 in total

Review 1.  Homology and homoplasy of swimming behaviors and neural circuits in the Nudipleura (Mollusca, Gastropoda, Opisthobranchia).

Authors:  James M Newcomb; Akira Sakurai; Joshua L Lillvis; Charuni A Gunaratne; Paul S Katz
Journal:  Proc Natl Acad Sci U S A       Date:  2012-06-20       Impact factor: 11.205

Review 2.  Evolution of central pattern generators and rhythmic behaviours.

Authors:  Paul S Katz
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2016-01-05       Impact factor: 6.237

Review 3.  Neural mechanisms underlying the evolvability of behaviour.

Authors:  Paul S Katz
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2011-07-27       Impact factor: 6.237

4.  Serotonin regulates voltage-dependent currents in type I(e(A)) and I(i) interneurons of Hermissenda.

Authors:  Nan Ge Jin; Terry Crow
Journal:  J Neurophysiol       Date:  2011-08-03       Impact factor: 2.714

Review 5.  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

Review 6.  Sound Localization Strategies in Three Predators.

Authors:  Catherine E Carr; Jakob Christensen-Dalsgaard
Journal:  Brain Behav Evol       Date:  2015-09-24       Impact factor: 1.808

7.  Variations on a theme: species differences in synaptic connectivity do not predict central pattern generator activity.

Authors:  Charuni A Gunaratne; Akira Sakurai; Paul S Katz
Journal:  J Neurophysiol       Date:  2017-05-24       Impact factor: 2.714

8.  Serotonin influences locomotion in the nudibranch mollusc Melibe leonina.

Authors:  Stefanie L Lewis; Deborah E Lyons; Tiffanie L Meekins; James M Newcomb
Journal:  Biol Bull       Date:  2011-06       Impact factor: 1.818

9.  Premotor Neuron Divergence Reflects Vocal Evolution.

Authors:  Charlotte L Barkan; Darcy B Kelley; Erik Zornik
Journal:  J Neurosci       Date:  2018-05-21       Impact factor: 6.167

10.  Serotoninergic control of glycinergic inhibitory postsynaptic currents in rat hypoglossal motoneurons.

Authors:  John K Engelhardt; Valentina Silveira; Francisco R Morales; Ines Pose; Michael H Chase
Journal:  Brain Res       Date:  2010-05-10       Impact factor: 3.252

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