Literature DB >> 20226670

A hormone-activated central pattern generator for courtship.

Daniel A Wagenaar1, M Sarhas Hamilton, Tracy Huang, William B Kristan, Kathleen A French.   

Abstract

BACKGROUND: Medicinal leeches (Hirudo spp.) are simultaneous hermaphrodites. Mating occurs after a stereotyped twisting and oral exploration that result in the alignment of the male and/or female gonopores of one leech with the complementary gonopores of a partner. The neural basis of this behavior is presently unknown and currently impossible to study directly because electrophysiological recording techniques disrupt the behavior.
RESULTS: Here we report that (Arg(8))-conopressin G and two other members of the oxytocin/vasopressin family of peptide hormones induce in Hirudo verbana a sequence of behaviors that closely mimic elements of spontaneous reproductive behavior. Through a series of progressively more reduced preparations, we show that one of these behaviors, a stereotyped twisting that is instrumental in aligning gonopores in preparation for copulation, is the product of a central pattern generator that consists of oscillators in ganglia M5 and M6 (the ganglia in the reproductive segments of the leech), and also in ganglion M4, which was not previously known to play a role in reproductive behavior. We find that the behavior is periodic, with a remarkably long cycle period of around five minutes, placing it among the slowest behavioral rhythms (other than diurnal and annual rhythms) yet described.
CONCLUSION: These results establish the leech as a new model system for studying aspects of the neuronal basis of reproductive behavior. 2010 Elsevier Ltd. All rights reserved.

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Year:  2010        PMID: 20226670      PMCID: PMC2858972          DOI: 10.1016/j.cub.2010.02.027

Source DB:  PubMed          Journal:  Curr Biol        ISSN: 0960-9822            Impact factor:   10.834


  31 in total

1.  Motor pattern switching in the heartbeat pattern generator of the medicinal leech: membrane properties and lack of synaptic interaction in switch interneurons.

Authors:  J Lu; S Gramoll; J Schmidt; R L Calabrese
Journal:  J Comp Physiol A       Date:  1999-03       Impact factor: 1.836

2.  Cloning, expression and pharmacological characterization of a vasopressin-related receptor in an annelid, the leech Theromyzon tessulatum.

Authors:  A Levoye; B Mouillac; G Rivière; D Vieau; M Salzet; C Breton
Journal:  J Endocrinol       Date:  2005-01       Impact factor: 4.286

3.  Peripheral organs control central neurogenesis in the leech.

Authors:  C A Baptista; T R Gershon; E R Macagno
Journal:  Nature       Date:  1990-08-30       Impact factor: 49.962

4.  Annetocin, an annelid oxytocin-related peptide, induces egg-laying behavior in the earthworm, Eisenia foetida.

Authors:  T Oumi; K Ukena; O Matsushima; T Ikeda; T Fujita; H Minakata; K Nomoto
Journal:  J Exp Zool       Date:  1996-10-01

5.  Possible functions of oxytocin/vasopressin-superfamily peptides in annelids with special reference to reproduction and osmoregulation.

Authors:  Y Fujino; T Nagahama; T Oumi; K Ukena; F Morishita; Y Furukawa; O Matsushima; M Ando; H Takahama; H Satake; H Minakata; K Nomoto
Journal:  J Exp Zool       Date:  1999-09-01

6.  Structural and functional evolution of the vasopressin/oxytocin superfamily: vasopressin-related conopressin is the only member present in Lymnaea, and is involved in the control of sexual behavior.

Authors:  R E Van Kesteren; A B Smit; R P De Lange; K S Kits; F A Van Golen; R C Van Der Schors; N D De With; J F Burke; W P Geraerts
Journal:  J Neurosci       Date:  1995-09       Impact factor: 6.167

Review 7.  Central oxytocin and reproductive behaviours.

Authors:  T R Insel; L Young; Z Wang
Journal:  Rev Reprod       Date:  1997-01

8.  Evidence for conservation of the vasopressin/oxytocin superfamily in Annelida.

Authors:  H Satake; K Takuwa; H Minakata; O Matsushima
Journal:  J Biol Chem       Date:  1999-02-26       Impact factor: 5.157

9.  Oxytocin-like peptide: a novel epitope colocalized with the FMRFamide-like peptide in the supernumerary neurons of the sex segmental ganglia of leeches--morphological and biochemical characterization; putative anti-diuretic function.

Authors:  M Salzet; C Wattez; M Verger-Bocquet; J C Beauvillain; J Malecha
Journal:  Brain Res       Date:  1993-01-22       Impact factor: 3.252

10.  Switching in the activity state of an interneuron that controls coordination of the hearts in the medicinal leech (Hirudo medicinalis).

Authors:  S Gramoll; J Schmidt; R L Calabrese
Journal:  J Exp Biol       Date:  1994-01       Impact factor: 3.312

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  26 in total

1.  Neurosecretion in reproductive behaviour of leeches.

Authors:  Nirmal Kumar Mishra
Journal:  J Biosci       Date:  2010-09       Impact factor: 1.826

Review 2.  Neuropeptide modulation of microcircuits.

Authors:  Michael P Nusbaum; Dawn M Blitz
Journal:  Curr Opin Neurobiol       Date:  2012-02-01       Impact factor: 6.627

3.  Centrally patterned rhythmic activity integrated by a peripheral circuit linking multiple oscillators.

Authors:  John Jellies; Daniel Kueh
Journal:  J Comp Physiol A Neuroethol Sens Neural Behav Physiol       Date:  2012-05-11       Impact factor: 1.836

4.  Responses to conflicting stimuli in a simple stimulus-response pathway.

Authors:  Pieter Laurens Baljon; Daniel A Wagenaar
Journal:  J Neurosci       Date:  2015-02-11       Impact factor: 6.167

5.  Global view of the evolution and diversity of metazoan neuropeptide signaling.

Authors:  Gáspár Jékely
Journal:  Proc Natl Acad Sci U S A       Date:  2013-05-01       Impact factor: 11.205

6.  The neuroanatomical distribution of oxytocin receptor binding and mRNA in the male rhesus macaque (Macaca mulatta).

Authors:  Sara M Freeman; Kiyoshi Inoue; Aaron L Smith; Mark M Goodman; Larry J Young
Journal:  Psychoneuroendocrinology       Date:  2014-04-12       Impact factor: 4.905

7.  Oxytocin in schizophrenia: a review of evidence for its therapeutic effects.

Authors:  Kai Macdonald; David Feifel
Journal:  Acta Neuropsychiatr       Date:  2011-12-19       Impact factor: 3.403

8.  Responses to mechanically and visually cued water waves in the nervous system of the medicinal leech.

Authors:  Andrew M Lehmkuhl; Arunkumar Muthusamy; Daniel A Wagenaar
Journal:  J Exp Biol       Date:  2018-02-22       Impact factor: 3.312

9.  Expression of arginine vasotocin receptors in the developing zebrafish CNS.

Authors:  Kenichi Iwasaki; Meari Taguchi; Joshua L Bonkowsky; John Y Kuwada
Journal:  Gene Expr Patterns       Date:  2013-07-02       Impact factor: 1.224

10.  Alpha-conotoxin ImI disrupts central control of swimming in the medicinal leech.

Authors:  Daniel A Wagenaar; Ruben Gonzalez; David C Ries; William B Kristan; Kathleen A French
Journal:  Neurosci Lett       Date:  2010-09-15       Impact factor: 3.046

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