Feedforward compensation mediated by the central and peripheral actions of a single neuropeptide discovered using representational difference analysis

Jian Jing, Jonathan V. Sweedler, Elizabeth C. Cropper, Vera Alexeeva, Ji Ho Park, Elena V. Romanova, Fang Xie, Nikolai C. Dembrow, Bjoern C. Ludwar, Klaudiusz R. Weiss, Ferdinand S. Vilim

Research output: Contribution to journalArticle

Abstract

Compensatory mechanisms are often used to achieve stability by reducing variance, which can be accomplished via negative feedback during homeostatic regulation. In principle, compensation can also be implemented through feedforward mechanisms where a regulator acts to offset the anticipated output variation; however, few such neural mechanisms have been demonstrated. We provide evidence that an Aplysia neuropeptide, identified using an enhanced representational difference analysis procedure, implements feedforward compensation within the feeding network. We named the novel peptide "allatotropin-related peptide" (ATRP) because of its similarity to insect allatotropin. Mass spectrometry confirmed the peptide's identity, and in situ hybridization and immunostaining mapped its distribution in the Aplysia CNS. ATRP is present in the higher-order cerebral-buccal interneuron (CBI) CBI-4, but not in CBI-2. Previous work showed that CBI-4-elicited motor programs have a shorter protraction duration than those elicited by CBI-2. Here we show that ATRP shortens protraction duration of CBI-2-elicited ingestive programs, suggesting a contribution of ATRP to the parametric differences between CBI-4-evoked and CBI-2-evoked programs. Importantly, because Aplysia muscle contractions are a graded function of motoneuronal activity, one consequence of the shortening of protraction is that it can weaken protraction movements. However, this potential weakening is offset by feedforward compensatory actions exerted by ATRP. Centrally, ATRP increases the activity of protraction motoneurons. Moreover, ATRP is present in peripheral varicosities of protraction motoneurons and enhances peripheral motoneuron-elicited protraction muscle contractions. Therefore, feedforward compensatory mechanisms mediated by ATRP make it possible to generate a faster movement with an amplitude that is not greatly reduced, thereby producing stability.

Original languageEnglish (US)
Pages (from-to)16545-16558
Number of pages14
JournalJournal of Neuroscience
Volume30
Issue number49
DOIs
StatePublished - Dec 8 2010

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Neuropeptides
Cheek
Interneurons
Peptides
Aplysia
Motor Neurons
Muscle Contraction
allatotropin
In Situ Hybridization
Insects
Mass Spectrometry

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Feedforward compensation mediated by the central and peripheral actions of a single neuropeptide discovered using representational difference analysis. / Jing, Jian; Sweedler, Jonathan V.; Cropper, Elizabeth C.; Alexeeva, Vera; Park, Ji Ho; Romanova, Elena V.; Xie, Fang; Dembrow, Nikolai C.; Ludwar, Bjoern C.; Weiss, Klaudiusz R.; Vilim, Ferdinand S.

In: Journal of Neuroscience, Vol. 30, No. 49, 08.12.2010, p. 16545-16558.

Research output: Contribution to journalArticle

Jing, Jian ; Sweedler, Jonathan V. ; Cropper, Elizabeth C. ; Alexeeva, Vera ; Park, Ji Ho ; Romanova, Elena V. ; Xie, Fang ; Dembrow, Nikolai C. ; Ludwar, Bjoern C. ; Weiss, Klaudiusz R. ; Vilim, Ferdinand S. / Feedforward compensation mediated by the central and peripheral actions of a single neuropeptide discovered using representational difference analysis. In: Journal of Neuroscience. 2010 ; Vol. 30, No. 49. pp. 16545-16558.
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AU - Jing, Jian

AU - Sweedler, Jonathan V.

AU - Cropper, Elizabeth C.

AU - Alexeeva, Vera

AU - Park, Ji Ho

AU - Romanova, Elena V.

AU - Xie, Fang

AU - Dembrow, Nikolai C.

AU - Ludwar, Bjoern C.

AU - Weiss, Klaudiusz R.

AU - Vilim, Ferdinand S.

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