Glutamatergic innervation of the heart initiates retrograde contractions in adult Drosophila melanogaster

Davide Dulcis, Richard B Levine

Research output: Contribution to journalArticle

73 Citations (Scopus)

Abstract

The adult abdominal heart of Drosophila melanogaster receives extensive innervation from glutamatergic neurons at specific cardiac regions during metamorphosis. Here, we show that the neurons form presynaptic specializations, as indicated by the localization of synaptotagmin and active zone markers, adjacent to postsynaptic sites that have aggregates of glutamate IIA receptors. To determine the role of this innervation in cardiac function, we developed an optical technique, based on the movement of green fluorescent protein-labeled nerve terminals, to monitor heart beat in intact and semi-intact preparations. Simultaneous monitoring of adjacent cardiac chambers revealed the direction of contractions and allowed correlation with volume changes. The cardiac cycle is composed of an anterograde beat in alternation with a retrograde beat, which correlate respectively with systole and diastole of this multichambered heart. The periodic change in hemolymph direction is referred to as cardiac reversal. Intracellular recordings from muscles of the first abdominal cardiac chamber, the conical chamber, revealed pacemaker action potentials and the excitatory effect of local glutamate application, which initiated retrograde contractions in semi-intact preparations. Unilateral electrical stimulation of the transverse nerve containing the glutamatergic neuron that serves the conical chamber caused a chronotropic effect and initiation of retrograde contractions. This effect is distinct from that of peripheral crustacean cardioactive peptide (CCAP) neurons, which potentiate the anterograde beat. Cardiac reversal was evoked pharmacologically by sequentially applying CCAP and glutamate to the heart.

Original languageEnglish (US)
Pages (from-to)271-280
Number of pages10
JournalJournal of Neuroscience
Volume25
Issue number2
DOIs
StatePublished - Jan 12 2005

Fingerprint

Drosophila melanogaster
Neurons
Glutamic Acid
Synaptotagmins
Abdominal Muscles
Diastole
Hemolymph
Systole
Glutamate Receptors
Green Fluorescent Proteins
Electric Stimulation
Action Potentials
Direction compound
crustacean cardioactive peptide

Keywords

  • Active zones
  • Cardiac pacemaker
  • Crustacean cardioactive peptide
  • DGluRIIA receptors
  • Glutamate
  • Insect circulatory systems

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Glutamatergic innervation of the heart initiates retrograde contractions in adult Drosophila melanogaster. / Dulcis, Davide; Levine, Richard B.

In: Journal of Neuroscience, Vol. 25, No. 2, 12.01.2005, p. 271-280.

Research output: Contribution to journalArticle

@article{18a45ed5896240d2969c91b1fa7fadfa,
title = "Glutamatergic innervation of the heart initiates retrograde contractions in adult Drosophila melanogaster",
abstract = "The adult abdominal heart of Drosophila melanogaster receives extensive innervation from glutamatergic neurons at specific cardiac regions during metamorphosis. Here, we show that the neurons form presynaptic specializations, as indicated by the localization of synaptotagmin and active zone markers, adjacent to postsynaptic sites that have aggregates of glutamate IIA receptors. To determine the role of this innervation in cardiac function, we developed an optical technique, based on the movement of green fluorescent protein-labeled nerve terminals, to monitor heart beat in intact and semi-intact preparations. Simultaneous monitoring of adjacent cardiac chambers revealed the direction of contractions and allowed correlation with volume changes. The cardiac cycle is composed of an anterograde beat in alternation with a retrograde beat, which correlate respectively with systole and diastole of this multichambered heart. The periodic change in hemolymph direction is referred to as cardiac reversal. Intracellular recordings from muscles of the first abdominal cardiac chamber, the conical chamber, revealed pacemaker action potentials and the excitatory effect of local glutamate application, which initiated retrograde contractions in semi-intact preparations. Unilateral electrical stimulation of the transverse nerve containing the glutamatergic neuron that serves the conical chamber caused a chronotropic effect and initiation of retrograde contractions. This effect is distinct from that of peripheral crustacean cardioactive peptide (CCAP) neurons, which potentiate the anterograde beat. Cardiac reversal was evoked pharmacologically by sequentially applying CCAP and glutamate to the heart.",
keywords = "Active zones, Cardiac pacemaker, Crustacean cardioactive peptide, DGluRIIA receptors, Glutamate, Insect circulatory systems",
author = "Davide Dulcis and Levine, {Richard B}",
year = "2005",
month = "1",
day = "12",
doi = "10.1523/JNEUROSCI.2906-04.2005",
language = "English (US)",
volume = "25",
pages = "271--280",
journal = "Journal of Neuroscience",
issn = "0270-6474",
publisher = "Society for Neuroscience",
number = "2",

}

TY - JOUR

T1 - Glutamatergic innervation of the heart initiates retrograde contractions in adult Drosophila melanogaster

AU - Dulcis, Davide

AU - Levine, Richard B

PY - 2005/1/12

Y1 - 2005/1/12

N2 - The adult abdominal heart of Drosophila melanogaster receives extensive innervation from glutamatergic neurons at specific cardiac regions during metamorphosis. Here, we show that the neurons form presynaptic specializations, as indicated by the localization of synaptotagmin and active zone markers, adjacent to postsynaptic sites that have aggregates of glutamate IIA receptors. To determine the role of this innervation in cardiac function, we developed an optical technique, based on the movement of green fluorescent protein-labeled nerve terminals, to monitor heart beat in intact and semi-intact preparations. Simultaneous monitoring of adjacent cardiac chambers revealed the direction of contractions and allowed correlation with volume changes. The cardiac cycle is composed of an anterograde beat in alternation with a retrograde beat, which correlate respectively with systole and diastole of this multichambered heart. The periodic change in hemolymph direction is referred to as cardiac reversal. Intracellular recordings from muscles of the first abdominal cardiac chamber, the conical chamber, revealed pacemaker action potentials and the excitatory effect of local glutamate application, which initiated retrograde contractions in semi-intact preparations. Unilateral electrical stimulation of the transverse nerve containing the glutamatergic neuron that serves the conical chamber caused a chronotropic effect and initiation of retrograde contractions. This effect is distinct from that of peripheral crustacean cardioactive peptide (CCAP) neurons, which potentiate the anterograde beat. Cardiac reversal was evoked pharmacologically by sequentially applying CCAP and glutamate to the heart.

AB - The adult abdominal heart of Drosophila melanogaster receives extensive innervation from glutamatergic neurons at specific cardiac regions during metamorphosis. Here, we show that the neurons form presynaptic specializations, as indicated by the localization of synaptotagmin and active zone markers, adjacent to postsynaptic sites that have aggregates of glutamate IIA receptors. To determine the role of this innervation in cardiac function, we developed an optical technique, based on the movement of green fluorescent protein-labeled nerve terminals, to monitor heart beat in intact and semi-intact preparations. Simultaneous monitoring of adjacent cardiac chambers revealed the direction of contractions and allowed correlation with volume changes. The cardiac cycle is composed of an anterograde beat in alternation with a retrograde beat, which correlate respectively with systole and diastole of this multichambered heart. The periodic change in hemolymph direction is referred to as cardiac reversal. Intracellular recordings from muscles of the first abdominal cardiac chamber, the conical chamber, revealed pacemaker action potentials and the excitatory effect of local glutamate application, which initiated retrograde contractions in semi-intact preparations. Unilateral electrical stimulation of the transverse nerve containing the glutamatergic neuron that serves the conical chamber caused a chronotropic effect and initiation of retrograde contractions. This effect is distinct from that of peripheral crustacean cardioactive peptide (CCAP) neurons, which potentiate the anterograde beat. Cardiac reversal was evoked pharmacologically by sequentially applying CCAP and glutamate to the heart.

KW - Active zones

KW - Cardiac pacemaker

KW - Crustacean cardioactive peptide

KW - DGluRIIA receptors

KW - Glutamate

KW - Insect circulatory systems

UR - http://www.scopus.com/inward/record.url?scp=12144249953&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=12144249953&partnerID=8YFLogxK

U2 - 10.1523/JNEUROSCI.2906-04.2005

DO - 10.1523/JNEUROSCI.2906-04.2005

M3 - Article

C2 - 15647470

AN - SCOPUS:12144249953

VL - 25

SP - 271

EP - 280

JO - Journal of Neuroscience

JF - Journal of Neuroscience

SN - 0270-6474

IS - 2

ER -