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Circadian pacemaker coupling by multi-peptidergic neurons in the cockroach Leucophaea maderae.

Soehler S, Stengl M, Reischig T - Cell Tissue Res. (2011)

Bottom Line: Although two-thirds of all PDF-expressing medulla neurons coexpressed FMRFamide and orcokinin immunoreactivity in their somata, colocalization of PDF and FMRFamide immunoreactivity was observed in only a few termination sites.Colocalization of PDF and orcokinin immunoreactivity was never observed in any of the terminals or optic commissures.We suggest that circadian pacemaker cells employ axonal peptide sorting to phase-control physiological processes at specific times of the day.

View Article: PubMed Central - PubMed

Affiliation: Department of Natural Sciences, Animal Physiology, University of Kassel, Heinrich-Plett-Strasse 40, 34132 Kassel, Germany.

ABSTRACT
Lesion and transplantation studies in the cockroach, Leucophaea maderae, have located its bilaterally symmetric circadian pacemakers necessary for driving circadian locomotor activity rhythms to the accessory medulla of the optic lobes. The accessory medulla comprises a network of peptidergic neurons, including pigment-dispersing factor (PDF)-expressing presumptive circadian pacemaker cells. At least three of the PDF-expressing neurons directly connect the two accessory medullae, apparently as a circadian coupling pathway. Here, the PDF-expressing circadian coupling pathways were examined for peptide colocalization by tracer experiments and double-label immunohistochemistry with antisera against PDF, FMRFamide, and Asn(13)-orcokinin. A fourth group of contralaterally projecting medulla neurons was identified, additional to the three known groups. Group one of the contralaterally projecting medulla neurons contained up to four PDF-expressing cells. Of these, three medium-sized PDF-immunoreactive neurons coexpressed FMRFamide and Asn(13)-orcokinin immunoreactivity. However, the contralaterally projecting largest PDF neuron showed no further peptide colocalization, as was also the case for the other large PDF-expressing medulla cells, allowing the easy identification of this cell group. Although two-thirds of all PDF-expressing medulla neurons coexpressed FMRFamide and orcokinin immunoreactivity in their somata, colocalization of PDF and FMRFamide immunoreactivity was observed in only a few termination sites. Colocalization of PDF and orcokinin immunoreactivity was never observed in any of the terminals or optic commissures. We suggest that circadian pacemaker cells employ axonal peptide sorting to phase-control physiological processes at specific times of the day.

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a Horizontal reconstruction of the PDF-expressing neuron system of the cockroach Leucophaea maderae in the supraesophageal ganglion (AMe accessory medulla, aPDFMe anterior group of PDF-expressing neurons, AOC anterior optic commissure, dPDFLa dorsal group of PDF-expressing lamina neurons, La lamina, Me medulla, pPDFMe posterior group of PDF-expressing medulla neurons, POC posterior optic commissure, POTu posterior optic tubercle). Bar 500 μm. b Representation of the neuron groups of the accessory medulla (AMe) including the PDF-expressing medulla neurons (PDFMe, colored) as derived from morphological and immunohistological analyses (DFVNe distal group of frontoventral neurons, MFVNe medial group of frontoventral neurons, MNe medial neurons, VNe ventral neurons, VMNe ventromedial neurons, VPNe ventroposterior neurons). Although the numbers of gray circles do not reflect the actual group sizes, the numbers of colored circles represent the rounded mean numbers of the respective PDFMe neurons according to previous work. Large (purple, plus one largest) and medium-sized (dark blue) PDFMe belong to the VNe, whereas small PDFMe (light blue) appear to belong to the DFVNe neurons. Previous work has suggested that two large and one medium-sized PDFMe together with one unspecified VNe (C) project to the contralateral AMe to provide a mutual pacemaker coupling input. The unspecified VNe is suggested to express either an FMRFamide-related peptide or orcokinin (di distal, do dorsal)
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Fig1: a Horizontal reconstruction of the PDF-expressing neuron system of the cockroach Leucophaea maderae in the supraesophageal ganglion (AMe accessory medulla, aPDFMe anterior group of PDF-expressing neurons, AOC anterior optic commissure, dPDFLa dorsal group of PDF-expressing lamina neurons, La lamina, Me medulla, pPDFMe posterior group of PDF-expressing medulla neurons, POC posterior optic commissure, POTu posterior optic tubercle). Bar 500 μm. b Representation of the neuron groups of the accessory medulla (AMe) including the PDF-expressing medulla neurons (PDFMe, colored) as derived from morphological and immunohistological analyses (DFVNe distal group of frontoventral neurons, MFVNe medial group of frontoventral neurons, MNe medial neurons, VNe ventral neurons, VMNe ventromedial neurons, VPNe ventroposterior neurons). Although the numbers of gray circles do not reflect the actual group sizes, the numbers of colored circles represent the rounded mean numbers of the respective PDFMe neurons according to previous work. Large (purple, plus one largest) and medium-sized (dark blue) PDFMe belong to the VNe, whereas small PDFMe (light blue) appear to belong to the DFVNe neurons. Previous work has suggested that two large and one medium-sized PDFMe together with one unspecified VNe (C) project to the contralateral AMe to provide a mutual pacemaker coupling input. The unspecified VNe is suggested to express either an FMRFamide-related peptide or orcokinin (di distal, do dorsal)

Mentions: Much research on the structural, functional, and molecular properties of endogenous circadian clocks has been performed in a variety of insect species. Whereas the first circadian pacemaker center controlling behavioral activity patterns was located to the optic lobes of the cockroach Leucophaea maderae, the cellular nature of the clock remained elusive (Nishiitsutsuji-Uwo and Pittendrigh 1968; Roberts 1974; Sokolove 1975; Page 1982). Subsequent lesion and transplantation studies have identified the accessory medulla (AMe, plural AMae; Ehnbom 1948) at the anterior ventromedial border of the medulla as this circadian clock (Stengl and Homberg 1994; Reischig and Stengl 2003a; for a review, see Homberg et al. 2003). The AMe is formed by a set of about 250 associated neurons, most of which can be classified into several groups according to their morphological and immunohistochemical characteristics (Reischig and Stengl 2003b; see also Materials and methods). Among these is a distinct set of about a dozen pigment-dispersing factor (PDF)-expressing medulla neurons (PDFMe, Fig. 1a, b). In Drosophila melanogaster, homologous PDF-expressing neurons (the ventral group of the lateral neurons, LNvs) have been shown to be circadian pacemakers indispensable for maintaining circadian locomotor rhythms under constant conditions (for a review, see Helfrich-Förster 2005). In cockroaches and other insects, the homologous PDFMe are circadian pacemaker cells that control locomotor activity rhythms (Stengl and Homberg 1994; Singaravel et al. 2003; Reischig and Stengl 2003a; Wen and Lee 2008). Furthermore, the neuropeptide PDF as a clock output factor is indispensable for circadian locomotor rhythms as pdf RNAi experiments have demonstrated in the German cockroach Blatella germanica (Lee et al. 2009).Fig. 1


Circadian pacemaker coupling by multi-peptidergic neurons in the cockroach Leucophaea maderae.

Soehler S, Stengl M, Reischig T - Cell Tissue Res. (2011)

a Horizontal reconstruction of the PDF-expressing neuron system of the cockroach Leucophaea maderae in the supraesophageal ganglion (AMe accessory medulla, aPDFMe anterior group of PDF-expressing neurons, AOC anterior optic commissure, dPDFLa dorsal group of PDF-expressing lamina neurons, La lamina, Me medulla, pPDFMe posterior group of PDF-expressing medulla neurons, POC posterior optic commissure, POTu posterior optic tubercle). Bar 500 μm. b Representation of the neuron groups of the accessory medulla (AMe) including the PDF-expressing medulla neurons (PDFMe, colored) as derived from morphological and immunohistological analyses (DFVNe distal group of frontoventral neurons, MFVNe medial group of frontoventral neurons, MNe medial neurons, VNe ventral neurons, VMNe ventromedial neurons, VPNe ventroposterior neurons). Although the numbers of gray circles do not reflect the actual group sizes, the numbers of colored circles represent the rounded mean numbers of the respective PDFMe neurons according to previous work. Large (purple, plus one largest) and medium-sized (dark blue) PDFMe belong to the VNe, whereas small PDFMe (light blue) appear to belong to the DFVNe neurons. Previous work has suggested that two large and one medium-sized PDFMe together with one unspecified VNe (C) project to the contralateral AMe to provide a mutual pacemaker coupling input. The unspecified VNe is suggested to express either an FMRFamide-related peptide or orcokinin (di distal, do dorsal)
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Related In: Results  -  Collection

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Fig1: a Horizontal reconstruction of the PDF-expressing neuron system of the cockroach Leucophaea maderae in the supraesophageal ganglion (AMe accessory medulla, aPDFMe anterior group of PDF-expressing neurons, AOC anterior optic commissure, dPDFLa dorsal group of PDF-expressing lamina neurons, La lamina, Me medulla, pPDFMe posterior group of PDF-expressing medulla neurons, POC posterior optic commissure, POTu posterior optic tubercle). Bar 500 μm. b Representation of the neuron groups of the accessory medulla (AMe) including the PDF-expressing medulla neurons (PDFMe, colored) as derived from morphological and immunohistological analyses (DFVNe distal group of frontoventral neurons, MFVNe medial group of frontoventral neurons, MNe medial neurons, VNe ventral neurons, VMNe ventromedial neurons, VPNe ventroposterior neurons). Although the numbers of gray circles do not reflect the actual group sizes, the numbers of colored circles represent the rounded mean numbers of the respective PDFMe neurons according to previous work. Large (purple, plus one largest) and medium-sized (dark blue) PDFMe belong to the VNe, whereas small PDFMe (light blue) appear to belong to the DFVNe neurons. Previous work has suggested that two large and one medium-sized PDFMe together with one unspecified VNe (C) project to the contralateral AMe to provide a mutual pacemaker coupling input. The unspecified VNe is suggested to express either an FMRFamide-related peptide or orcokinin (di distal, do dorsal)
Mentions: Much research on the structural, functional, and molecular properties of endogenous circadian clocks has been performed in a variety of insect species. Whereas the first circadian pacemaker center controlling behavioral activity patterns was located to the optic lobes of the cockroach Leucophaea maderae, the cellular nature of the clock remained elusive (Nishiitsutsuji-Uwo and Pittendrigh 1968; Roberts 1974; Sokolove 1975; Page 1982). Subsequent lesion and transplantation studies have identified the accessory medulla (AMe, plural AMae; Ehnbom 1948) at the anterior ventromedial border of the medulla as this circadian clock (Stengl and Homberg 1994; Reischig and Stengl 2003a; for a review, see Homberg et al. 2003). The AMe is formed by a set of about 250 associated neurons, most of which can be classified into several groups according to their morphological and immunohistochemical characteristics (Reischig and Stengl 2003b; see also Materials and methods). Among these is a distinct set of about a dozen pigment-dispersing factor (PDF)-expressing medulla neurons (PDFMe, Fig. 1a, b). In Drosophila melanogaster, homologous PDF-expressing neurons (the ventral group of the lateral neurons, LNvs) have been shown to be circadian pacemakers indispensable for maintaining circadian locomotor rhythms under constant conditions (for a review, see Helfrich-Förster 2005). In cockroaches and other insects, the homologous PDFMe are circadian pacemaker cells that control locomotor activity rhythms (Stengl and Homberg 1994; Singaravel et al. 2003; Reischig and Stengl 2003a; Wen and Lee 2008). Furthermore, the neuropeptide PDF as a clock output factor is indispensable for circadian locomotor rhythms as pdf RNAi experiments have demonstrated in the German cockroach Blatella germanica (Lee et al. 2009).Fig. 1

Bottom Line: Although two-thirds of all PDF-expressing medulla neurons coexpressed FMRFamide and orcokinin immunoreactivity in their somata, colocalization of PDF and FMRFamide immunoreactivity was observed in only a few termination sites.Colocalization of PDF and orcokinin immunoreactivity was never observed in any of the terminals or optic commissures.We suggest that circadian pacemaker cells employ axonal peptide sorting to phase-control physiological processes at specific times of the day.

View Article: PubMed Central - PubMed

Affiliation: Department of Natural Sciences, Animal Physiology, University of Kassel, Heinrich-Plett-Strasse 40, 34132 Kassel, Germany.

ABSTRACT
Lesion and transplantation studies in the cockroach, Leucophaea maderae, have located its bilaterally symmetric circadian pacemakers necessary for driving circadian locomotor activity rhythms to the accessory medulla of the optic lobes. The accessory medulla comprises a network of peptidergic neurons, including pigment-dispersing factor (PDF)-expressing presumptive circadian pacemaker cells. At least three of the PDF-expressing neurons directly connect the two accessory medullae, apparently as a circadian coupling pathway. Here, the PDF-expressing circadian coupling pathways were examined for peptide colocalization by tracer experiments and double-label immunohistochemistry with antisera against PDF, FMRFamide, and Asn(13)-orcokinin. A fourth group of contralaterally projecting medulla neurons was identified, additional to the three known groups. Group one of the contralaterally projecting medulla neurons contained up to four PDF-expressing cells. Of these, three medium-sized PDF-immunoreactive neurons coexpressed FMRFamide and Asn(13)-orcokinin immunoreactivity. However, the contralaterally projecting largest PDF neuron showed no further peptide colocalization, as was also the case for the other large PDF-expressing medulla cells, allowing the easy identification of this cell group. Although two-thirds of all PDF-expressing medulla neurons coexpressed FMRFamide and orcokinin immunoreactivity in their somata, colocalization of PDF and FMRFamide immunoreactivity was observed in only a few termination sites. Colocalization of PDF and orcokinin immunoreactivity was never observed in any of the terminals or optic commissures. We suggest that circadian pacemaker cells employ axonal peptide sorting to phase-control physiological processes at specific times of the day.

Show MeSH
Related in: MedlinePlus