Identification and characterisation of the circadian pacemaker of the cockroach Leucophaea maderae (original) (raw)
Related papers
1997
An antiserum against the crustacean neuropeptide pigmentdispersing hormone stains a small set of neurons in the optic lobes of several hemimetabolous and holometabolous insects. These cells, the primary branches of which in the optic lobe lie in the accessory medulla, fulfill several criteria predicted for neurons of the circadian clock. For example, in fruit flies they express timeless and period, which are two molecular components of the circadian pacemaker.
2003 Neural organization of the circadian system of the cockroach Leucophaea maderae
2020
The cockroach Leucophaea maderae was the first animal in which lesion experiments localized an endogenous circadian clock to a particular brain area, the optic lobe. The neural organization of the circadian system, however, including entrainment pathways, coupling elements of the bilaterally distributed internal clock, and output pathways controlling circadian locomotor rhythms are only recently beginning to be elucidated. As in flies and other insect species, pigment-dispersing hormone (PDH)-immunoreactive neurons of the accessory medulla of the cockroach are crucial elements of the circadian system. Lesions and transplantation experiments showed that the endogeneous circadian clock of the brain resides in neurons associated with the accessory medulla. The accessory medulla is organized into a nodular core receiving photic input, and into internodular and peripheral neuropil involved in efferent output and coupling input. Photic entrainment of the clock through compound eye photore...
Cell and Tissue Research, 1999
The accessory medulla with its associated pigment-dispersing hormone-immunoreactive neurons appears to be the pacemaker that controls the circadian locomotor activity rhythm of the cockroach Leucophaea maderae. To permit studies at the level of individual, identified, pacemaker neurons, we developed specific long-term primary cell cultures of fully differentiated adult neurons of the accessory medulla. As judged from soma diameter distribution, the cultures contain an unbiased representation of apparently all neuronal types of the accessory medulla. The cultured cells survive and grow processes for more than 2 months with or without additional hemocyte coculturing. However, a strong positive effect on initial outgrowth was observed with hemocyte coculturing. At least six different morphological cell types of the accessory medulla could be distinguished in vitro. Among these only one cell type, the monopolar type C cell, was recognized in vitro with an antiserum against the neuropeptide pigment-dispersing hormone. Thus, the identifiable monopolar type C cells are candidates for circadian pacemaker neurons and will be the focus of further physiological characterizations.
The 24-h rhythm of metabolic activity of the cockroach circadian pacemaker
Neuroscience Letters, 1989
In the cockroach, Leucophaea maderae, the optic lobes contain a circadian pacemaker. The metabolic activity of optic lobe neuropils was measured at 17 time points over a 24-h period in constant darkness, using cytochrome oxidase activity as functional marker. The results revealed a clear 24-h energy metabolism rhythm in neuropils and particularly in the lobula plate, a part of the region which is assumed to include a circadian pacemaker in this species.
Neural Organization of the Circadian System of the Cockroach Leucophaea maderae
Chronobiology International, 2003
The cockroach Leucophaea maderae was the first animal in which lesion experiments localized an endogenous circadian clock to a particular brain area, the optic lobe. The neural organization of the circadian system, however, including entrainment pathways, coupling elements of the bilaterally distributed internal clock, and output pathways controlling circadian locomotor rhythms are only recently beginning to be elucidated. As in flies and other insect species, pigment-dispersing hormone (PDH)-immunoreactive neurons of the accessory medulla of the cockroach are crucial elements of the circadian system. Lesions and transplantation experiments showed that the endogeneous circadian clock of the brain resides in neurons associated with the accessory medulla. The accessory medulla is organized into a nodular core receiving photic input, and into internodular and peripheral neuropil involved in efferent output and coupling input. Photic entrainment of the clock through compound eye photoreceptors appears to occur via parallel, indirect pathways through the medulla. Light-like phase shifts in circadian locomotor activity after injections of g-aminobutyric acid (GABA)-or Masallatotropin into the vicinity of the accessory medulla suggest that both substances are involved in photic entrainment. Extraocular, cryptochrome-based photoreceptors appear to be present in the optic lobe, but their role in photic entrainment has not 577 been examined. Pigment-dispersing hormone-immunoreactive neurons provide efferent output from the accessory medulla to several brain areas and to the peripheral visual system. Pigment-dispersing hormone-immunoreactive neurons, and additional heterolateral neurons are, furthermore, involved in bilateral coupling of the two pacemakers. The neuronal organization, as well as the prominent involvement of GABA and neuropeptides, shows striking similarities to the organization of the suprachiasmatic nucleus, the circadian clock of the mammalian brain.
Immunocytochemical characterization of the accessory medulla in the cockroach Leucophaea maderae
Cell and Tissue Research, 1995
Several lines of evidence suggest that pigment-dispersing hormone-immunoreactive neurons with ramifications in the accessory medulla are involved in the circadian system of insects. The present study provides a detailed analysis of the anatomical and neurochemical organization of the accessory medulla in the brain of the cockroach Leucophaea maderae. We show that the accessory medulla is compartmentalized into central dense nodular neuropil surrounded by a shell of coarse fibers. It is innervated by neurons immunoreactive to antisera against serotonin and the neuropeptides allatostatin 7, allatotropin, corazonin, gastrin/cholecystokinin, FMRFamide, leucokinin I, and pigment-dispersing hormone. Some of the immunostained neurons appear to be local neurons of the accessory medulla, whereas others connect this neuropil to various brain areas, including the lamina, the contralateral optic lobe, the posterior optic tubercles, and the superior protocerebrum. Double-label experiments show the colocalization of immunoreactivity against pigment-dispersing hormone with compounds related to FMRFamide, serotonin, and leucokinin I. The neuronal and neurochemical organization of the accessory medulla is consistent with the current hypothesis for a role of this brain area as a circadian pacemaking center in the insect brain.
Journal of Experimental Biology, 2003
The presence of an endogenous circadian clock in the brain of an animal was first demonstrated in the cockroach Leucophaea maderae. However, the clock's cellular basis remained elusive until pigment-dispersing hormone-immunoreactive neurons, which express the clock genes period and timeless in Drosophila, were proposed as pacemaker candidates. In several insect species, pigment-dispersing hormone-immunoreactive neurons are closely associated with the accessory medulla, a small neuropil in the optic lobe, which was suggested to be a circadian clock neuropil. Here, we demonstrate that ectopic transplantation of adult accessory medulla into optic lobe-less cockroaches restores circadian locomotor activity rhythms in L. maderae. All histologically examined cockroaches that regained circadian activity regenerated pigment-dispersing hormone-immunoreactive fibres from the grafts to original targets in the protocerebrum. The data show that the accessory medulla is the circadian pacemaker controlling locomotor activity rhythms in the cockroach. Whether pigment-dispersing hormoneimmunoreactive neurons are the only circadian pacemaker cells controlling locomotor activity rhythms remains to be examined.
The Journal of Experimental Biology, 2002
Accumulating evidence suggests that the accessory medulla is the location of the circadian pacemaker in the fruit fly Drosophila melanogaster and the cockroach Leucophaea maderae. γ-Aminobutyric acid (GABA) and Mas-allatotropin are two putative neurotransmitters in the accessory medulla in the cockroach Leucophaea maderae. Neurons immunoreactive to the neuropeptide Mas-allatotropin are local neurons with arborizations in the noduli of the accessory medulla, while GABAimmunoreactive neurons connect the noduli of the accessory medulla to the medulla and to the lamina via processes in the distal tract. Injections of GABA and Mas-allatotropin into the vicinity of the accessory medulla resulted in stable phase-dependent resetting of the circadian locomotor activity of the cockroach. The resulting phase response curves closely matched lightdependent phase response curves, suggesting that both substances play a role in circuits relaying photic information from circadian photoreceptors to the central pacemaker.
Journal of Experimental Biology, 2002
SUMMARY Accumulating evidence suggests that the accessory medulla is the location of the circadian pacemaker in the fruit fly Drosophila melanogasterand the cockroach Leucophaea maderae. γ-Aminobutyric acid(GABA) and Mas-allatotropin are two putative neurotransmitters, in the accessory medulla in the cockroach Leucophaea maderae. Neurons immunoreactive to the neuropeptide Mas-allatotropin are local neurons with arborizations in the noduli of the accessory medulla, while GABA-immunoreactive neurons connect the noduli of the accessory medulla to the medulla and to the lamina via processes in the distal tract. Injections of GABA and Mas-allatotropin into the vicinity of the accessory medulla resulted in stable phase-dependent resetting of the circadian locomotor activity of the cockroach. The resulting phase response curves closely matched light-dependent phase response curves, suggesting that both substances play a role in circuits relaying photic information from circadian photorecep...
Cell and Tissue Research, 2004
Circadian locomotor activity rhythms of the cockroach Leucophaea maderae are driven by two bilaterally paired and mutually coupled pacemakers that reside in the optic lobes of the brain. Transplantation studies have shown that this circadian pacemaker is located in the accessory medulla (AMe), a small neuropil of the medulla of the optic lobe. The AMe is densely innervated by about 12 anterior pigment-dispersing-hormone-immunoreactive (PDH-ir) medulla (PDHMe) neurons. PDH-ir neurons are circadian pacemaker candidates in the fruitfly and cockroach. A subpopulation of these neurons also appears to connect both optic lobes and may constitute at least one of the circadian coupling pathways. To determine whether PDHMe neurons directly connect both accessory medullae, we injected rhodamine-labeled dextran as neuronal tracer into one AMe and performed PDH immunocytochemistry. Double-labeled fibers in the anterior, shell, and internodular neuropil of the AMe contralaterally to the injection site showed that PDH-ir fibers directly connect both accessory medullae. This connection is formed by three anterior PDHMe neurons of each optic lobe, which, thus, fulfill morphological criteria for a direct circadian coupling pathway. Our double-label studies also showed that all except one of the midbrain projection areas of anterior PDHMe neurons were innervated ipsilaterally and contralaterally. Thus, anterior PDHMe neurons seem to play multiple roles in generating circadian rhythms. They also deliver timing information output and perform mutual pacemaker coupling in L. maderae.