Candidates for photic entrainment pathways to the circadian clock via optic lobe neuropils in the Madeira cockroach

Arnold, Thordis; Korek, Sebastian; Massah, Azar; Eschstruth, David; Stengl, Monika

doi:10.1002/cne.24844

Cited by 8 publications

(25 citation statements)

References 82 publications

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“…A small set of branches from the DNs innervates the calyces of the mushroom bodies [81] (Figure 5B). The group of LK neurons associated with the medulla [27] has been described in more detail as part of the accessory medulla complex that is a pacemaker region of the circadian clock [91][92][93]. Some of these LK neurons colocalize pigment-dispersing factor (PDF), which is one of the major neuromodulators of the clock in L. maderae and Drosophila [91,93,94].…”

Section: Lk Expression Is In Diverse Types Of Neurons In the Cockroach L Maderae (R Maderae)mentioning

confidence: 99%

Leucokinins: Multifunctional Neuropeptides and Hormones in Insects and Other Invertebrates

Nässel

2021

IJMS

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Leucokinins (LKs) constitute a neuropeptide family first discovered in a cockroach and later identified in numerous insects and several other invertebrates. The LK receptors are only distantly related to other known receptors. Among insects, there are many examples of species where genes encoding LKs and their receptors are absent. Furthermore, genomics has revealed that LK signaling is lacking in several of the invertebrate phyla and in vertebrates. In insects, the number and complexity of LK-expressing neurons vary, from the simple pattern in the Drosophila larva where the entire CNS has 20 neurons of 3 main types, to cockroaches with about 250 neurons of many different types. Common to all studied insects is the presence or 1–3 pairs of LK-expressing neurosecretory cells in each abdominal neuromere of the ventral nerve cord, that, at least in some insects, regulate secretion in Malpighian tubules. This review summarizes the diverse functional roles of LK signaling in insects, as well as other arthropods and mollusks. These functions include regulation of ion and water homeostasis, feeding, sleep–metabolism interactions, state-dependent memory formation, as well as modulation of gustatory sensitivity and nociception. Other functions are implied by the neuronal distribution of LK, but remain to be investigated.

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Section: Lk Expression Is In Diverse Types Of Neurons In the Cockroach L Maderae (R Maderae)mentioning

confidence: 99%

Leucokinins: Multifunctional Neuropeptides and Hormones in Insects and Other Invertebrates

Nässel

2021

IJMS

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“…The glomeruli of the cockroach AME are densely innervated by GABA-immunoreactive (GABA-ir) processes of the distal tract that connects the AME to distal layers of the medulla where long photoreceptor neurons of the compound eye terminate (Giese et al, 2018a). Thus, it was suggested that the distal tract relays indirect light input as photic entrainment pathway into the circadian clock (Arnold et al, 2020;Petri et al, 2002;Reischig & Stengl, 1996).…”

Section: Introductionmentioning

confidence: 99%

“…Furthermore, GABA-ir neurons belong to different soma groups associated with the AME that innervate glomeruli as well as interglomerular regions of the AME (Arnold et al, 2020;Giese et al, 2018a, b).…”

Section: Introductionmentioning

confidence: 99%

Distribution and daily oscillation of GABA in the circadian system of the cockroach Rhyparobia maderae

Massah

Neupert

Brodesser

et al. 2021

J of Comparative Neurology

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Gamma-aminobutyric acid (GABA) is the prevalent inhibitory neurotransmitter in nervous systems promoting sleep in both mammals and insects. In the Madeira cockroach, sleep-wake cycles are controlled by a circadian clock network in the brain's optic lobes, centered in the accessory medulla (AME) with its innervating pigment-dispersing factor (PDF) expressing clock neurons at the anterior-ventral rim of the medulla. GABA is present in cell clusters that innervate different circuits of the cockroach's AME clock, without colocalizing in PDF clock neurons. Physiological, immunohistochemical, and behavioral assays provided evidence for a role of GABA in light entrainment, possibly via the distal tract that connects the AME's glomeruli to the medulla. Furthermore, GABA was implemented in clock outputs to multiple effector systems in optic lobe and midbrain. Here, GABAergic brain circuits were analyzed further, focusing on the circadian system in search for sleep/wake controlling brain circuits. All GABAimmunoreactive neurons of the cockroach brain were also stained with an antiserum against the GABA-synthesizing enzyme glutamic acid decarboxylase. We found strong overlap of the distribution of GABA-immunoreactive networks with PDF clock networks in optic lobes and midbrain. Neurons in five of the six soma groups that innervate the clock exhibited GABA immunoreactivity. The intensity of GABA immunoreactivity in the distal tract showed daily fluctuations with maximum staining intensity in the middle of the day and weakest staining at the end of the day. Quantification via enzyme-linked immunosorbent assay and quantitative liquid chromatography coupled to electrospray ionization tandem mass spectrometry, likewise, showed higher GABA levels in the optic lobe during the inactivity phase of the cockroach during the day and lower levels during its activity phase at dusk. Our data further support the hypothesis that light-and PDF-dependently the circadian clock network of the cockroach controls GABA levels and thereby promotes sleep during the day.

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“…In addition, contralaterally projecting clock neurons such as contralateral aPDFMEs are clock outputs connecting the clock to locomotor control centers [ 12 , 46 – 48 , 39 , 49 – 52 ]. Thus, it was suggested that contralaterally projecting aPDFMEs control locomotor activity rhythms, while ipsilaterally remaining aPDFMEs control sleep/rest in the Madeira cockroach [ 53 , 54 ].…”

Section: Discussionmentioning

confidence: 99%

Neither per, nor tim1, nor cry2 alone are essential components of the molecular circadian clockwork in the Madeira cockroach

et al. 2020

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Circadian clocks control rhythms in physiology and behavior entrained to 24 h light-dark cycles. Despite of conserved general schemes, molecular circadian clockworks differ between insect species. With RNA interference (RNA i) we examined an ancient circadian clockwork in a basic insect, the hemimetabolous Madeira cockroach Rhyparobia maderae. With injections of double-stranded RNA (dsRNA) of cockroach period (Rm´per), timeless 1 (Rm´tim1), or cryptochrome 2 (Rm´cry2) we searched for essential components of the clocḱ s core negative feedback loop. Single injections of dsRNA of each clock gene into adult cockroaches successfully and permanently knocked down respective mRNA levels withiñ two weeks deleting daytime-dependent mRNA rhythms for Rm´per and Rm´cry2. Rḿ per RNAi or Rm´cry2 RNAi affected total mRNA levels of both genes, while Rm´tim1 transcription was independent of both, also keeping rhythmic expression. Unexpectedly, circadian locomotor activity of most cockroaches remained rhythmic for each clock gene knockdown employed. It expressed weakened rhythms and unchanged periods for Rm´per RNAi and shorter periods for Rm´tim1 RNAi and Rm´cry2 RNAi .As a hypothesis of the cockroach´s molecular clockwork, a basic network of switched differential equations was developed to model the oscillatory behavior of clock cells expressing respective clock genes. Data were consistent with two synchronized main groups of coupled oscillator cells, a leading (morning) oscillator, or a lagging (evening) oscillator that couple via mutual inhibition. The morning oscillators express shorter, the evening oscillators longer endogenous periods based on core feedback loops with either PER, TIM1, or CRY2/PER complexes as dominant negative feedback of the clockwork. We hypothesize that dominant morning oscillator cells with shorter periods express PER, but not CRY2, or TIM1 as suppressor of clock gene expression, while two groups of evening oscillator cells with longer periods either comprise TIM1 or CRY2/PER suppressing complexes. Modelling suggests that there is an additional negative feedback next to Rm´PER in cockroach morning oscillator cells.

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Candidates for photic entrainment pathways to the circadian clock via optic lobe neuropils in the Madeira cockroach

Cited by 8 publications

References 82 publications

Leucokinins: Multifunctional Neuropeptides and Hormones in Insects and Other Invertebrates

Leucokinins: Multifunctional Neuropeptides and Hormones in Insects and Other Invertebrates

Distribution and daily oscillation of GABA in the circadian system of the cockroach Rhyparobia maderae

Neither per, nor tim1, nor cry2 alone are essential components of the molecular circadian clockwork in the Madeira cockroach

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