Circadian rhythm in brain gamma aminobutyric acid levels in the cockroach,Leucophaea maderae

McCay, J. A.; Romero, Kristoffer; Gibson, Jay R.; Newton, Janette; Wilson, Lori; Wright, J. L.; Dahl, Dominik; Ferrell, Blaine R.

doi:10.1002/(sici)1097-010x(19961101)276:4<262::aid-jez3>3.0.co;2-m

Cited by 3 publications

(4 citation statements)

References 25 publications

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“…The spatial overlap of GABA immunostaining with PDF-ir terminals in several brain areas, such as the superior lateral, superior medial, and ventrolateral protocerebrum, suggests that GABAergic neuropils in various brain areas are under circadian control, possibly being postsynaptic to PDF neurons. As already reported for the whole brain (McCay et al, 1996), our measurements in the optic lobes, likewise, indicate that GABA levels are under control of the circadian clock and express a circadian rhythm with maximum abundance during the day, when the nocturnal cockroaches rest.…”

Section: Role Of Gaba In the Circadian Timekeeping System Of R Maderaesupporting

confidence: 88%

“…Furthermore, employing sensitive quantitative mass spectrometry (Figure 13) of optic lobes hinted at a slightly higher GABA titer in the optic lobes detected from individual brains (n = 3; n = 6 measurements) at ZT 06 (4.50 µmol l −1 /2 optic lobes) as compared to ZT 12 (4.24 µmol l −1 /2 optic lobes, Kruskal-Wallis test, p = .127). Thus, while there is more variability during light dark cycles, GABA levels show circadian regulation in optic lobes of the Madeira cockroach, confirming previous measurement in whole brains (McCay et al, 1996).…”

Section: 5supporting

confidence: 87%

“…Daily and circadian variation in GABA levels in the optic lobe McCay et al (1996) reported daily and circadian fluctuations of GABA levels in the brain of the Madeira cockroach with highest levels occurring at midday. To investigate possible changes of GABA levels in neu-F I G U R E 1 1 Box plots illustrating relative intensity of GABA staining in the distal tract at zeitgeber times (ZT) 00, ZT 06, ZT 12, and ZT 18 in LD 12:12 with ZT 00-ZT 12 light phase and ZT 12-ZT 00 dark phase.…”

Section: 5mentioning

confidence: 99%

“…Furthermore, GABA was proposed to be involved in clock-dependent gating mechanisms, possibly regulating sleep-wake cycles via postsynaptic neuropils in the central brain (Giese et al, 2018a, b;Schneider & Stengl, 2005). Accordingly, circadian changes in GABA levels in the whole cockroach brain were found (McCay et al, 1996).…”

Section: Introductionmentioning

confidence: 99%

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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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Section: Role Of Gaba In the Circadian Timekeeping System Of R Maderaesupporting

confidence: 88%

Section: 5supporting

confidence: 87%

Section: 5mentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

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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Extracellular long-term recordings of the isolated accessory medulla, the circadian pacemaker center of the cockroach Leucophaea maderae, reveal ultradian and hint circadian rhythms

Schneider

Stengl

2006

J Comp Physiol A

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In the cockroach Leucophaea maderae transplantation studies located the circadian pacemaker center, which controls locomotor activity rhythms, to the accessory medulla (AMe), ventromedially to the medulla of the brain's optic lobes. The AMe is densely innervated via GABA- and manyfold peptide-immunoreactive neurons. They express ultradian action potential oscillations in the gamma frequency range and form phase-locked assemblies of synchronously spiking cells. Peptide application resulted in transient rises of extracellularly recorded activity. It remained unknown whether transient rises in spontaneous electrical activity as a possible indication of peptide release occur in the isolated circadian clock in a rhythmic manner. In extracellular glass electrode recordings of the isolated AMe in constant darkness, which lasted at least 12 h, the distribution of daytime-dependent changes in activity independently of the absolute action potential frequency was examined. Rapid, transient changes in activity preferentially occurred at the mid-subjective night, with a minimum at the middle of the subjective day, hinting the presence of circadian rhythms in the isolated circadian clock. Additionally, ultradian rhythms in activity change that are multiples of a fundamental 2 h period were observed. We hypothesize that circadian rhythms might originate from coupled ultradian oscillations, possibly already at the single cell level.

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The sublethal effects of endosulfan on the circadian rhythms and locomotor activity of two sympatric parasitoid species

2015

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Circadian rhythm in brain gamma aminobutyric acid levels in the cockroach,Leucophaea maderae

Cited by 3 publications

References 25 publications

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

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

Extracellular long-term recordings of the isolated accessory medulla, the circadian pacemaker center of the cockroach Leucophaea maderae, reveal ultradian and hint circadian rhythms

The sublethal effects of endosulfan on the circadian rhythms and locomotor activity of two sympatric parasitoid species

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