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

Abstract

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.

Circadian pacemaker neurons of the Madeira cockroach are inhibited and activated by GABAA and GABAB receptors

“…Furthermore, the GABAergic interneurons between AME and the other optic lobe neuropils were assumed to control the gain of clock in‐ and outputs serving homeostatic plasticity. In addition, GABA‐ and PDF‐dependent synchronisation was shown to generate ensembles of AME neurons that fire synchronously in the gamma‐frequency range indicative of information processing in the mammalian cortex (Schneider & Stengl, , , ). These neuropeptide‐ and GABA‐dependent ensembles were hypothesised to gate inputs to‐ and outputs of the clock (reviews: Stengl et al., ; Stengl & Arendt, ).…”

Examination of the role of FMRFamide-related peptides in the circadian clock of the cockroach Leucophaea maderae

“…Thus, some FaRPs possibly located in DFVNes might relay light-dependent phase-delays during the early night from the contralateral eye. Schneider and Stengl (2007) have postulated that peaks of changes in the electrical activity of AMe neurons occurring at the early day, the late day/early night and the middle of the night are correlated with a vast amount of peptide release. Interestingly, the activity peak distribution of AMe neurons correlates well with the maxima of phase responses obtained after the injections of PDF (CT 9), GABA CT 19), and serotonin (CT 7-13).…”

Circadian regulation of membrane physiology in neural oscillators throughout the brain

“…Taken together, these results suggest that the electrical activity rhythms of the optic lobe are a critical component of the insect circadian clock. More recent work has shown specifically that the accessory medulla of the optic lobe is critical for nocturnal behavior such that electrical recordings from this region show rapid increases in electrical activity more frequently at night (Schneider & Stengl, ). Neurophysiological activity of clock neurons in these invertebrates is inhibited or excited by GABA (see Giese, Wei, & Stengl, in this Special Issue) similar to results reported in vertebrate clocks, where GABA is involved in entrainment and synchronization (Albers, Walton, Gamble, McNeill, & Hummer, ).…”