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.
Similar content being viewed by others
Abbreviations
- AMe:
-
Accessory medulla
- APs:
-
Action potentials
- DD:
-
Constant darkness
- PDF:
-
Pigment-dispersing factor
- ZT:
-
Zeitgebertime
References
Bhumbra GS, Inyushkin N, Saeb-Parsy K, Hon A, Dyball RE (2005) Rhythmic changes in spike coding in the rat suprachiasmatic nucleus. J Physiol 563:291–307
Bloch G, Solomon SM, Robinson GE, Fahrbach SE (2003) Patterns of PERIOD and pigment-dispersing hormone immunoreactivity in the brain of the European honeybee Apis mellifera: age- and time-related plasticity. J Comp Neurol 464:269–284
Colwell CS, Page TL (1990) A circadian rhythm in neural activity can be recorded from the central nervous system of the cockroach. J Comp Physiol A 166:643–649
Dietl H, Prast H, Philippu A (1992) Pulsatile release of catecholamines in the hopothalamus of conscious rats. Naunyn Schmiedbergs Arch Pharmacol 347:28–33
Ding JM, Chen D, Weber ET, Faiman LE, Rea MA, Gillette MU (1994) Resetting the biological clock: mediation of nocturnal circadian shifts by glutamate and NO. Science 266:1713–1717
Grass K, Prast H, Philippu A (1996) Influence of mediobasal hypothalamic lesion and catecholamine receptor antagonists on ultradian rhythm of EEG in the posterior hypothalamus of the rat. Neurosci Lett 207:93–96
Helfrich-Förster C (1995) The period clock gene is expressed in central nervous system neurons which also produce a neuropeptide that reveals the projections of circadian pacemaker cells within the brain of Drosophila melanogaster. Proc Natl Acad Sci USA 92:612–616
Helfrich-Förster C, Homberg U (1993) Pigment-dispersing hormone-immunoreactive neurons in the nervous system of wild-type Drosophila melanogaster and of several mutants with altered circadian rhythmicity. J Comp Neurol 337:177–190
Homberg U, Würden S, Dircksen H, Rao KR (1991) Comparative anatomy of pigment-dispersing hormone-immunoreactive neurons in the brain of orthopteroid insects. Cell Tissue Res 266:343–357
Homberg U, Reischig T, Stengl M (2003) Neural organization of the circadian system of the cockroach Leucophaea maderae. Chronobiol Int 20:577–591
Inouye ST, Kawamura H (1982) Characteristics of a circadian pacemaker in the suprachiasmatic nucleus. J Comp Physiol 146:153–160
Klevecz RR, Pilliod J, Bolen J (1991) Autogenous formation of spiral waves by coupled chaotic attractors. Chronobiol Int 8:6–13
Loesel R, Homberg U (2001) Anatomy and physiology of neurons with processes in the accessory medulla of the cockroach Leucophaea maderae. J Comp Neurol 439:193–207
McCay J, Romero K, Gibson J, Newton J, Wilson L, Wright J, Dahl DB, Ferrell BR (1996) Circadian rhythm in brain gamma aminobutyric acid levels in the cockroach, Leucophaea maderae. J Exp Zool 276:262–269
Meijer JH, Schaap J, Watanabe K, Albus H (1997) Multiunit activity recordings in the suprachiasmatic nuclei: in vivo versus in vitro models. Brain Res 753:322–327
Meyer-Spasche A, Reed HE, Piggins HD (2002) Neurotensin phase-shifts the firing rate rhythm of neurons in the rat suprachiasmatic nuclei in vitro. Eur J Neurosci 16:339–344
Petri B, Stengl M (1997) Pigment-dispersing hormone shifts the phase of the circadian pacemaker of the cockroach Leucophaea maderae. J Neurosci 17:4087–4093
Petri B, Stengl M (1999) Presumptive insect circadian pacemakers in vitro: immunocytochemical characterization of cultured pigment-dispersing hormone-immunoreactive neurons of Leucophaea maderae. Cell Tissue Res 296:635–643
Petri B, Stengl M (2001) Phase response curves of a model oscillator: implications for mutual coupling of paired oscillators. J Biol Rhythms 16:125–141
Petri B, Stengl M, Würden S, Homberg U (1995) Immunocytochemical characterization of the accessory medulla in the cockroach Leucophaea maderae. Cell Tissue Res 282:3–19
Petri B, Homberg U, Loesel R, Stengl M (2002) Evidence for a role of GABA and Mas-allatotropin in photic entrainment of the circadian clock of the cockroach Leucophaea maderae. J Exp Biol 205:1459–1469
Prast H, Dietl H, Philippu A (1992) Pulsatile release of histamine in the hypothalamus of conscious rats. J Auton Nerv Syst 39:105–110
Reischig T, Stengl M (1996) Morphology and pigment-dispersing hormone immunocytochemistry of the accessory medulla, the presumptive circadian pacemaker of the cockroach Leucophaea maderae: a light and electron microscopic study. Cell Tissue Res 285:306–319
Reischig T, Stengl M (2003a) Ectopic transplantation of the accessory medulla restores circadian locomotor rhythms in arrhythmic cockroaches (Leucophaea maderae). J Exp Biol 206:1877–1886
Reischig T, Stengl M (2003b) Ultrastructure of pigment-dispersing hormone-immunoreactive neurons in a three-dimensional model of the accessory medulla of the cockroach Leucophaea maderae. Cell Tissue Res 314:421–435
Reischig T, Stengl M (2004) Pigment-dispersing hormone (PDH)-immunoreactive neurons form a direct coupling pathway between the bilaterally symmetric circadian pacemakers of the cockroach Leucophaea maderae. Cell Tissue Res 318:553–564
Sato S, Chuman Y, Matsushima A, Tominaga Y, Shimohigashi Y, Shimohigashi M (2002) A circadian neuropeptide, pigment-dispersing factor-PDF, in the last-summer cicada Meimuna opalifera: cDNA cloning and immunocytochemistry. Zool Sci 19:821–828
Schaap J, Pennartz CM, Meijer JH (2003) Electrophysiology of the circadian pacemaker in mammals. Chronobiol Int 20:171–188
Schneider NL, Stengl M (2005) Pigment-dispersing factor and GABA synchronize cells of the isolated circadian clock of the cockroach Leucophaea maderae. J Neurosci 25:5138–5147
Schneider NL, Stengl M (2006) Gap junctions between accessory medulla neurons appear to synchronize circadian clock cells of the cockroach Leucophaea maderae. J Neurophysiol 95(3):1996–2002
Sehadová H, Sauman I, Sehnal F (2003) Immunocytochemical distribution of pigment-dispersing hormone in the cephalic ganglia of polyneopteran insects. Cell Tissue Res 312:113–125
Stengl M, Homberg U (1994) Pigment-dispersing hormone-immunoreactive neurons in the cockroach Leucophaea maderae share properties with circadian pacemaker neurons. J Comp Physiol A 175:203–213
Tomioka K, Chiba Y (1992) Characterization of an optic lobe pacemaker by in situ and in vitro recording of neural activity in the cricket, Gryllus bimaculatus. J Comp Physiol A 171:1–7
Yamazaki S, Kerbeshian MC, Hocker CG, Block GD, Menaker M (1998) Rhythmic properties of the hamster suprachiasmatic nucleus in vivo. J Neurosci 18:10709–10723
Závodská R, Sauman I, Sehnal F (2003) Distribution of PER protein, pigment-dispersing hormone, prothoracicotropic hormone, and eclosion hormone in the cephalic nervous system of insects. J Biol Rhythms 18:106–122
Acknowledgments
We thank Dr. Jan Dolzer (Axon Instruments, Burlingame) for his help with establishing the recording technique and Dr. Thomas Reischig (University of Marburg and Göttingen) who introduced us to the isolation of accessory medullae. Additionally, we thank Dr. Thomas Schanze and Keram Pfeiffer (University of Marburg) for helpful discussions of analysis methods.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Schneider, NL., Stengl, M. Extracellular long-term recordings of the isolated accessory medulla, the circadian pacemaker center of the cockroach Leucophaea maderae, reveal ultradian and hint circadian rhythms. J Comp Physiol A 193, 35–42 (2007). https://doi.org/10.1007/s00359-006-0169-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00359-006-0169-7