Synchronization of circadian firing rhythms in cultured rat suprachiasmatic neurons

Shirakawa, Tetsuo; Honma, Sato; Katsuno, Yumiko; Oguchi, Haruhisa; Honma, Ken‐ichi

doi:10.1046/j.1460-9568.2000.00170.x

Cited by 116 publications

(106 citation statements)

References 35 publications

(49 reference statements)

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“…Mechanisms for synchronization between SCN neurons may be nonsynaptic (22) or synaptic (14). Nonsynaptic synchronization may involve electrical coupling via gap junctions and ionic mechanisms (22)(23)(24) or paracrine factors such as nitric oxide (25), whereas synaptic coupling may involve ␥-aminobutyric acid (26).…”

Section: Discussionmentioning

confidence: 99%

“…After dissociation, isolated SCN neurons express circadian rhythms in their firing patterns (12,13). The freerunning periods of the individual neurons vary from 20 to 28 h. The average period matches the behavioral activity pattern of Ϸ24 h. In these cultured dispersals, synaptically coupled neurons can sometimes be observed with synchronized firing patterns (14). In SCN tissue explants cultured on multielectrode plates, the variation in free-running period is considerably smaller (15)(16)(17).…”

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confidence: 97%

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Heterogeneity of rhythmic suprachiasmatic nucleus neurons: Implications for circadian waveform and photoperiodic encoding

Schaap

Albus

vanderLeest

et al. 2003

Proc. Natl. Acad. Sci. U.S.A.

188

176

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Circadian rhythms in neuronal ensemble, subpopulations, and single unit activity were recorded in the suprachiasmatic nuclei (SCN) of rat hypothalamic slices. Decomposition of the ensemble pattern revealed that neuronal subpopulations and single units within the SCN show surprisingly short periods of enhanced electrical activity of Ϸ5 h and show maximal activity at different phases of the circadian cycle. The summed activity accounts for the neuronal ensemble pattern of the SCN, indicating that circadian waveform of electrical activity is a composed tissue property. The recorded single unit activity pattern was used to simulate the responsiveness of SCN neurons to different photoperiods. We inferred predictions on changes in peak width, amplitude, and peak time in the multiunit activity pattern and confirmed these predictions with hypothalamic slices from animals that had been kept in a short or long photoperiod. We propose that the animals' ability to code for day length derives from plasticity in the neuronal network of oscillating SCN neurons.T he suprachiasmatic nuclei (SCN) contain a major pacemaker of circadian rhythms in mammals (1, 2). The SCN control circadian rhythms in the central nervous system and peripheral organs and as such ensures that organisms are able to anticipate and adjust to predictable changes in the environment that occur with the day-night cycle (3-5). The SCN is also involved in adaptation of the organism to the annual cycle by monitoring seasonal changes in day length (6). As an example, animals will accommodate their daily behavioral activity to the photoperiod. A multioscillator structure has been proposed to fulfill this dual task (7).At least nine candidate genes have been identified that play a role in rhythm generation on the basis of a transcriptionaltranslational feedback loop (8, 9). A number of additional genes may be involved to further refine or shape circadian rhythms (10). Although great progress has been made in understanding the molecular basis for circadian rhythm generation, it is unknown how individual neuronal activity rhythms are integrated to render a functioning pacemaker that is able to code for circadian and seasonal rhythms. The SCN each contain Ϸ10,000 neurons, which are small and densely packed (11). After dissociation, isolated SCN neurons express circadian rhythms in their firing patterns (12, 13). The freerunning periods of the individual neurons vary from 20 to 28 h. The average period matches the behavioral activity pattern of Ϸ24 h. In these cultured dispersals, synaptically coupled neurons can sometimes be observed with synchronized firing patterns (14). In SCN tissue explants cultured on multielectrode plates, the variation in free-running period is considerably smaller (15)(16)(17). In these explants, firing patterns can be observed which are in phase, or 6 -12 h out of phase. The range of phase relationships observed within the SCN in vitro suggests a level of temporal complexity that challenges our understanding of how a singular phase and perio...

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 97%

Heterogeneity of rhythmic suprachiasmatic nucleus neurons: Implications for circadian waveform and photoperiodic encoding

Schaap

Albus

vanderLeest

et al. 2003

Proc. Natl. Acad. Sci. U.S.A.

188

176

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“…For example, a previous analysis of the role of GABA in SCN neurons in culture found that blocking GABA receptors alters the firing rate and precision of the neural activity rhythms but does not impair synchrony or rhythmicity of the population (Aton et al, 2006). However, previous work has also shown that exogenously applied GABA can phase shift the rhythms in electrical activity (Tominaga et al, 1994;Shirakawa et al, 2000) and can synchronize the population of cellular oscillators in culture (Liu and Reppert, 2000). The GABAergic excitation described in the present study is likely to have a robust impact on how dorsal SCN neurons respond to afferent input.…”

Section: Functional Significance Of Gabaergic Excitationmentioning

confidence: 99%

“…Early work suggested that GABA could evoke excitatory responses during the day (Wagner et al, 1997), but the generality of this finding has been questioned by other laboratories (Gribkoff et al, 1999;De Jeu and Pennartz, 2002). Functionally, the exogenous application of GABA can synchronize the electrical activity of SCN neurons (Liu and Reppert, 2000;Shirakawa et al, 2000); however, GABAergic signaling does not appear to be required for cultured SCN neurons to remain synchronized (Aton et al, 2006). Intriguingly, there is evidence to suggest that GABA-mediated mechanisms are responsible for coupling ventral and dorsal cell populations in the SCN (Albus et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

Excitatory Actions of GABA in the Suprachiasmatic Nucleus

Choi¹,

Lee²,

Schroeder³

et al. 2008

J. Neurosci.

152

221

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Neurons in the suprachiasmatic nucleus (SCN) are responsible for the generation of circadian oscillations, and understanding how these neurons communicate to form a functional circuit is a critical issue. The neurotransmitter GABA and its receptors are widely expressed in the SCN where they mediate cell-to-cell communication. Previous studies have raised the possibility that GABA can function as an excitatory transmitter in adult SCN neurons during the day, but this work is controversial. In the present study, we first tested the hypothesis that GABA can evoke excitatory responses during certain phases of the daily cycle by broadly sampling how SCN neurons respond to GABA using extracellular single-unit recording and gramicidin-perforated-patch recording techniques. We found that, although GABA inhibits most SCN neurons, some level of GABA-mediated excitation was present in both dorsal and ventral regions of the SCN, regardless of the time of day. These GABA-evoked excitatory responses were most common during the night in the dorsal SCN region. The Na ϩ -K ϩ -2Cl Ϫ cotransporter (NKCC) inhibitor, bumetanide, prevented these excitatory responses. In individual neurons, the application of bumetanide was sufficient to change GABA-evoked excitation to inhibition. Calcium-imaging experiments also indicated that GABA-elicited calcium transients in SCN cells are highly dependent on the NKCC isoform 1 (NKCC1). Finally, Western blot analysis indicated that NKCC1 expression in the dorsal SCN is higher in the night. Together, this work indicates that GABA can play an excitatory role in communication between adult SCN neurons and that this excitation is critically dependent on NKCC1.

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“…Ces résultats viennent en appui de données, obtenues in vitro, démontrant que les rythmes de sécrétion d'AVP et de VIP peuvent être découplés [37,38]. Chaque NSC serait donc, hypothétiquement, composé de deux oscillateurs couplés.…”

Section: Combien D'horloges Dans Les Nsc?unclassified