The eye is necessary for a circadian rhythm in the suprachiasmatic nucleus

Lee, Han S.; Nelms, Jennifer L.; Nguyen, Mary M.N.; Silver, Rae; Lehman, Michael N.

doi:10.1038/nn1006

Cited by 128 publications

(127 citation statements)

References 14 publications

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“…This was confirmed quantitatively: in split hamsters, the area of antiphase pERK expression was ϳ45,000 m 2 , much larger than the ϳ23,000 m 2 in the controls. c-FOS, pERK, and PER1 were all rhythmic, but they were not simultaneously expressed, consistent with previous reports (Chambille et al, 1993;Guido et al, 1999;Field et al, 2000;Lee et al, 2003a). At 3 h after activity onset, c-FOS was high on the side contralateral to high PER1, whereas at 9 h after activity onset, it was high on the same side as PER1 for both core-and shell-like areas.…”

Section: Resultssupporting

confidence: 90%

“…7D). The individual oscillators in the antiphase population with the linear gate-resetting function, however, change over time in contrast to the localized antiphase population of oscillating neurons identified in vivo (Obrietan et al, 1998;King et al, 2003;Lee et al, 2003a). To better conform to physiological data showing a stable population of antiphase oscillators, in the present model we replace the linear gate phaseresetting function with a sigmoid gate phase-resetting function as follows:…”

Section: Mathematical Model Of In-phase and Antiphase Cellsmentioning

confidence: 99%

“…In contrast, the dorsal (shell) SCN contains cells expressing robust circadian rhythmicity in clock genes and clock-controlled genes, although mostly lacking direct retinal input. More surprisingly, a small population of cells exhibit rhythmic phosphorylated extracellular signal-regulated kinase (pERK), which is dependent on the eye and cycles in antiphase to the pERK rhythm in the shell SCN (Lee et al, 2003a). These studies point to an important role for retinal input and photic cues in contributing to SCN function.…”

Section: Introductionmentioning

confidence: 99%

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Two Antiphase Oscillations Occur in Each Suprachiasmatic Nucleus of Behaviorally Split Hamsters

Yan¹,

Foley²,

Bobula³

et al. 2005

J. Neurosci.

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The suprachiasmatic nuclei (SCNs) control circadian rhythms of numerous behavioral and physiological responses. In hamsters, constant light causes "splitting" of circadian rhythms, such that a single daily bout of activity separates into two components, 12 h apart, with antiphase circadian oscillations in the left and right SCN. Given the phenotypic and functional heterogeneity of the SCN, in which ventrolateral but not dorsomedial neurons are retinorecipient, we asked how these two compartments respond to the constant lighting conditions that produce splitting, using three different phase markers of neuronal activity: PER1 (Period 1), c-FOS, and pERK (phosphorylated extracellular signal-regulated kinase). We report the emergence of a coherent novel network in which each side of the SCN exhibits two antiphase oscillating subregions, here termed "core-like" and "shell-like," in addition to the known antiphase oscillation between the right and left SCN. The novel SCN response entails a coherent rhythm in a core-like region of the SCN, which otherwise is not cycling. A mathematical model is presented, and this model interprets the observed changes in the proportion of in-phase and antiphase populations of SCN oscillators and suggests novel testable hypotheses. Finally, the functional significance of this network was explored by investigating the adjacent hypothalamus. Activation of the paraventricular nucleus is in-phase with the ipsilateral core-like SCN, whereas activation of the lateral subparaventricular zone is in-phase with the ipsilateral shell-like SCN, pointing to a multiplicity of SCN output signals. These results suggest a neural basis for internal coincidence of SCN oscillators, and a novel mechanism of plasticity in SCN neural networks and outputs.

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Section: Resultssupporting

confidence: 90%

Section: Mathematical Model Of In-phase and Antiphase Cellsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Two Antiphase Oscillations Occur in Each Suprachiasmatic Nucleus of Behaviorally Split Hamsters

Yan¹,

Foley²,

Bobula³

et al. 2005

J. Neurosci.

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show abstract

“…Further ultra-structural, binding and gene expression studies are needed to determine the potential involvement of the brain in regulating melatonin synthesis through neural pathways such as the retinohypothalamic tract as shown in mammals (Herzog and Tosini, 2001;Lee et al, 2003). If demonstrated, then it would suggest a convergent evolution of this system between species belonging to two distinct and divergent groups of vertebrates (teleosts and mammals).…”

Section: Discussionmentioning

confidence: 99%

Retinal light input is required to sustain plasma melatonin rhythms in Nile tilapia Oreochromis niloticus niloticus

Martinez-Chavez

Migaud

2009

Brain Research

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The aim of this work was to confirm previous findings suggesting that the eyes are required for night-time melatonin production in Nile tilapia and further characterise this divergent circadian organisation. To do so, melatonin levels were firstly measured in eyecups and plasma to determine circadian patterns of melatonin production.Secondly, the effect of partial ophthalmectomy on the suppression of melatonin production was determined in vivo as well as ex vivo pineal light/dark sensitivity.Finally, to investigate whether such findings could be related to post-surgery stress, melatonin analyses were performed in the subsequent 24 h and 7 days postophthalmectomy with cortisol levels assessed as an indicator of stress. Our results showed an inverse pattern of melatonin production in the eye cups of tilapia compared to blood circulating levels, suggesting different roles played by melatonin in these two tissues. Results then demonstrated that total or partial ophthalmectomy resulted in the suppression of night-time melatonin production. Furthermore, although pineals in culture were shown to be photosensitive, night-time melatonin levels were much lower than seen in other species. Finally, when performing sampling immediately or one week post-surgery, no difference in the melatonin profiles were observed. It is therefore unlikely that post-surgery stress would explain such suppression in melatonin production although all fish displayed high cortisol levels most probably due to social and handling stress. Taken together, these results provide further evidence of a new type of circadian organisation in a teleost species where the eyes are required to sustain night time melatonin levels. Section: Regulatory systems

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“…We explore how the cells of the bilateral SCN are organized in space and time, and how unique clock functions are achieved by this organization of SCN cellular elements. The cells that constitute SCN circuits include diverse elements: cell-autonomous oscillators, slave oscillators, and cells that do not appear to oscillate at all (Lee et al 2003;Hastings and Herzog 2004;. Thus, within the SCN, heterogeneous, independently phased cellular oscillators occur in a spatially and temporally ordered pattern, and this underlies the timekeeping function of the nucleus.…”

Section: The Tissue Is the Issuementioning

confidence: 99%

Exploring Spatiotemporal Organization of SCN Circuits

Yan

Karatsoreos

LeSauter

et al. 2007

Cold Spring Harbor Symposia on Quantitative Biology

104

111

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Suprachiasmatic nucleus (SCN) neuroanatomy has been a subject of intense interest since the discovery of the SCN's function as a brain clock and subsequent studies revealing substantial heterogeneity of its component neurons. Understanding the network organization of the SCN has become increasingly relevant in the context of studies showing that its functional circuitry, evident in the spatial and temporal expression of clock genes, can be reorganized by inputs from the internal and external environment. Although multiple mechanisms have been proposed for coupling among SCN neurons, relatively little is known of the precise pattern of SCN circuitry. To explore SCN networks, we examine responses of the SCN to various photic conditions, using in vivo and in vitro studies with associated mathematical modeling to study spatiotemporal changes in SCN activity. We find an orderly and reproducible spatiotemporal pattern of oscillatory gene expression in the SCN, which requires the presence of the ventrolateral core region. Without the SCN core region, behavioral rhythmicity is abolished in vivo, whereas low-amplitude rhythmicity can be detected in SCN slices in vitro, but with loss of normal topographic organization. These studies reveal SCN circuit properties required to signal daily time.

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The eye is necessary for a circadian rhythm in the suprachiasmatic nucleus

Cited by 128 publications

References 14 publications

Two Antiphase Oscillations Occur in Each Suprachiasmatic Nucleus of Behaviorally Split Hamsters

Two Antiphase Oscillations Occur in Each Suprachiasmatic Nucleus of Behaviorally Split Hamsters

Retinal light input is required to sustain plasma melatonin rhythms in Nile tilapia Oreochromis niloticus niloticus

Exploring Spatiotemporal Organization of SCN Circuits

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