Lateralization of Circadian Pacemaker Output: Activation of Left- and Right-Sided Luteinizing Hormone-Releasing Hormone Neurons Involves a Neural Rather Than a Humoral Pathway

Iglesia, Horacio O. de la; Meyer, Jennifer L.; Schwartz, William J.

doi:10.1523/jneurosci.23-19-07412.2003

Cited by 113 publications

(72 citation statements)

References 15 publications

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“…This finding suggests that the SCN splits before behavioral splitting and agrees with a previous report by de la Iglesia et al (2003).…”

Section: Resultssupporting

confidence: 93%

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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“…This finding suggests that the SCN splits before behavioral splitting and agrees with a previous report by de la Iglesia et al (2003).…”

Section: Resultssupporting

confidence: 93%

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

Yan¹,

Foley²,

Bobula³

et al. 2005

J. Neurosci.

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“…Circadian control of gonadotropin secretion. Syrian hamsters normally exhibit one consolidated bout of activity every 24 h. Under conditions of constant light, the hamsters activity splits into two components separated by about 12 h. In one ingenious study (de la Iglesia et al, 2003), the investigators killed animals prior to each of the activity bouts (see asterisk on activity records). Brains were analyzed for FOS activity in the SCN and in neurons of the GnRH neuronal system.…”

Section: Discussionmentioning

confidence: 99%

“…In ovariectomized, estrogen-implanted split hamsters killed during one of their activity bouts, however, activation of the SCN occurs on one side of the brain (monitored by FOS expression) but not on the other, suggesting that each half of the SCN can control an activity bout (de la Iglesia et al, 2000). Remarkably, FOS activation in GnRH neurons was only seen on the side of the brain in which SCN FOS expression occurred (de la Iglesia et al, 2003). These findings suggest that the precise timing of the LH surge is derived from a neural signal originating in the SCN and communicated to ipsilateral GnRH neurons, as a diffusible output signal would reach both sides of the brain.…”

Section: Neural Control Of Neurosecretory Factorsmentioning

confidence: 97%

The regulation of neuroendocrine function: Timing is everything

Kriegsfeld

Silver

2006

Hormones and Behavior

131

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Hormone secretion is highly organized temporally, achieving optimal biological functioning and health. The master clock located in the suprachiasmatic nucleus (SCN) of the hypothalamus coordinates the timing of circadian rhythms, including daily control of hormone secretion. In the brain, the SCN drives hormone secretion. In some instances, SCN neurons make direct synaptic connections with neurosecretory neurons. In other instances, SCN signals set the phase of "clock genes" that regulate circadian function at the cellular level within neurosecretory cells. The protein products of these clock genes can also exert direct transcriptional control over neuroendocrine releasing factors. Clock genes and proteins are also expressed in peripheral endocrine organs providing additional modes of temporal control. Finally, the SCN signals endocrine glands via the autonomic nervous system, allowing for rapid regulation via multisynaptic pathways. Thus, the circadian system achieves temporal regulation of endocrine function by a combination of genetic, cellular, and neural regulatory mechanisms to ensure that each response occurs in its correct temporal niche. The availability of tools to assess the phase of molecular/cellular clocks and of powerful tract tracing methods to assess connections between "clock cells" and their targets provides an opportunity to examine circadian-controlled aspects of neurosecretion, in the search for general principles by which the endocrine system is organized. KeywordsCircadian; Diurnal; Endocrinel; Neurosecretion; Clock genes; Suprachiasmatic Circadian aspects of reproductionThe importance of circadian (about a day) timing in hormone production/secretion has been known since the 1950s when Everett and Sawyer determined that a stimulatory signal occurring during a narrow temporal window on the afternoon of proestrus is necessary for induction of ovulation later that night (Everett and Sawyer, 1950). Such close temporal organization is important for successful reproduction, as numerous hormone-dependent behavioral and physiological processes must be coordinated. If optimal temporal relationships are disrupted, pronounced deficits in fertility can result. For example, ovulation, behavioral estrus, fertilization, and pregnancy maintenance require a specific

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“…To begin to explore the role of neural connections as well as to exclude the role of activity, we assessed the expression of PER2 immunoreactivity separately in the left and right BNST-OV in behaviorally rhythmic rats bearing a unilateral SCN lesion. Neural connections between the SCN and some of its targets are lateralized (de la Iglesia et al, 2003). Accordingly, we hypothesized that if the rhythm in expression of PER2 in the BNST-OV depends on neural connections from the SCN, then the rhythm in expression of PER2 in the BNST-OV ipsilateral to the lesion would be attenuated and different from that in the contralateral side.…”

Section: Per2 Oscillation In the Left And Right Bnst-ov After Unilatementioning

confidence: 99%

A Circadian Rhythm in the Expression of PERIOD2 Protein Reveals a Novel SCN-Controlled Oscillator in the Oval Nucleus of the Bed Nucleus of the Stria Terminalis

Amir

Lamont²,

Robinson³

et al. 2004

J. Neurosci.

146

166

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Lateralization of Circadian Pacemaker Output: Activation of Left- and Right-Sided Luteinizing Hormone-Releasing Hormone Neurons Involves a Neural Rather Than a Humoral Pathway

Cited by 113 publications

References 15 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

The regulation of neuroendocrine function: Timing is everything

A Circadian Rhythm in the Expression of PERIOD2 Protein Reveals a Novel SCN-Controlled Oscillator in the Oval Nucleus of the Bed Nucleus of the Stria Terminalis

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