Regulation of vasoactive intestinal polypeptide release in the suprachiasmatic nucleus circadian clock

Francl, Jessica M.; Kaur, Gagandeep; Glass, John D.

doi:10.1097/wnr.0b013e32833fcba4

Cited by 42 publications

(39 citation statements)

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“…Daily oscillations in the expression of the transcript encoding VIP, as well as in VIP protein expression and VIP release in the SCN, have been reported (Okamoto et al, 1991; Shinohara et al, 1993; Francl et al, 2010). Indeed, it has been shown that the peak expression of both VIP mRNA and protein occurs during the subjective night (Okamoto et al, 1991; Shinohara et al, 1993; Ban et al, 1997).…”

Section: Discussionmentioning

confidence: 99%

“…Indeed, it has been shown that the peak expression of both VIP mRNA and protein occurs during the subjective night (Okamoto et al, 1991; Shinohara et al, 1993; Ban et al, 1997). VIP release, however, increases during the day (Francl et al, 2010), likely reflecting the daytime increase in the repetitive firing in VIP neurons. Interestingly, bath application of VIP alters the membrane and firing properties of SCN neurons for hours (Kudo et al, 2013), which may result in continued VIP release.…”

Section: Discussionmentioning

confidence: 99%

“…Located primarily in the ventral-lateral region of the SCN, VIP neurons receive direct retinal input and project to other neurons throughout the SCN (Romijn et al, 1997; An et al, 2012). These neurons release VIP in response to light in vivo and in a circadian pattern in vitro (Shinohara et al, 1995; Shinohara et al, 1998; Francl et al, 2010). VIP mRNA and protein levels in the SCN have also been shown to vary with time of day depending on age and ambient lighting conditions (Okamoto et al, 1991; Takeuchi et al, 1992; Shinohara et al, 1993; Fukuhara et al, 1994; Okamura et al, 1995; Ban et al, 1997; Kawakami et al, 1997; Kunst et al, 2015).…”

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Distinct Firing Properties of Vasoactive Intestinal Peptide-Expressing Neurons in the Suprachiasmatic Nucleus

et al. 2015

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The suprachiasmatic nucleus (SCN) regulates daily rhythms in physiology and behavior. Previous studies suggest a critical role for neurons expressing vasoactive intestinal peptide (VIP) in coordinating rhythmicity and synchronization in the SCN. Here we examined the firing properties of VIP-expressing SCN neurons in acute brain slices. Active and passive membrane properties were measured in VIP and in non-VIP neurons during the day and at night. Current-clamp recordings revealed that both VIP and non-VIP neurons were spontaneously active, with higher firing rates during the day than at night. Average firing frequencies, however, were higher in VIP neurons (3.1 ± 0.2 Hz, day and 2.4 ± 0.2 Hz, night) than in non-VIP neurons (1.8 ± 0.2 Hz, day and 0.9 ± 0.2 Hz, night), both day and night. The waveforms of individual action potentials in VIP and non-VIP neurons were also distinct. Action potential durations (APD50) were shorter in VIP neurons (3.6 ± 0.1 ms, day and 2.9 ± 0.1 ms, night) than in non-VIP neurons (4.4 ± 0.3 ms, day and 3.5 ± 0.2 ms, night) throughout the light-dark cycle. In addition, after hyper polarization (AHP) amplitudes were larger in VIP neurons (21 ± 0.8 mV, day and 24.9 ± 0.9 mV, night) than in non-VIP neurons (17.2 ± 1.1 mV, day and 20.5 ± 1.2 mV, night) during the day and at night. Furthermore, significant day/night differences were observed in APD50 and AHP amplitudes in both VIP and non-VIP SCN neurons, consistent with rhythmic changes in ionic conductances that contribute to shaping the firing properties of both cell types. The higher day and night firing rates of VIP neurons likely contribute to synchronizing electrical activity in the SCN.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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Distinct Firing Properties of Vasoactive Intestinal Peptide-Expressing Neurons in the Suprachiasmatic Nucleus

et al. 2015

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“…The degree of desynchronization is dose dependent in that VIP synchronizes at lower concentrations (21) and desynchronizes at higher concentrations. Although absolute concentrations of VIP in the SCN are unknown, VIP release is circadian and at low levels in the SCN based on in vitro and in vivo measures and, in vivo, increases as a function of light intensity (6,(37)(38)(39)(40)(41).…”

Section: Discussionmentioning

confidence: 99%

A neuropeptide speeds circadian entrainment by reducing intercellular synchrony

Harang

Meeker

et al. 2013

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

112

117

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Shift work or transmeridian travel can desynchronize the body's circadian rhythms from local light-dark cycles. The mammalian suprachiasmatic nucleus (SCN) generates and entrains daily rhythms in physiology and behavior. Paradoxically, we found that vasoactive intestinal polypeptide (VIP), a neuropeptide implicated in synchrony among SCN cells, can also desynchronize them. The degree and duration of desynchronization among SCN neurons depended on both the phase and the dose of VIP. A model of the SCN consisting of coupled stochastic cells predicted both the phase-and the dosedependent response to VIP and that the transient phase desynchronization, or "phase tumbling", could arise from intrinsic, stochastic noise in small populations of key molecules (notably, Period mRNA near its daily minimum). The model also predicted that phase tumbling following brief VIP treatment would accelerate entrainment to shifted environmental cycles. We tested this using a prepulse of VIP during the day before a shift in either a light cycle in vivo or a temperature cycle in vitro. Although VIP during the day does not shift circadian rhythms, the VIP pretreatment approximately halved the time required for mice to reentrain to an 8-h shifted light schedule and for SCN cultures to reentrain to a 10-h shifted temperature cycle. We conclude that VIP below 100 nM synchronizes SCN cells and above 100 nM reduces synchrony in the SCN. We show that exploiting these mechanisms that transiently reduce cellular synchrony before a large shift in the schedule of daily environmental cues has the potential to reduce jet lag.circadian oscillator | biological clock | vasopressin | vasoactive intestinal peptide | period gene C ircadian rhythms of living organisms entrain (synchronize) to daily environmental cues such as light and dark. Living organisms have not evolved to make large daily adjustments in their circadian timing, so it is a challenge for them to respond to changes such as those that humans are subjected to during shift work and travel across time zones. Long-term misalignment between internal circadian rhythms in mammals and environmental cycles can induce physiological and psychological abnormalities, including depression, cancer, heart problems, obesity, and increased mortality (1, 2).The master circadian pacemaker in mammals, the bilateral suprachiasmatic nucleus (SCN), is composed of ∼20,000 neurons that synchronize their daily rhythms to each other and entrain to ambient light cycles (3, 4). Vasoactive intestinal polypeptide (VIP), released in the SCN as a function of circadian time and light intensity (5-7), plays a critical role in this circadian synchronization. In the absence of VIP or its receptor, VPAC2R, SCN neurons fail to synchronize to each other and consequently many daily rhythms of the organism are lost (8-12). The addition of VIP to SCN cultures induces the production of Period (Per) 1 and 2 (13), two genes implicated in light-induced resetting (14-16), and shifts rhythms in behavior and SCN physiology (17-21). Notably...

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“…In particular, VIP is involved in photic signaling (An, et al 2013; Colwell et al 2003; Dragich, et al 2010; Hughes, et al 2004; Kuhlman et al 2003; Lucassen, et al 2012; Shen, et al 2000), and light influences VIP expression in the SCN (Duncan et al 1995; Francl, et al 2010; Isobe and Nishino 1998; Shinohara and Inouye 1995; Smith and Canal 2009). Deficits in VIP signaling cause abnormal responses to light, with one result being an unusual responsiveness to light during the day.…”

Section: Scn Coupling Mechanismsmentioning

confidence: 99%

Collective timekeeping among cells of the master circadian clock

Evans

2016

Journal of Endocrinology

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The suprachiasmatic nucleus (SCN) of the anterior hypothalamus is the master circadian clock that coordinates daily rhythms in behavior and physiology in mammals. Like other hypothalamic nuclei, the SCN displays an impressive array of distinct cell types characterized by differences in neurotransmitter and neuropeptide expression. Individual SCN neurons and glia are able to display self-sustained circadian rhythms in cellular function that are regulated at the molecular level by a 24 h transcriptional-translational feedback loop. Remarkably, SCN cells are able to harmonize with one another to sustain coherent rhythms at the tissue level. Mechanisms of cellular communication in the SCN network are not completely understood, but recent progress has provided insight into the functional roles of several SCN signaling factors. This review discusses SCN organization, how intercellular communication is critical for maintaining network function, and the signaling mechanisms that play a role in this process. Despite recent progress, our understanding of SCN circuitry and coupling is far from complete. Further work is needed to map the circuitry of the SCN fully and define the signaling mechanisms that allow for collective timekeeping in the SCN network.

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Regulation of vasoactive intestinal polypeptide release in the suprachiasmatic nucleus circadian clock

Cited by 42 publications

References 24 publications

Distinct Firing Properties of Vasoactive Intestinal Peptide-Expressing Neurons in the Suprachiasmatic Nucleus

Distinct Firing Properties of Vasoactive Intestinal Peptide-Expressing Neurons in the Suprachiasmatic Nucleus

A neuropeptide speeds circadian entrainment by reducing intercellular synchrony

Collective timekeeping among cells of the master circadian clock

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