In vivo metabolic activity of the suprachiasmatic nuclei: a comparative study

doi:10.1016/0006-8993(83)90538-3

Brain Research

Volume 274, Issue 1, 5 September 1983, Pages 184-187

https://doi.org/10.1016/0006-8993(83)90538-3 Get rights and content

Abstract

In vivo glucose utilization was measured in the suprachiasmatic nuclei (SCN) of the rat, monkey, and cat using the¹⁴C-labeled deoxyglucose technique. SCN metabolic activity in all species was endogenously rhythmic with high levels during the subjective daylight portion of the 24 h day. Such phase conservation across night-, day-, and randomly-active species is in agreement with formal analyses of the properties of entrainable circadian oscillators, and our data suggest that the biochemical processes which underlie the activity of this circadian clock are similar in mammals with differing patterns of expressed circadian rhythmicity.

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Chronobiology is the study of physiological rhythms, examining the timing of behavior in relation to both daily and seasonal environmental cycles [100]. Circadian rhythms are endogenous biological cycles of 24 h. Biological ‘clocks’ are located in the suprachiasmatic nucleus (SCN) [101], as well as in peripheral tissues [102]. The activity of the SCN peaks during the day and acts as a physiological pacemaker driving the circadian rhythm of the organism [103].
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The Ts65Dn mouse is a well-studied model of trisomy 21, Down syndrome. This mouse strain has severe learning disability as measured by several rodent learning tests that depend on hippocampal spatial memory function. Hippocampal long-term potentiation (LTP) is deficient in these mice. Short-term daily treatment with low-dose GABA receptor antagonists rescue spatial learning and LTP in Ts65Dn mice leading to the hypothesis that the learning disability is due to GABAergic over-inhibition of hippocampal circuits. The fact that the GABA receptor antagonists were only effective if delivered during the daily light phase suggested that the source of the excess GABA was controlled directly or indirectly by the circadian system. The central circadian pacemaker of mammals is the suprachiasmatic nucleus (SCN), which is largely a GABAergic nucleus. In this study we investigated whether elimination of the SCN in Ts65Dn mice would restore their ability to form recognition memories as tested by the novel object recognition (NOR) task. Full, but not partial lesions of the SCN of Ts65Dn mice normalized their ability to perform on the NOR test. These results suggest that the circadian system modulates neuroplasticity over the time frame involved in the process of consolidation of recognition memories.
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Functions such as energy balance and metabolism, sleep, and hot flashes—all regulated by the hypothalamus in a circadian manner—are highly sensitive to age, the estrogenic milieu, and their interactions (Landau and Zucker, 1976; Mauvais-Jarvis et al., 2013; Poehlman et al., 1995; Toth et al., 2000). Within the hypothalamus, the suprachiasmatic nucleus, the master circadian clock (Reppert and Weaver, 2002; Schwartz et al., 1983; Yoo et al., 2005), undergoes age-related dampening in its oscillatory rhythms and output (Davidson et al., 2008; Duncan et al., 2013; Gibson et al., 2009; Krajnak et al., 1998; Mattis and Sehgal, 2016; Oster et al., 2003; Sutin et al., 1993; Whealin et al., 1993; Wise et al., 1988; Wyse and Coogan, 2010; Zhang et al., 1996). The suprachiasmatic nucleus projects to, and receives afferent inputs from, other hypothalamic and nonhypothalamic regions, thereby influencing energy balance (e.g., arcuate nucleus [ARC] [Elias et al., 2000; Wang et al., 2014]), thermoregulation (median preoptic area [Mittelman-Smith et al., 2015]), and other physiological processes.
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Second, the input sensors could be changed such that they affect the molecular clock mechanism in opposite ways, and third, the interpretation of the clock signal could be opposite, which would lead to appropriate regulation of physiological pathways. Deoxyglucose uptake experiments revealed that in the SCN, the rhythm of metabolic activity is similar in both nocturnal and diurnal animals (Schwartz et al., 1983). At the molecular level, the expression of clock genes shows the same phase in diurnal and nocturnal SCN, and their light-dependent synchronization is comparable (Mrosovsky et al., 2001).
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Oxidation-reduction reactions are essential to life as the core mechanisms of energy transfer. A large body of evidence in recent years presents an extensive and complex network of interactions between the circadian and cellular redox systems. Recent advances show that cellular redox state undergoes a ~24-h (circadian) oscillation in most tissues and is conserved across the domains of life. In nucleated cells, the metabolic oscillation is dependent upon the circadian transcription-translation machinery and, vice versa, redox-active proteins and cofactors feed back into the molecular oscillator. In the suprachiasmatic nucleus (SCN), a hypothalamic region of the brain specialized for circadian timekeeping, redox oscillation was found to modulate neuronal membrane excitability. The SCN redox environment is relatively reduced in daytime when neuronal activity is highest and relatively oxidized in nighttime when activity is at its lowest. There is evidence that the redox environment directly modulates SCN K⁺ channels, tightly coupling metabolic rhythms to neuronal activity. Application of reducing or oxidizing agents produces rapid changes in membrane excitability in a time-of-day-dependent manner. We propose that this reciprocal interaction may not be unique to the SCN. In this review, we consider the evidence for circadian redox oscillation and its interdependencies with established circadian timekeeping mechanisms. Furthermore, we will investigate the effects of redox on ion-channel gating dynamics and membrane excitability. The susceptibility of many different ion channels to modulation by changes in the redox environment suggests that circadian redox rhythms may play a role in the regulation of all excitable cells.

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In vivo metabolic activity of the suprachiasmatic nuclei: a comparative study

Abstract

Brain Research

Brain Research

Brain Research

Circadian rhythm of body temperature persists after suprachiasmatic lesions in the squirrel monkey

Amer. J. Physiol.

Circadian rhythms (activity, temperature, urine, and microfilariae) in dog, cat, hen, duck, thamnomys and gerbillus

J. interdiscipl. Cycle Res.

Brain Work

Persistence of circadian rhythmicity in a mammalian hypothalamic ‘island’ containing the suprachiasmatic nucleus

Characteristics of a circadian pacemaker in the suprachiasmatic nucleus

J. comp. Physiol.

Locomotion and activity phasing of some medium-sized mammals

J. Mammalogy

[14C]-2-deoxyglucose uptake in ground squirrel brain during hibernation

J. Neurosci.

Three-dimensional structure of the mammalian suprachiasmatic nuclei: a comparative study of five species

J. comp. Neurol.

Activity-dependent energy metabolism in rat posterior pituitary primarily reflects sodium pump activity

J. Neurochem.

The suprachiasmatic nucleus, circadian rhythms, and regulation of brain peptides

Cortisol-mediated synchronization of circadian rhythm in urinary potassium excretion

Amer. J. Physiol.

[¹⁴C]-2-deoxyglucose uptake in ground squirrel brain during hibernation