Correlation with Behavioral Activity and Rest Implies Circadian Regulation by SCN Neuronal Activity Levels

Houben, Thijs; Deboer, Tom; Oosterhout, Floor van; Meijer, Johanna H.

doi:10.1177/0748730409349895

Cited by 56 publications

(55 citation statements)

References 51 publications

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“…Methylphenidate treatment also altered SCN electrical activity, producing a delayed trough, increased amplitude, and reduced variability. Changes in the SCN MUA rhythm, specifically the downward slope and trough, have been previously shown to correlate with behavioral activity (Houben et al, 2009), a pattern observed in the present study. All parameters of the SCN waveform taken together (trough, peak, rising, and downward slope) were also shifted, suggesting a delay in the SCN electrical activity rhythm.…”

Section: Discussionsupporting

confidence: 70%

“…Animals in the behavioral part of the study were individually housed in cages equipped with running wheels (n ¼ 24), with passive infrared motion sensors (PIRs, n ¼ 12), or with both (n ¼ 9). Animals in the electrophysiology and sleep part of the study were individually housed in standard mouse cages before recording, and were transferred to large recording chambers (Deboer et al, 2007b;Houben et al, 2009). Animals started the experiment under a 12 h : 12 h lightdark cycle, with ad libitum access to food and drink throughout the experiment.…”

Section: Animals and Housingmentioning

confidence: 99%

“…Animals were placed in custom-designed recording chambers and were connected to a recording system with a counterbalanced swivel allowing the animals to freely move during the recording, as described previously (Houben et al, 2009). The electrical activity was amplified and bandwidth filtered (0.5-5 kHz).…”

Section: In-vivo Electrophysiologymentioning

confidence: 99%

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Methylphenidate Modifies the Motion of the Circadian Clock

Antle

Diepen

Deboer

et al. 2012

Neuropsychopharmacol

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People with attention-deficit/hyperactivity disorder (ADHD) often experience sleep problems, and these are frequently exacerbated by the methylphenidate they take to manage their ADHD symptoms. Many of the changes to sleep are consistent with a change in the underlying circadian clock. The present study was designed to determine if methylphenidate alone could alter properties of the circadian clock. Young male mice were examined in light-dark cycles and in constant darkness and recordings were performed on behavioral activity, sleep, and electrical activity in the suprachiasmatic nucleus (SCN) of freely moving mice. Methylphenidate in the drinking water (0.08%) significantly increased activity in the mid-to-late night, and led to a delay in the onset of activity and sleep relative to the light-dark cycle. While locomotor levels returned to baseline after treatment ended, the phase angle of entrainment required at least a week to return to baseline levels. In constant darkness, the free-running period of both wheel-running and general locomotor rhythms was lengthened by methylphenidate. When the treatment ended, the free-running period either remained stable or only partially reverted to baseline levels. Methylphenidate also altered the electrical firing rate rhythms in the SCN. It induced a delay in the trough of the rhythm, an increment in rhythm amplitude, and a reduction in rhythm variability. These observations suggest that methylphenidate alters the underlying circadian clock. The observed changes are consistent with clock alterations that would promote sleep-onset insomnia.

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Section: Discussionsupporting

confidence: 70%

Section: Animals and Housingmentioning

confidence: 99%

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Methylphenidate Modifies the Motion of the Circadian Clock

Antle

Diepen

Deboer

et al. 2012

Neuropsychopharmacol

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“…P hysiology and behavior of all mammals is organized in an alternating pattern of rest and activity cycles, whereby the endogenous and light-induced daily neuronal activity of the suprachiasmatic nucleus (SCN) signals rest in nocturnal rodents and activity in diurnal primates, such as humans (1,2). Restricting food access to a short and predictable episode during the rest phase changes this behavioral pattern, such that an animal becomes active and for up to several hours anticipates the upcoming feeding event.…”

mentioning

confidence: 99%

Interaction between hypothalamic dorsomedial nucleus and the suprachiasmatic nucleus determines intensity of food anticipatory behavior

Acosta-Galvan

Vliet

et al. 2011

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

160

131

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Food anticipatory behavior (FAA) is induced by limiting access to food for a few hours daily. Animals anticipate this scheduled meal event even without the suprachiasmatic nucleus (SCN), the biological clock. Consequently, a food-entrained oscillator has been proposed to be responsible for meal time estimation. Recent studies suggested the dorsomedial hypothalamus (DMH) as the site for this food-entrained oscillator, which has led to considerable controversy in the literature. Herein we demonstrate by means of c-Fos immunohistochemistry that the neuronal activity of the suprachiasmatic nucleus (SCN), which signals the rest phase in nocturnal animals, is reduced when animals anticipate the scheduled food and, simultaneously, neuronal activity within the DMH increases. Using retrograde tracing and confocal analysis, we show that inhibition of SCN neuronal activity is the consequence of activation of GABA-containing neurons in the DMH that project to the SCN. Next, we show that DMH lesions result in a loss or diminution of FAA, simultaneous with increased activity in the SCN. A subsequent lesion of the SCN restored FAA. We conclude that in intact animals, FAA may only occur when the DMH inhibits the activity of the SCN, thus permitting locomotor activity. As a result, FAA originates from a neuronal network comprising an interaction between the DMH and SCN. Moreover, this study shows that the DMH-SCN interaction may serve as an intrahypothalamic system to gate activity instead of rest overriding circadian predetermined temporal patterns. P hysiology and behavior of all mammals is organized in an alternating pattern of rest and activity cycles, whereby the endogenous and light-induced daily neuronal activity of the suprachiasmatic nucleus (SCN) signals rest in nocturnal rodents and activity in diurnal primates, such as humans (1, 2). Restricting food access to a short and predictable episode during the rest phase changes this behavioral pattern, such that an animal becomes active and for up to several hours anticipates the upcoming feeding event. This food anticipatory activity (FAA) is even exhibited without the known circadian oscillator, the SCN (3), and thus may rely on a different circadian pacemaker.In search of the location of this so-called "food entrained oscillator" (FEO), two recent studies have claimed that its position is within the dorsomedial nucleus of the hypothalamus (DMH) (4, 5). The designation of the DMH as master clock for food entrainment is, however, controversial because some groups reported unimpaired FAA despite large lesions of the DMH (6, 7); others have shown that lesions of the DMH disturb and diminish the intensity of FAA (6). The possible participation of other brain structures in FAA is evident from studies that demonstrate modulation of neuronal activity and induction of clock-gene rhythmicity in hypothalamic and limbic structures by feeding schedules (8-11). Thus, it has been suggested that FAA depends on a multioscillatory system comprised of a complex and redundant neuronal netwo...

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“…Recent experimental results demonstrate that circadian modulation of behavioural activity is reliably predicted by the circadian variation of SCN electrical activity [1]. In both nocturnal and diurnal animals, the overall firing rate of SCN neurons varies over 24 h, with a generally higher firing rate during the light period and a generally lower firing rate during the dark period [2][3][4], though some subpopulations show different firing profiles [5][6][7].…”

Section: Introductionmentioning

confidence: 99%

Circadian regulation of sleep–wake behaviour in nocturnal rats requires multiple signals from suprachiasmatic nucleus

Fleshner

Booth

Forger

et al. 2011

Phil. Trans. R. Soc. A.

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The dynamics of sleep and wake are strongly linked to the circadian clock. Many models have accurately predicted behaviour resulting from dynamic interactions between these two systems without specifying physiological substrates for these interactions. By contrast, recent experimental work has identified much of the relevant physiology for circadian and sleep-wake regulation, but interaction dynamics are difficult to study experimentally. To bridge these approaches, we developed a neuronal population model for the dynamic, bidirectional, neurotransmitter-mediated interactions of the sleepwake and circadian regulatory systems in nocturnal rats. This model proposes that the central circadian pacemaker, located within the suprachiasmatic nucleus (SCN) of the hypothalamus, promotes sleep through single neurotransmitter-mediated signalling to sleep-wake regulatory populations. Feedback projections from these populations to the SCN alter SCN firing patterns and fine-tune this modulation. Although this model reproduced circadian variation in sleep-wake dynamics in nocturnal rats, it failed to describe the sleep-wake dynamics observed in SCN-lesioned rats. We thus propose two alternative, physiologically based models in which neurotransmitter-and neuropeptidemediated signalling from the SCN to sleep-wake populations introduces mechanisms to account for the behaviour of both the intact and SCN-lesioned rat. These models generate testable predictions and offer a new framework for modelling sleep-wake and circadian interactions.

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Correlation with Behavioral Activity and Rest Implies Circadian Regulation by SCN Neuronal Activity Levels

Cited by 56 publications

References 51 publications

Methylphenidate Modifies the Motion of the Circadian Clock

Methylphenidate Modifies the Motion of the Circadian Clock

Interaction between hypothalamic dorsomedial nucleus and the suprachiasmatic nucleus determines intensity of food anticipatory behavior

Circadian regulation of sleep–wake behaviour in nocturnal rats requires multiple signals from suprachiasmatic nucleus

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