Modulation of Purkinje cell response to glutamate during the sleep–waking cycle

André, Paolo; Arrighi, Pieranna

doi:10.1016/s0306-4522(01)00208-1

Cited by 17 publications

(7 citation statements)

References 45 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…(C)]. Although various forms of state‐dependent cerebellar activity have been reported in adult rats, cats, and monkeys (Mano, ; Hobson and McCarley, ; Andre and Arrighi, ), this is the first demonstration of state‐dependent activity in the newborn cerebellum.…”

Section: Resultsmentioning

confidence: 77%

REM sleep twitches rouse nascent cerebellar circuits: Implications for sensorimotor development

Sokoloff

Uitermarkt

Blumberg

2014

Developmental Neurobiology

View full text Add to dashboard Cite

The cerebellum is critical for sensorimotor integration and undergoes extensive postnatal development. During the first postnatal week in rats, climbing fibers polyinnervate Purkinje cells and, before granule cell migration, mossy fibers make transient, direct connections with Purkinje cells. Activity-dependent processes are assumed to play a critical role in the development and refinement of these and other aspects of cerebellar circuitry. However, the sources and patterning of activity have not been described. We hypothesize that sensory feedback (i.e., reafference) from myoclonic twitches in sleeping newborn rats is a prominent driver of activity for the developing cerebellum. Here, in 6-day-old rats, we show that Purkinje cells exhibit substantial state-dependent changes in complex and simple spike activity—primarily during active sleep. In addition, this activity increases significantly during bouts of twitching. Moreover, the surprising observation of twitch-dependent increases in simple spike activity at this age suggests a functional engagement of mossy fibers before the parallel fiber system has developed. Based on these and other results, we propose that twitching comprises a unique class of self-produced movement that drives critical aspects of activity-dependent development in the cerebellum and other sensorimotor systems.

show abstract

Section: Resultsmentioning

confidence: 77%

REM sleep twitches rouse nascent cerebellar circuits: Implications for sensorimotor development

Sokoloff

Uitermarkt

Blumberg

2014

Developmental Neurobiology

View full text Add to dashboard Cite

show abstract

“…Serotonin was initially thought to be a true neuromodulator of sleep because the destruction of 5-HT neurons of the raphe system or the inhibition of 5-HT synthesis with p-chloro-phenylalanine induced severe insomnia that could be reversed by restoring 5-HT synthesis [2]. More recent experiments suggest that the release of 5-HT during the sleep-wakefulness cycle initiates a cascade of genomic events in some hypnogenic neurons located in the preoptic area and the neighboring suprachiasmatic nucleus including vasoactive intestinal polypeptide and GABAergic mechanism [1,3,9,15,28,35].…”

Section: Introductionmentioning

confidence: 99%

Valerian extract and valerenic acid are partial agonists of the 5-HT5a receptor in vitro

Dietz

Mahady

Pauli

et al. 2005

Molecular Brain Research

126

View full text Add to dashboard Cite

Insomnia is the most frequently encountered sleep complaint worldwide. While many prescription drugs are used to treat insomnia, extracts of valerian (Valeriana officinalis L., Valerianaceae) are also used for the treatment of insomnia and restlessness. To determine novel mechanisms of action, radioligand binding studies were performed with valerian extracts (100% methanol, 50% methanol, dichloromethane [DCM], and petroleum ether [PE]) at the melatonin, glutamate, and GABA A receptors, and 8 serotonin receptor subtypes. Both DCM and PE extracts had strong binding affinity to the 5-HT 5a receptor, but only weak binding affinity to the 5-HT 2b and the serotonin transporter. Subsequent binding studies focused on the 5-HT 5a receptor due to the distribution of this receptor in the suprachiasmatic nucleus of the brain, which is implicated in the sleep-wake cycle. The PE extract inhibited [ 3 H]lysergic acid diethylamide (LSD) binding to the human 5-HT 5a receptor (86% at 50 μg/ml) and the DCM extract inhibited LSD binding by 51%. Generation of an IC 50 curve for the PE extract produced a biphasic curve, thus GTP shift experiments were also performed. In the absence of GTP, the competition curve was biphasic (two affinity sites) with an IC 50 of 15.7 ng/ml for the high-affinity state and 27.7 μg/ml for the lowaffinity state. The addition of GTP (100 AM) resulted in a right-hand shift of the binding curve with an IC 50 of 11.4 μg/ml. Valerenic acid, the active constituent of both extracts, had an IC 50 of 17.2 AM. These results indicate that valerian and valerenic acid are new partial agonists of the 5-HT 5a receptor.

show abstract

“…Both their simple spike activity, which is driven by the excitatory inputs from parallel fiber synapses, and their complex spike activity, which reflects the excitatory input from a single climbing fiber, are lower during non-rapid eye movement (NREM) sleep than during wake or REM sleep ( Mano, 1970 ; Marchesi and Strata, 1971 ; Hobson and McCarley, 1972 ; Harlay et al, 1974 ; Canto et al, 2017 ). The response of Purkinje cells to microiontophoretically applied glutamate is also smaller in NREM sleep than in wake ( Andre and Arrighi, 2001 ). This effect is not accounted for by changes in spontaneous firing rate but may be associated with the decreased level of acetylcholine and noradrenaline in NREM sleep, which is observed across the brain, including in the cerebellum ( Andre and Arrighi, 2001 ).…”

Section: Discussionmentioning

confidence: 99%

“…The response of Purkinje cells to microiontophoretically applied glutamate is also smaller in NREM sleep than in wake ( Andre and Arrighi, 2001 ). This effect is not accounted for by changes in spontaneous firing rate but may be associated with the decreased level of acetylcholine and noradrenaline in NREM sleep, which is observed across the brain, including in the cerebellum ( Andre and Arrighi, 2001 ). However, whether the sleep-wake cycle is also accompanied by changes in the number or strength of synaptic connections was completely unknown.…”

Section: Discussionmentioning

confidence: 99%

Ultrastructural effects of sleep and wake on the parallel fiber synapses of the cerebellum

Loschky

Spano

Marshall

et al. 2022

eLife

View full text Add to dashboard Cite

Multiple evidence in rodents shows that the strength of excitatory synapses in the cerebral cortex and hippocampus is greater after wake than after sleep. The widespread synaptic weakening afforded by sleep is believed to keep the cost of synaptic activity under control, promote memory consolidation, and prevent synaptic saturation, thus preserving the brain’s ability to learn day after day. The cerebellum is highly plastic and the Purkinje cells, the sole output neurons of the cerebellar cortex, are endowed with a staggering number of excitatory parallel fiber synapses. However, whether these synapses are affected by sleep and wake is unknown. Here, we used serial block face scanning electron microscopy to obtain the full 3D reconstruction of more than 7000 spines and their parallel fiber synapses in the mouse posterior vermis. This analysis was done in mice whose cortical and hippocampal synapses were previously measured, revealing that average synaptic size was lower after sleep compared to wake with no major changes in synapse number. Here, instead, we find that while the average size of parallel fiber synapses does not change, the number of branched synapses is reduced in half after sleep compared to after wake, corresponding to ~16% of all spines after wake and ~8% after sleep. Branched synapses are harbored by two or more spines sharing the same neck and, as also shown here, are almost always contacted by different parallel fibers. These findings suggest that during wake, coincidences of firing over parallel fibers may translate into the formation of synapses converging on the same branched spine, which may be especially effective in driving Purkinje cells to fire. By contrast, sleep may promote the off-line pruning of branched synapses that were formed due to spurious coincidences.

show abstract

Modulation of Purkinje cell response to glutamate during the sleep–waking cycle

Cited by 17 publications

References 45 publications

REM sleep twitches rouse nascent cerebellar circuits: Implications for sensorimotor development

REM sleep twitches rouse nascent cerebellar circuits: Implications for sensorimotor development

Valerian extract and valerenic acid are partial agonists of the 5-HT5a receptor in vitro

Ultrastructural effects of sleep and wake on the parallel fiber synapses of the cerebellum

Contact Info

Product

Resources

About