The cholinergic system, circadian rhythmicity, and time memory

The cholinergic system, circadian rhythmicity, and time memory

► Rat but not mouse SCN contains cholinergic neurons. ► SCN cholinergic neurotransmission supports time memory formation via time stamping. ► The neurppeptide AVP acts as an SCN output for time stamping. This review provides an overview of the interaction between the mammalian cholinergic system and...

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Published in:Behavioural brain research Vol. 221; no. 2; pp. 466 - 480
Main Authors: Hut, R.A., Van der Zee, E.A.
Format: Journal Article
Language:English
Published: Netherlands Elsevier B.V 10-08-2011
Subjects:
Acetylcholine
Acetylcholine - physiology
Aging
Aging - physiology
Alzheimer Disease - physiopathology
Alzheimer's disease
Animals
Arginine Vasopressin - physiology
Biological rhythms
Brain - physiology
Cholinergic Fibers - physiology
Cholinergic system
Circadian Clocks - physiology
Circadian Rhythm - physiology
Circadian system
Humans
Memory - physiology
Models, Biological
Muscarinic receptor
Nicotinic receptor
Receptors, Muscarinic - physiology
Suprachiasmatic nucleus
Suprachiasmatic Nucleus - physiology
Synaptic Transmission - physiology
Time memory
Time stamping
Circadian system
Suprachiasmatic nucleus
Biological rhythms
Time stamping
Aging
Acetylcholine
Cholinergic system
Time memory
Muscarinic receptor
Nicotinic receptor
Alzheimer's disease
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Abstract ► Rat but not mouse SCN contains cholinergic neurons. ► SCN cholinergic neurotransmission supports time memory formation via time stamping. ► The neurppeptide AVP acts as an SCN output for time stamping. This review provides an overview of the interaction between the mammalian cholinergic system and circadian system, and its possible role in time memory. Several studies made clear that circadian (daily) fluctuations in acetylcholine (ACh) release, cholinergic enzyme activity and cholinergic receptor expression varies remarkably between species and even strains. Apparently, cholinergic features can be flexibly adjusted to the needs of a species or strain. Nevertheless, it can be generalized that circadian rhythmicity in the cholinergic system is characterized by high ACh release during the active phase of an individual. During the active phase, the activity of the ACh synthesizing enzyme Choline Acetyltransferase (ChAT) is enhanced, and the activity of the ACh degrading enzyme Acetylcholinesterase (AChE) is reduced. The number of free, unbound and thus available muscarinic acetylcholine receptors (mAChRs) is highest when ACh release is lowest. The cholinergic innervation of the suprachiasmatic nucleus (SCN), the hypothalamic circadian master clock, arises from the cholinergic forebrain and brain stem nuclei. The density of cholinergic fibers and terminals is modest as compared to other hypothalamic nuclei. This is the case for rat, hamster and mouse, three chronobiological model rodent species studied by us. A new finding is that the rat SCN contains some local cholinergic neurons. Hamster SCN contains less cholinergic neurons, whereas the mouse SCN is devoid of such cells. ACh has an excitatory effect on SCN cells (at least in vivo), and functions in close interaction with other neurotransmitters. Originally it was thought that ACh transferred retinal light information to the SCN. This turned out to be wrong. Thereafter, the phase shifting effects of ACh prompted researches to view ACh as an agent for nocturnal clock resetting. It is still not clear, however, what the function consequence is of SCN cholinergic neurotransmission. Here, we postulate the hypothesis that cholinergic neurotransmission in the SCN provides the brain with a mechanism to support the formation of time memory via ‘time stamping’. We define time memory as the memory of a specific time of the day, for which an animal made an association with a certain event and/or location (for example in case of time-place association). We use the term ‘time stamping’ to refer to the process underlying the encoding of a specific time of day (the time stamp). Only relatively brief but arousing events seem to be time stamped at SCN level. This time stamping requires the engagement of mAChRs. New data suggests that the SCN uses the neuropeptide vasopressin (AVP) as an output system to transfer the specific time of day information to other brain regions such as hippocampus and neocortex where time memory is supposed to be acquired, consolidated and stored. Since time stamping is a cholinergically mediated function of the circadian system, the early disruption of the cholinergic and circadian systems as seen in Alzheimer's disease (AD) may contribute to the cognitive disruption of temporal organization of memory and behavior in these patients.
AbstractList This review provides an overview of the interaction between the mammalian cholinergic system and circadian system, and its possible role in time memory. Several studies made clear that circadian (daily) fluctuations in acetylcholine (ACh) release, cholinergic enzyme activity and cholinergic receptor expression varies remarkably between species and even strains. Apparently, cholinergic features can be flexibly adjusted to the needs of a species or strain. Nevertheless, it can be generalized that circadian rhythmicity in the cholinergic system is characterized by high ACh release during the active phase of an individual. During the active phase, the activity of the ACh synthesizing enzyme Choline Acetyltransferase (ChAT) is enhanced, and the activity of the ACh degrading enzyme Acetylcholinesterase (AChE) is reduced. The number of free, unbound and thus available muscarinic acetylcholine receptors (mAChRs) is highest when ACh release is lowest. The cholinergic innervation of the suprachiasmatic nucleus (SCN), the hypothalamic circadian master clock, arises from the cholinergic forebrain and brain stem nuclei. The density of cholinergic fibers and terminals is modest as compared to other hypothalamic nuclei. This is the case for rat, hamster and mouse, three chronobiological model rodent species studied by us. A new finding is that the rat SCN contains some local cholinergic neurons. Hamster SCN contains less cholinergic neurons, whereas the mouse SCN is devoid of such cells. ACh has an excitatory effect on SCN cells (at least in vivo), and functions in close interaction with other neurotransmitters. Originally it was thought that ACh transferred retinal light information to the SCN. This turned out to be wrong. Thereafter, the phase shifting effects of ACh prompted researches to view ACh as an agent for nocturnal clock resetting. It is still not clear, however, what the function consequence is of SCN cholinergic neurotransmission. Here, we postulate the hypothesis that cholinergic neurotransmission in the SCN provides the brain with a mechanism to support the formation of time memory via 'time stamping'. We define time memory as the memory of a specific time of the day, for which an animal made an association with a certain event and/or location (for example in case of time-place association). We use the term 'time stamping' to refer to the process underlying the encoding of a specific time of day (the time stamp). Only relatively brief but arousing events seem to be time stamped at SCN level. This time stamping requires the engagement of mAChRs. New data suggests that the SCN uses the neuropeptide vasopressin (AVP) as an output system to transfer the specific time of day information to other brain regions such as hippocampus and neocortex where time memory is supposed to be acquired, consolidated and stored. Since time stamping is a cholinergically mediated function of the circadian system, the early disruption of the cholinergic and circadian systems as seen in Alzheimer's disease (AD) may contribute to the cognitive disruption of temporal organization of memory and behavior in these patients.
► Rat but not mouse SCN contains cholinergic neurons. ► SCN cholinergic neurotransmission supports time memory formation via time stamping. ► The neurppeptide AVP acts as an SCN output for time stamping. This review provides an overview of the interaction between the mammalian cholinergic system and circadian system, and its possible role in time memory. Several studies made clear that circadian (daily) fluctuations in acetylcholine (ACh) release, cholinergic enzyme activity and cholinergic receptor expression varies remarkably between species and even strains. Apparently, cholinergic features can be flexibly adjusted to the needs of a species or strain. Nevertheless, it can be generalized that circadian rhythmicity in the cholinergic system is characterized by high ACh release during the active phase of an individual. During the active phase, the activity of the ACh synthesizing enzyme Choline Acetyltransferase (ChAT) is enhanced, and the activity of the ACh degrading enzyme Acetylcholinesterase (AChE) is reduced. The number of free, unbound and thus available muscarinic acetylcholine receptors (mAChRs) is highest when ACh release is lowest. The cholinergic innervation of the suprachiasmatic nucleus (SCN), the hypothalamic circadian master clock, arises from the cholinergic forebrain and brain stem nuclei. The density of cholinergic fibers and terminals is modest as compared to other hypothalamic nuclei. This is the case for rat, hamster and mouse, three chronobiological model rodent species studied by us. A new finding is that the rat SCN contains some local cholinergic neurons. Hamster SCN contains less cholinergic neurons, whereas the mouse SCN is devoid of such cells. ACh has an excitatory effect on SCN cells (at least in vivo), and functions in close interaction with other neurotransmitters. Originally it was thought that ACh transferred retinal light information to the SCN. This turned out to be wrong. Thereafter, the phase shifting effects of ACh prompted researches to view ACh as an agent for nocturnal clock resetting. It is still not clear, however, what the function consequence is of SCN cholinergic neurotransmission. Here, we postulate the hypothesis that cholinergic neurotransmission in the SCN provides the brain with a mechanism to support the formation of time memory via ‘time stamping’. We define time memory as the memory of a specific time of the day, for which an animal made an association with a certain event and/or location (for example in case of time-place association). We use the term ‘time stamping’ to refer to the process underlying the encoding of a specific time of day (the time stamp). Only relatively brief but arousing events seem to be time stamped at SCN level. This time stamping requires the engagement of mAChRs. New data suggests that the SCN uses the neuropeptide vasopressin (AVP) as an output system to transfer the specific time of day information to other brain regions such as hippocampus and neocortex where time memory is supposed to be acquired, consolidated and stored. Since time stamping is a cholinergically mediated function of the circadian system, the early disruption of the cholinergic and circadian systems as seen in Alzheimer's disease (AD) may contribute to the cognitive disruption of temporal organization of memory and behavior in these patients.
Author Van der Zee, E.A.
Hut, R.A.
Author_xml – sequence: 1
  givenname: R.A.
  surname: Hut
  fullname: Hut, R.A.
  email: r.a.hut@rug.nl
  organization: Chronobiology Unit, Centre for Behaviour and Neurosciences, University of Groningen, Nijenborg 7, 9747 AG Groningen, The Netherlands
– sequence: 2
  givenname: E.A.
  surname: Van der Zee
  fullname: Van der Zee, E.A.
  organization: Molecular Biology Unit, Centre for Behaviour and Neurosciences, University of Groningen, Nijenborg 7, 9747 AG Groningen, The Netherlands
BackLink https://www.ncbi.nlm.nih.gov/pubmed/21115064$$D View this record in MEDLINE/PubMed
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Keywords Circadian system
Suprachiasmatic nucleus
Biological rhythms
Time stamping
Aging
Acetylcholine
Cholinergic system
Time memory
Muscarinic receptor
Nicotinic receptor
Alzheimer's disease
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Snippet ► Rat but not mouse SCN contains cholinergic neurons. ► SCN cholinergic neurotransmission supports time memory formation via time stamping. ► The neurppeptide...
This review provides an overview of the interaction between the mammalian cholinergic system and circadian system, and its possible role in time memory....
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SubjectTerms Acetylcholine
Acetylcholine - physiology
Aging
Aging - physiology
Alzheimer Disease - physiopathology
Alzheimer's disease
Animals
Arginine Vasopressin - physiology
Biological rhythms
Brain - physiology
Cholinergic Fibers - physiology
Cholinergic system
Circadian Clocks - physiology
Circadian Rhythm - physiology
Circadian system
Humans
Memory - physiology
Models, Biological
Muscarinic receptor
Nicotinic receptor
Receptors, Muscarinic - physiology
Suprachiasmatic nucleus
Suprachiasmatic Nucleus - physiology
Synaptic Transmission - physiology
Time memory
Time stamping
Title The cholinergic system, circadian rhythmicity, and time memory
URI https://dx.doi.org/10.1016/j.bbr.2010.11.039
https://www.ncbi.nlm.nih.gov/pubmed/21115064
https://search.proquest.com/docview/866533014
https://search.proquest.com/docview/883040976
Volume 221
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