Rapid eye movement sleep deprivation modifies expression of long-term potentiation in visual cortex of immature rats

doi:10.1016/S0306-4522(01)00589-9

Neuroscience

Volume 110, Issue 3, 20 March 2002, Pages 431-443

https://doi.org/10.1016/S0306-4522(01)00589-9 Get rights and content

Abstract

During rapid eye movement (REM) sleep, activity of non-retinal origin is propagated into central visual-system pathways in a manner similar, in pattern and intensity, to central visual-system activity that is exogenously generated in waking. It has been hypothesized that REM sleep, which is more abundantly represented early in life than later, functions to provide adjunct ‘afferent’ input for shaping synaptic connectivity during brain maturation. Here we present data that support this proposal.

Recent studies have described a developmentally regulated form of in vitro long-term potentiation (LTP) in the visual cortex that is experience- and age-dependent. In immature rats, suppression of retinal activation of the visual system by removal of visual experience (dark rearing) extends the age when the developmentally regulated form of LTP can be produced. This study tests whether suppression of REM-state activation of the visual system also lengthens the developmental period in which this specific form of LTP can be elicited. Young rats were deprived of REM sleep by the multiple-small-platforms-over-water method during the typically latest week for induction of such LTP in slices of visual cortex. After this week, we could still induce LTP in slices from nearly all the REM-sleep-deprived rats (8/9) but not from age-matched rats that had not lost REM sleep (0/5). The control rats had been housed on large platforms that allow the animals to obtain REM sleep. Only body weights and the concentration of thyrotrophin-releasing hormone in the hypothalamus distinguished home-caged, normal-sleeping controls from both groups of platform animals. On all measures, stress levels were not dissimilar in the two platforms groups.

After 7 days of behavioral suppression of REM sleep in immature rats, and consequent reduction of the intense, extra-retinal activity endogenously generated during this sleep state, we found that the period was extended in which developmentally regulated synaptic plasticity (LTP) could be elicited in slices of visual neocortex. These studies support the role of REM sleep and its associated neuronal activity in brain maturation.

Section snippets

Subjects

All procedures were carried out in conformity with guidelines of the NIH and approval of the local Internal Review Board for Care and Use of Animals. Every effort was made to minimize animal suffering, and only the minimum number of animals necessary to obtain reliable data was utilized. Long–Evans hooded rat pups were obtained either from timed-pregnant dams housed in our own animal facilities or directly from the breeder as independent groups of weaned, 21-day-old littermates (Harlan, IL,

Developmental LTP studies in untreated, home-cage-housed animals

The data for the developmentally regulated form of LTP (cf. Kirkwood et al., 1995, Perkins and Teyler, 1988) in untreated animals, all of whom resided with their home-cage littermates until time of death, were derived from three age groups: (1) P20–22 – just after weaning; (2) P28–30 – near the end of the critical period for the developmental type of LTP; and (3) P36–40 – beyond the reported end of the critical period. LTP could be obtained until P28–30 (see Fig. 1). The oldest animal in which

Discussion

Behavioral observation documented that young rats residing on small platforms lose postural control, indicating entry into REM sleep, and are awakened repeatedly at variable intervals virtually every time they fall asleep. Immature rats lying on larger platforms that support their whole body, even after entering REM sleep and losing muscle tone, continue sleeping. Though our behavioral data do not permit scoring of sleep-stage amounts, the small-pedestal method of REM sleep deprivation appears

Concluding remarks

REM sleep deprivation extends the usual postnatal critical period for production of a developmental form of LTP. This result, detected with in vitro LTP studies performed in visual cortex slices from REM-sleep-deprived, immature rats, accords with earlier experiments that found other measures of increased synaptic plasticity in the developing visual system following suppression of REM-sleep-related activation (Oksenberg et al., 1996, Shaffery et al., 1998a). The current study provides

Acknowledgements

The authors thank Thomas Fitch, Christian Birabil and Dr. Zizhaung Li for their able technical assistance. This work was supported by NIH Grant NS31720.

References (96)

M.F Bear et al.
Neocortical long-term potentiation
Curr. Opin. Neurobiol.
(1993)
R.L Berry et al.
Visual deprivation decreases long-term potentiation in rat visual cortical slices
Brain Res.
(1993)
J.A Brandt et al.
Sleep deprivation but not a whisker trim increases nerve growth factor within barrel cortical neurons
Brain Res.
(2001)
S Brocher et al.
Agonists of cholinergic and noradrenergic receptors facilitate synergistically the induction of long-term potentiation in slices of rat visual cortex
Brain Res.
(1992)
L Chen et al.
Developmental changes in the expression of NMDA receptor subunits (NR1, NR2A, NR2B) in the cat visual cortex and the effects of dark rearing
Mol. Brain Res.
(2000)
D.M Diamond et al.
Psychological stress repeatedly blocks hippocampal primed burst potentiation in behaving rats
Behav. Brain Res.
(1994)
M.G Frank et al.
Sleep enhances plasticity in the developing visual cortex
Neuron
(2001)
Z Gil et al.
Differential regulation of neocortical synapses by neuromodulators and activity
Neuron
(1997)
B Hu et al.
The cellular mechanisms of thalamic ponto-geniculo-occipital (PGO) waves
Neuroscience
(1989)
L Kojic et al.
Serotonin facilitates synaptic plasticity in kitten visual cortex: an in vitro study
Brain Res. Dev. Brain Res.
(1997)

L Kojic et al.

Laminar distribution of cholinergic- and serotonergic-dependent plasticity within kitten visual cortex

Dev. Brain Res.

(2001)

V.M Kovalzon et al.

REM-sleep deprivation, stress and emotional behvior in rats

Behav. Brain Res.

(1984)

G.A Marks et al.

Neuronal activity in the lateral geniculate nucleus associated with ponto-geniculo-occipital waves lacks lamina specificity

Brain Res.

(1999)

G.A Marks et al.

A functional role for REM sleep in brain maturation

Behav. Brain Res.

(1995)

F Marrosu et al.

Microdialysis measurement of cortical and hippocampal acetylcholine release during sleep-wake cycle in freely moving cats

Brain Res.

(1995)

W.B Mendelson et al.

The flower pot technique of rapid eye movement (REM) sleep deprivation

Pharmacol. Biochem. Behav.

(1974)

G.D Mower

The effect of dark rearing on the time course of the critical period in cat visual cortex

Dev. Brain Res.

(1991)

A Oksenberg et al.

Rapid eye movement sleep deprivation in kittens amplifies LGN cell-size disparity induced by monocular deprivation

Dev. Brain Res.

(1996)

C Pavlides et al.

Role of adrenal steroid mineralocorticoid and glucocorticoid receptors in long-term potentiation in the CA1 field of hippocampal slices

Brain Res.

(1996)

G.R Poe et al.

Experience-dependent phase-reversal of hippocampal neuron firing during REM sleep

Brain Res.

(2000)

C Rampin et al.

Immobilization stress induced a paradoxical sleep rebound in rat

Neurosci. Lett.

(1991)

E Satinoff et al.

Paleocortical excitability and sensory filtering during REM sleep deprivation

Physiol. Behav.

(1971)

J.P Shaffery et al.

Ponto-geniculo-occipital-wave suppression amplifies lateral geniculate nucleus cell-size changes in monocularly deprived kittens

Dev. Brain Res.

(1999)

C.J Shatz

Impulse activity and the patterning of connections during CNS development

Neuron

(1990)

M Steriade et al.

Projections of cholinergic and non-cholinergic neurons of the brainstem core to relay and associational thalamic nuclei in the cat and macaque monkey

Neuroscience

(1988)

R.O Wong et al.

Transient period of correlated bursting activity during development of the mammalian retina

Neuron

(1993)

C.D Aizenman et al.

A current source density analysis of evoked responses in slices of adult rat visual cortex: implications for the regulation of long-term potentiation

Cereb. Cortex

(1996)

M.F Bear et al.

Binocular competition in the control of geniculate cell size depends upon visual cortical N-methyl-D-aspartate receptor activation

Proc. Natl. Acad. Sci. USA

(1990)

M.F Bear et al.

Long-term potentiation in slices of kitten visual cortex and the effects of NMDA receptor blockade

J. Neurophysiol.

(1992)

E.L Bienenstock et al.

Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex

J. Neurosci.

(1982)

G Bissette et al.

Neuropeptide alterations in REM sleep deprived rat brain regions

Soc. Neurosci. Abstr.

(1998)

E Bizzi et al.

Functional connections between pontine reticular formation and lateral geniculate nucleus during deep sleep

Arch. Ital. Biol.

(1963)

T.V Bliss et al.

A synaptic model of memory: long-term potentiation in the hippocampus

Nature

(1993)

T.V Bliss et al.

Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path

J. Physiol.

(1973)

D.C Brooks et al.

Brainstem electrical activity during deep sleep

Arch. Ital. Biol.

(1963)

G Buzsaki

Functions for interneuronal nets in the hippocampus

Can. J. Physiol. Pharmacol.

(1997)

G Buzsaki

Memory consolidation during sleep: a neurophysiological perspective

J. Sleep Res.

(1998)

G Buzsaki et al.

Somadendritic backpropagation of action potentials in cortical pyramidal cells of the awake rat

J. Neurophysiol.

(1998)

W.B Carden et al.

Development of the cholinergic, nitrergic, and GABAergic innervation of the cat dorsal lateral geniculate nucleus

J. Comp. Neurol.

(2000)

F Crick et al.

The function of dream sleep

Nature

(1983)

M Cynader et al.

Prolonged sensitivity to monocular deprivation in dark-reared cats

J. Neurophysiol.

(1980)

S Datta

Avoidance task training potentiates phasic pontine-wave density in the rat: A mechanism for sleep-dependent plasticity

J. Neurosci.

(2000)

S Datta et al.

Localization of pontine PGO wave generation sites and their anatomical projections in the rat

Synapse

(1998)

N.W Daw et al.

Injection of MK-801 affects ocular dominance shifts more than visual activity

J. Neurophysiol.

(1999)

N.W Daw et al.

Cortisol reduces plasticity in the kitten visual cortex

J. Neurobiol.

(1991)

Dement, W., 1969. The biological role of REMS sleep (circa 1968). In: Kales, A. (Ed.), Sleep: Physiology and Pathology....

D.M Diamond et al.

Stress impairs LTP and hippocampal-dependent memory

Ann. NY Acad. Sci.

(1994)

S.M Dudek et al.

Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade

Proc. Natl. Acad. Sci. USA

(1992)

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Rapid eye movement sleep deprivation modifies expression of long-term potentiation in visual cortex of immature rats

Abstract

Section snippets

Subjects

Developmental LTP studies in untreated, home-cage-housed animals

Discussion

Concluding remarks

Acknowledgements

Curr. Opin. Neurobiol.

Brain Res.

Brain Res.

Brain Res.

Mol. Brain Res.

Behav. Brain Res.

Neuron

Neuron

Neuroscience

Brain Res. Dev. Brain Res.

Dev. Brain Res.

Behav. Brain Res.

Brain Res.

Behav. Brain Res.

Brain Res.

Pharmacol. Biochem. Behav.

Dev. Brain Res.

Dev. Brain Res.

Brain Res.

Brain Res.

Neurosci. Lett.

Physiol. Behav.

Dev. Brain Res.

Neuron

Neuroscience

Neuron

A current source density analysis of evoked responses in slices of adult rat visual cortex: implications for the regulation of long-term potentiation

Cereb. Cortex

Binocular competition in the control of geniculate cell size depends upon visual cortical N-methyl-D-aspartate receptor activation

Proc. Natl. Acad. Sci. USA

Long-term potentiation in slices of kitten visual cortex and the effects of NMDA receptor blockade

J. Neurophysiol.

Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex

J. Neurosci.

Neuropeptide alterations in REM sleep deprived rat brain regions

Soc. Neurosci. Abstr.

Functional connections between pontine reticular formation and lateral geniculate nucleus during deep sleep

Arch. Ital. Biol.

A synaptic model of memory: long-term potentiation in the hippocampus

Nature

Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path

J. Physiol.

Brainstem electrical activity during deep sleep

Arch. Ital. Biol.

Functions for interneuronal nets in the hippocampus

Can. J. Physiol. Pharmacol.

Memory consolidation during sleep: a neurophysiological perspective

J. Sleep Res.

Somadendritic backpropagation of action potentials in cortical pyramidal cells of the awake rat

J. Neurophysiol.

Development of the cholinergic, nitrergic, and GABAergic innervation of the cat dorsal lateral geniculate nucleus

J. Comp. Neurol.

The function of dream sleep

Nature

Prolonged sensitivity to monocular deprivation in dark-reared cats

J. Neurophysiol.

Avoidance task training potentiates phasic pontine-wave density in the rat: A mechanism for sleep-dependent plasticity

J. Neurosci.

Localization of pontine PGO wave generation sites and their anatomical projections in the rat

Synapse

Injection of MK-801 affects ocular dominance shifts more than visual activity

J. Neurophysiol.

Cortisol reduces plasticity in the kitten visual cortex

J. Neurobiol.

Stress impairs LTP and hippocampal-dependent memory

Ann. NY Acad. Sci.

Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade

Proc. Natl. Acad. Sci. USA