Effect of Acute Enriched Environment Exposure on Brain Oscillations and Activation of the Translation Initiation Factor 4E-BPs at Synapses Across Wakefulness and Sleep in Rats

Overview

Journal Cells

Publisher MDPI

Specialties Biochemistry
Biophysics
Cell Biology
Molecular Biology

Date 2023 Sep 28

PMID 37759542

Authors

Jose Lucas Santos

Evlalia Petsidou

Pallavi Saraogi

Ullrich Bartsch

Andre P Gerber

Julie Seibt

Affiliations

Soon will be listed here.

Abstract

Brain plasticity is induced by learning during wakefulness and is consolidated during sleep. But the molecular mechanisms involved are poorly understood and their relation to experience-dependent changes in brain activity remains to be clarified. Localised mRNA translation is important for the structural changes at synapses supporting brain plasticity consolidation. The translation mTOR pathway, via phosphorylation of 4E-BPs, is known to be activate during sleep and contributes to brain plasticity, but whether this activation is specific to synapses is not known. We investigated this question using acute exposure of rats to an enriched environment (EE). We measured brain activity with EEGs and 4E-BP phosphorylation at cortical and cerebellar synapses with Western blot analyses. Sleep significantly increased the conversion of 4E-BPs to their hyperphosphorylated forms at synapses, especially after EE exposure. EE exposure increased oscillations in the alpha band during active exploration and in the theta-to-beta (4-30 Hz) range, as well as spindle density, during NREM sleep. Theta activity during exploration and NREM spindle frequency predicted changes in 4E-BP hyperphosphorylation at synapses. Hence, our results suggest a functional link between EEG and molecular markers of plasticity across wakefulness and sleep.

References

Bidinosti M, Ran I, Sanchez-Carbente M, Martineau Y, Gingras A, Gkogkas C . Postnatal deamidation of 4E-BP2 in brain enhances its association with raptor and alters kinetics of excitatory synaptic transmission. Mol Cell. 2010; 37(6):797-808. PMC: 2861547. DOI: 10.1016/j.molcel.2010.02.022. View

Peyrache A, Seibt J . A mechanism for learning with sleep spindles. Philos Trans R Soc Lond B Biol Sci. 2020; 375(1799):20190230. PMC: 7209910. DOI: 10.1098/rstb.2019.0230. View

Hu Y, Ferrario C, Maitland A, Ionides R, Ghimire A, Watson B . : Quantification of user-defined animal behaviors using learning-based holistic assessment. Cell Rep Methods. 2023; 3(3):100415. PMC: 10088092. DOI: 10.1016/j.crmeth.2023.100415. View

Poulin F, Gingras A, Olsen H, Chevalier S, Sonenberg N . 4E-BP3, a new member of the eukaryotic initiation factor 4E-binding protein family. J Biol Chem. 1998; 273(22):14002-7. DOI: 10.1074/jbc.273.22.14002. View

Saraf A, Luo J, Morris D, Storm D . Phosphorylation of eukaryotic translation initiation factor 4E and eukaryotic translation initiation factor 4E-binding protein (4EBP) and their upstream signaling components undergo diurnal oscillation in the mouse hippocampus: implications for.... J Biol Chem. 2014; 289(29):20129-38. PMC: 4106328. DOI: 10.1074/jbc.M114.552638. View

van Praag H, Kempermann G, Gage F . Neural consequences of environmental enrichment. Nat Rev Neurosci. 2001; 1(3):191-8. DOI: 10.1038/35044558. View

Alwis D, Rajan R . Environmental enrichment and the sensory brain: the role of enrichment in remediating brain injury. Front Syst Neurosci. 2014; 8:156. PMC: 4151031. DOI: 10.3389/fnsys.2014.00156. View

Huber R, Deboer T, Tobler I . Effects of sleep deprivation on sleep and sleep EEG in three mouse strains: empirical data and simulations. Brain Res. 2000; 857(1-2):8-19. DOI: 10.1016/s0006-8993(99)02248-9. View

L Banko J, Hou L, Poulin F, Sonenberg N, Klann E . Regulation of eukaryotic initiation factor 4E by converging signaling pathways during metabotropic glutamate receptor-dependent long-term depression. J Neurosci. 2006; 26(8):2167-73. PMC: 6674817. DOI: 10.1523/JNEUROSCI.5196-05.2006. View

10.

Ramm P, Smith C . Rates of cerebral protein synthesis are linked to slow wave sleep in the rat. Physiol Behav. 1990; 48(5):749-53. DOI: 10.1016/0031-9384(90)90220-x. View

11.

Huber R, Deboer T, Tobler I . Topography of EEG dynamics after sleep deprivation in mice. J Neurophysiol. 2000; 84(4):1888-93. DOI: 10.1152/jn.2000.84.4.1888. View

12.

Blumberg M, Dooley J, Tiriac A . Sleep, plasticity, and sensory neurodevelopment. Neuron. 2022; 110(20):3230-3242. PMC: 9588561. DOI: 10.1016/j.neuron.2022.08.005. View

13.

Fares R, Belmeguenai A, Sanchez P, Kouchi H, Bodennec J, Morales A . Standardized environmental enrichment supports enhanced brain plasticity in healthy rats and prevents cognitive impairment in epileptic rats. PLoS One. 2013; 8(1):e53888. PMC: 3544705. DOI: 10.1371/journal.pone.0053888. View

14.

Fernandez L, Luthi A . Sleep Spindles: Mechanisms and Functions. Physiol Rev. 2019; 100(2):805-868. DOI: 10.1152/physrev.00042.2018. View

15.

Sigl-Glockner J, Seibt J . Peeking into the sleeping brain: Using in vivo imaging in rodents to understand the relationship between sleep and cognition. J Neurosci Methods. 2018; 316:71-82. PMC: 6390172. DOI: 10.1016/j.jneumeth.2018.09.011. View

16.

L Banko J, Poulin F, Hou L, DeMaria C, Sonenberg N, Klann E . The translation repressor 4E-BP2 is critical for eIF4F complex formation, synaptic plasticity, and memory in the hippocampus. J Neurosci. 2005; 25(42):9581-90. PMC: 6725736. DOI: 10.1523/JNEUROSCI.2423-05.2005. View

17.

Halassa M, Siegle J, Ritt J, Ting J, Feng G, Moore C . Selective optical drive of thalamic reticular nucleus generates thalamic bursts and cortical spindles. Nat Neurosci. 2011; 14(9):1118-20. PMC: 4169194. DOI: 10.1038/nn.2880. View

18.

Franken P, Dijk D, Tobler I, Borbely A . Sleep deprivation in rats: effects on EEG power spectra, vigilance states, and cortical temperature. Am J Physiol. 1991; 261(1 Pt 2):R198-208. DOI: 10.1152/ajpregu.1991.261.1.R198. View

19.

Frank M . Sleep and synaptic plasticity in the developing and adult brain. Curr Top Behav Neurosci. 2014; 25:123-49. PMC: 7485264. DOI: 10.1007/7854_2014_305. View

20.

Tononi G, Cirelli C . Sleep and synaptic homeostasis: a hypothesis. Brain Res Bull. 2003; 62(2):143-50. DOI: 10.1016/j.brainresbull.2003.09.004. View