Differential effects of duration of sleep fragmentation on spatial learning and synaptic plasticity in pubertal mice

Eli Wallace, Do Young Kim, Kye Min Kim, Stephanie Chen, Brittany Braden, Jeremy Williams, Kalene Jasso, Alex Garcia, Jong M. Rho, Heather Bimonte-Nelson, Rama Maganti

Research output: Contribution to journalArticle

9 Citations (Scopus)

Abstract

Study objective To examine the differential effects of acute and chronic sleep fragmentation (SF) on spatial learning and memory, and hippocampal long-term potentiation (LTP) in pubertal mice. Methods Two studies were performed during which adolescent C57/Bl6 mice were subjected to acute-SF 24 h a day×3 days or chronic-SF for 12 h a day×2 weeks using a programmable rotating lever that provides tactile stimulus with controls housed in similar cages. Spatial learning and memory was examined using the Morris water maze, and long-term potentiation (LTP) was evaluated after stimulation of Schaffer collaterals in CA1 hippocampus post SF. Actigraphy was used during the period of SF to monitor rest-activity patterns. Electroencephalographic (EEG) recordings were acquired for analysis of vigilance state patterns and delta-power. Serum corticosterone was measured to assess stress levels. Results Acute-SF via tactile stimulation negatively impacted spatial learning, as well as LTP maintenance, compared to controls with no tactile stimulation. While actigraphy showed significantly increased motor activity during SF in both groups, EEG data indicated that overall sleep efficiency did not differ between baseline and SF days, but significant increases in number of wakeful bouts and decreases in average NREM and REM bout lengths were seen during lights-on. Acute sleep fragmentation did not impact corticosterone levels. Conclusions The current results indicate that, during development in pubertal mice, acute-SF for 24 h a day×3 days negatively impacted spatial learning and synaptic plasticity. Further studies are needed to determine if any inherent long-term homeostatic mechanisms in the adolescent brain afford greater resistance to the deleterious effects of chronic-SF.

Original languageEnglish (US)
Pages (from-to)116-128
Number of pages13
JournalBrain Research
Volume1615
DOIs
StatePublished - 2015

Fingerprint

Neuronal Plasticity
Sleep Deprivation
Long-Term Potentiation
Touch
Actigraphy
Corticosterone
Hippocampus
Spatial Learning
Sleep
Motor Activity
Maintenance

Keywords

  • Adolescence
  • LTP
  • Mice
  • Morris water maze
  • Sleep fragmentation
  • Spatial memory

ASJC Scopus subject areas

  • Neuroscience(all)
  • Clinical Neurology
  • Developmental Biology
  • Molecular Biology
  • Medicine(all)

Cite this

Differential effects of duration of sleep fragmentation on spatial learning and synaptic plasticity in pubertal mice. / Wallace, Eli; Kim, Do Young; Kim, Kye Min; Chen, Stephanie; Braden, Brittany; Williams, Jeremy; Jasso, Kalene; Garcia, Alex; Rho, Jong M.; Bimonte-Nelson, Heather; Maganti, Rama.

In: Brain Research, Vol. 1615, 2015, p. 116-128.

Research output: Contribution to journalArticle

Wallace, Eli ; Kim, Do Young ; Kim, Kye Min ; Chen, Stephanie ; Braden, Brittany ; Williams, Jeremy ; Jasso, Kalene ; Garcia, Alex ; Rho, Jong M. ; Bimonte-Nelson, Heather ; Maganti, Rama. / Differential effects of duration of sleep fragmentation on spatial learning and synaptic plasticity in pubertal mice. In: Brain Research. 2015 ; Vol. 1615. pp. 116-128.
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abstract = "Study objective To examine the differential effects of acute and chronic sleep fragmentation (SF) on spatial learning and memory, and hippocampal long-term potentiation (LTP) in pubertal mice. Methods Two studies were performed during which adolescent C57/Bl6 mice were subjected to acute-SF 24 h a day×3 days or chronic-SF for 12 h a day×2 weeks using a programmable rotating lever that provides tactile stimulus with controls housed in similar cages. Spatial learning and memory was examined using the Morris water maze, and long-term potentiation (LTP) was evaluated after stimulation of Schaffer collaterals in CA1 hippocampus post SF. Actigraphy was used during the period of SF to monitor rest-activity patterns. Electroencephalographic (EEG) recordings were acquired for analysis of vigilance state patterns and delta-power. Serum corticosterone was measured to assess stress levels. Results Acute-SF via tactile stimulation negatively impacted spatial learning, as well as LTP maintenance, compared to controls with no tactile stimulation. While actigraphy showed significantly increased motor activity during SF in both groups, EEG data indicated that overall sleep efficiency did not differ between baseline and SF days, but significant increases in number of wakeful bouts and decreases in average NREM and REM bout lengths were seen during lights-on. Acute sleep fragmentation did not impact corticosterone levels. Conclusions The current results indicate that, during development in pubertal mice, acute-SF for 24 h a day×3 days negatively impacted spatial learning and synaptic plasticity. Further studies are needed to determine if any inherent long-term homeostatic mechanisms in the adolescent brain afford greater resistance to the deleterious effects of chronic-SF.",
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N2 - Study objective To examine the differential effects of acute and chronic sleep fragmentation (SF) on spatial learning and memory, and hippocampal long-term potentiation (LTP) in pubertal mice. Methods Two studies were performed during which adolescent C57/Bl6 mice were subjected to acute-SF 24 h a day×3 days or chronic-SF for 12 h a day×2 weeks using a programmable rotating lever that provides tactile stimulus with controls housed in similar cages. Spatial learning and memory was examined using the Morris water maze, and long-term potentiation (LTP) was evaluated after stimulation of Schaffer collaterals in CA1 hippocampus post SF. Actigraphy was used during the period of SF to monitor rest-activity patterns. Electroencephalographic (EEG) recordings were acquired for analysis of vigilance state patterns and delta-power. Serum corticosterone was measured to assess stress levels. Results Acute-SF via tactile stimulation negatively impacted spatial learning, as well as LTP maintenance, compared to controls with no tactile stimulation. While actigraphy showed significantly increased motor activity during SF in both groups, EEG data indicated that overall sleep efficiency did not differ between baseline and SF days, but significant increases in number of wakeful bouts and decreases in average NREM and REM bout lengths were seen during lights-on. Acute sleep fragmentation did not impact corticosterone levels. Conclusions The current results indicate that, during development in pubertal mice, acute-SF for 24 h a day×3 days negatively impacted spatial learning and synaptic plasticity. Further studies are needed to determine if any inherent long-term homeostatic mechanisms in the adolescent brain afford greater resistance to the deleterious effects of chronic-SF.

AB - Study objective To examine the differential effects of acute and chronic sleep fragmentation (SF) on spatial learning and memory, and hippocampal long-term potentiation (LTP) in pubertal mice. Methods Two studies were performed during which adolescent C57/Bl6 mice were subjected to acute-SF 24 h a day×3 days or chronic-SF for 12 h a day×2 weeks using a programmable rotating lever that provides tactile stimulus with controls housed in similar cages. Spatial learning and memory was examined using the Morris water maze, and long-term potentiation (LTP) was evaluated after stimulation of Schaffer collaterals in CA1 hippocampus post SF. Actigraphy was used during the period of SF to monitor rest-activity patterns. Electroencephalographic (EEG) recordings were acquired for analysis of vigilance state patterns and delta-power. Serum corticosterone was measured to assess stress levels. Results Acute-SF via tactile stimulation negatively impacted spatial learning, as well as LTP maintenance, compared to controls with no tactile stimulation. While actigraphy showed significantly increased motor activity during SF in both groups, EEG data indicated that overall sleep efficiency did not differ between baseline and SF days, but significant increases in number of wakeful bouts and decreases in average NREM and REM bout lengths were seen during lights-on. Acute sleep fragmentation did not impact corticosterone levels. Conclusions The current results indicate that, during development in pubertal mice, acute-SF for 24 h a day×3 days negatively impacted spatial learning and synaptic plasticity. Further studies are needed to determine if any inherent long-term homeostatic mechanisms in the adolescent brain afford greater resistance to the deleterious effects of chronic-SF.

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