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Sleep Modulation Alleviates Axonal Damage and Cognitive Decline after Rodent Traumatic Brain Injury

Marta M. Morawska, Fabian Büchele, Carlos Goncalves Moreira, Lukas L. Imbach, Daniela Noain and Christian R. Baumann
Journal of Neuroscience 23 March 2016, 36 (12) 3422-3429; DOI: https://doi.org/10.1523/JNEUROSCI.3274-15.2016
Marta M. Morawska
Department of Neurology, University Hospital of Zurich, 8091 Zurich, Switzerland
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Fabian Büchele
Department of Neurology, University Hospital of Zurich, 8091 Zurich, Switzerland
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Carlos Goncalves Moreira
Department of Neurology, University Hospital of Zurich, 8091 Zurich, Switzerland
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Lukas L. Imbach
Department of Neurology, University Hospital of Zurich, 8091 Zurich, Switzerland
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Daniela Noain
Department of Neurology, University Hospital of Zurich, 8091 Zurich, Switzerland
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Christian R. Baumann
Department of Neurology, University Hospital of Zurich, 8091 Zurich, Switzerland
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    Figure 1.

    Sleep modulation after TBI. A, Time schedule of modulation interventions and behavioral testing. TBI and sham animals were divided into three groups: Ctrl, SI, and SR animals. For 5 d after TBI induction, animals received 2×/d intraperitoneal saline injections (Ctrl), 2× day SO injections (400 mg/kg, i.p.; SI), or 2×/d intraperitoneal saline injections plus 6 h per day gentle handling (SR). B, Exemplary traces representing the four characterized behavioral states: wake, NREM, PS, and SWS-like state. C, Exemplary EEG traces showing the effect of SO administration on EEG and of sleep restriction on sleep rebound EEG.

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    Figure 2.

    Effect of sleep modulation on vigilance states, fragmentation, and delta power after TBI. A, Proportions of vigilance states during last day of sleep modulation (TBI only). Light period: Only the SR group showed increase time spent awake with subsequent decrease in time spent in SWS and PS compared with Ctrl (wake: p < 0.001, SWS: p < 0.001, PS: p < 0.05). During the dark period, both sleep-modulated groups showed a decrease in time spent in wake compared with control animals (p < 0.05) and an increase in time spent in SWS (p < 0.05); only the SR group showed an increase in the time spent in PS (p < 0.01). Over the 24 h, only the SI group showed increased time spent in SWS (p < 0.01) and decreased time spent awake (p < 0.001). B, Effect of sleep modulation on fragmentation of behavioral states. Differences in fragmentation index (bout/epoch) were only apparent during wake, whereas in the light period, the SR group showed more stable wake (p < 0.05) and the SI group showed more fragmented wake (p < 0.05) compared with controls. During the dark period, both of the groups had more fragmented wake compared with controls (SI: p < 0.01, SR: p < 0.05). C, Effect of sleep modulation on delta power. Both the SI and SR groups had a bigger proportion of delta power during SWS in the light period (p < 0.05), dark period (SI: p < 0.01, SR p < 0.05), and over 24 h (SI: p < 0.01, SR p < 0.05) compared with controls. Data presented in 10 min bins shows dynamic changes in delta power over the 24-h recording period.

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    Figure 3.

    Effect of sleep modulation on cognitive performance in novel object recognition test (NORT) after TBI. All charts show recognition index compared with chance level (0.5). Before TBI induction (baseline, BL), all animals showed intact cognitive abilities (p < 0.05). TBI resulted in a decrease of memory performance at 14 d after trauma, but cognitive abilities were spared in both the SI and SR TBI animals; the sham groups continued performing equally well after the surgical intervention (sham Ctrl: p < 0.05, sham SI: p < 0.05, sham SR: p < 0.05, TBI Ctrl: p > 0.05, TBI SI: p < 0.05, TBI SR: p < 0.05).

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    Figure 4.

    Effect of sleep modulation on histological markers after TBI. A, C, Representative images from sham and TBI animals (all groups) showing cortical (A) and hippocampal (C) APP staining. Only the non-sleep-modulated control TBI group showed marked axonal staining. B, D, Quantification of APP-immunoreactive cells in cortex (B) and hippocampus (D). All charts show the number of positive grid squares of one section divided by the area of cortex (number of positive squares per square millimeter of cortex). The TBI control group shows the highest APP trauma index (reflecting the highest expression of APP), which is significantly different from the sham group (p < 0.05). Sleep modulation resulted in decrease of APP expression in cortex and hippocampus, as indicated by the decreased APP trauma index in the sleep-induced TBI group (p < 0.01) and the sleep-restricted TBI group (p < 0.01). E, Quantification of ATF-4-immunoreactive cells in cortex. No difference was noted in ATF-4 immunoreactivity between the groups. F, Quantification of UB immunoreactivity in cortex. There was no difference in UB immunoreactivity between the groups.

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The Journal of Neuroscience: 36 (12)
Journal of Neuroscience
Vol. 36, Issue 12
23 Mar 2016
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Sleep Modulation Alleviates Axonal Damage and Cognitive Decline after Rodent Traumatic Brain Injury
Marta M. Morawska, Fabian Büchele, Carlos Goncalves Moreira, Lukas L. Imbach, Daniela Noain, Christian R. Baumann
Journal of Neuroscience 23 March 2016, 36 (12) 3422-3429; DOI: 10.1523/JNEUROSCI.3274-15.2016

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Sleep Modulation Alleviates Axonal Damage and Cognitive Decline after Rodent Traumatic Brain Injury
Marta M. Morawska, Fabian Büchele, Carlos Goncalves Moreira, Lukas L. Imbach, Daniela Noain, Christian R. Baumann
Journal of Neuroscience 23 March 2016, 36 (12) 3422-3429; DOI: 10.1523/JNEUROSCI.3274-15.2016
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Keywords

  • diffuse axonal damage
  • memory
  • sleep
  • traumatic brain injury

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JNeurosci   Print ISSN: 0270-6474   Online ISSN: 1529-2401