Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-23T17:00:27.405Z Has data issue: false hasContentIssue false

8 - Circadian Rhythms Regulate Neuroinflammation after Traumatic Brain Injury and Spinal Cord Injury

Published online by Cambridge University Press:  07 October 2023

By
Andrew D. Gaudet  and
Emily K. Greenough
Edited by
Laura K. Fonken  and
Randy J. Nelson
Laura K. Fonken
Affiliation:
University of Texas, Austin
Randy J. Nelson
Affiliation:
West Virginia University
Get access

Summary

The circadian system in mammals involves a hierarchy of clock regulators that entrain circadian rhythms in the periphery. The molecular circadian clock regulates all systems in the body, including the nervous and immune systems. Under healthy conditions, the circadian system enables effective function of the nervous and immune systems by promoting system vigilance during predicted daily active phases, and rejuvenation during rest phases. However, injury to the nervous system causes spiralling neuroimmune activation that exacerbates damage. Here, we will discuss how the circadian system regulates neuroinflammatory dynamics in the central nervous system during health and after neurotrauma. Traumatic brain injury or spinal cord injury dysregulate the circadian system, and circadian disruption is worsened during acute post-injury times by a suboptimal circadian environment in the hospital. In turn, circadian disruption unleashes immune activation and impairs reparative responses, thereby worsening damage. Given the intimate link between the circadian and neuroimmune systems, there are several levels of potential therapeutic intervention. Environmental interventions include improving light–dark amplitude between day and night and reducing nighttime interruptions acutely after neurotrauma. Pharmacologic interventions after injury could reinforce circadian rhythms or target clock genes to create a reparative neuroimmune milieu. Future studies should explore the circadian–neuroimmune axis, with a goal to use evidence-based chronotherapies to enhance repair and recovery after traumatic brain injury and spinal cord injury.

Keywords

circadian rhythmneuroinflammationspinal cord injury
Type
Chapter
Information
Biological Implications of Circadian Disruption
A Modern Health Challenge
 , pp. 183 - 205
Publisher: Cambridge University Press
Print publication year: 2023

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abell, J. G., Shipley, M. J., Ferrie, J. E., Kivimäki, M., & Kumari, M. (2016). Recurrent short sleep, chronic insomnia symptoms and salivary cortisol: A 10-year follow-up in the Whitehall II study. Psychoneuroendocrinology, 68, 91–99.CrossRefGoogle ScholarPubMed
Ajami, B., Bennett, J. L., Krieger, C., McNagny, K. M., & Rossi, F. M. (2011). Infiltrating monocytes trigger EAE progression, but do not contribute to the resident microglia pool. Nat Neurosci, 14(9), 1142–1149.Google Scholar
Alexander, R. K., Liou, Y. H., Knudsen, N. H., Starost, K. A., Xu, C., Hyde, A. L., Liu, S., Jacobi, D., Liao, N.-S., & Lee, C. H. (2020). Bmal1 integrates mitochondrial metabolism and macrophage activation. Elife, 9, e54090.Google Scholar
Alizadeh, A., Dyck, S. M., & Karimi-Abdolrezaee, S. (2019). Traumatic spinal cord injury: An overview of pathophysiology, models and acute injury mechanisms. Front Neurol, 10, 282.CrossRefGoogle ScholarPubMed
Andelic, N., Sigurdardottir, S., Schanke, A. K., Sandvik, L., Sveen, U., & Roe, C. (2010). Disability, physical health and mental health 1 year after traumatic brain injury. Disabil Rehabil, 32(13), 1122–1131.Google Scholar
Anderson, K. D. (2004). Targeting recovery: Priorities of the spinal cord-injured population. J Neurotrauma, 21(10), 1371–1383.CrossRefGoogle ScholarPubMed
Anderson, M. A., Burda, J. E., Ren, Y., Ao, Y., O’Shea, T. M., Kawaguchi, R., Coppola, G., Khakh, B. S., Deming, T. J., & Sofroniew, M. V. (2016). Astrocyte scar formation aids CNS axon regeneration. Nature, 532(7598), 195–200.CrossRefGoogle Scholar
Beck, K. D., Nguyen, H. X., Galvan, M. D., Salazar, D. L., Woodruff, T. M., & Anderson, A. J. (2010). Quantitative analysis of cellular inflammation after traumatic spinal cord injury: Evidence for a multiphasic inflammatory response in the acute to chronic environment. Brain, 133(Pt 2), 433–447.Google Scholar
Bellver-Landete, V., Bretheau, F., Mailhot, B., Vallieres, N., Lessard, M., Janelle, M. E., Vernoux, N., Tremblay, M.-È., Fuehrmann, T., Shoichet, M. S., & Lacroix, S. (2019). Microglia are an essential component of the neuroprotective scar that forms after spinal cord injury. Nat Commun, 10(1), 518.CrossRefGoogle ScholarPubMed
Berson, D. M., Dunn, F. A., & Takao, M. (2002). Phototransduction by retinal ganglion cells that set the circadian clock. Science, 295(5557), 1070–1073.CrossRefGoogle ScholarPubMed
Besedovsky, L., Lange, T., & Haack, M. (2019). The sleep-immune crosstalk in health and disease. Physiol Rev, 99(3), 1325–1380.Google Scholar
Boone, D. R., Sell, S. L., Micci, M. A., Crookshanks, J. M., Parsley, M., Uchida, T., Prough, D. S., DeWitt, D. S., & Hellmich, H. L. (2012). Traumatic brain injury-induced dysregulation of the circadian clock. PLoS One, 7(10), e46204.Google Scholar
Boudreau, P., Yeh, W. H., Dumont, G. A., & Boivin, D. B. (2013). Circadian variation of heart rate variability across sleep stages. Sleep, 36(12), 1919–1928.CrossRefGoogle ScholarPubMed
Boyko, Y., Jennum, P., & Toft, P. (2017). Sleep quality and circadian rhythm disruption in the intensive care unit: A review. Nat Sci Sleep, 9, 277–284.Google Scholar
Brancaccio, M., Patton, A. P., Chesham, J. E., Maywood, E. S., & Hastings, M. H. (2017). Astrocytes control circadian timekeeping in the suprachiasmatic nucleus via glutamatergic signaling. Neuron, 93(6), 1420–1435.e1425.Google Scholar
Bruce, J. H., Norenberg, M. D., Kraydieh, S., Puckett, W., Marcillo, A., & Dietrich, D. (2000). Schwannosis: Role of gliosis and proteoglycan in human spinal cord injury. J Neurotrauma, 17(9), 781–788.CrossRefGoogle ScholarPubMed
Bumgarner, J. R., Walker, W. H., 2nd, & Nelson, R. J. (2021). Circadian rhythms and pain. Neurosci Biobehav Rev, 129, 296–306.Google Scholar
Bunten, D. C., Warner, A. L., Brunnemann, S. R., & Segal, J. L. (1998). Heart rate variability is altered following spinal cord injury. Clin Auton Res, 8(6), 329–334.Google Scholar
Cash, A., & Theus, M. H. (2020). Mechanisms of blood–brain barrier dysfunction in traumatic brain injury. Int J Mol Sci, 21(9), 3344.CrossRefGoogle ScholarPubMed
Celik, S., Oztekin, D., Akyolcu, N., & Işsever, H. (2005). Sleep disturbance: The patient care activities applied at the night shift in the intensive care unit. J Clin Nurs, 14(1), 102–106.CrossRefGoogle ScholarPubMed
Chavan, S. S., Pavlov, V. A., & Tracey, K. J. (2017). Mechanisms and therapeutic relevance of neuro-immune communication. Immunity, 46(6), 927–942.Google Scholar
Craig, A., Guest, R., Tran, Y., & Middleton, J. (2017). Cognitive impairment and mood states after spinal cord injury. J Neurotrauma, 34(6), 1156–1163.Google Scholar
Cregg, J. M., DePaul, M. A., Filous, A. R., Lang, B. T., Tran, A., & Silver, J. (2014). Functional regeneration beyond the glial scar. Exp Neurol, 253, 197–207.CrossRefGoogle ScholarPubMed
Dantzer, R., O’Connor, J. C., Freund, G. G., Johnson, R. W., & Kelley, K. W. (2008). From inflammation to sickness and depression: When the immune system subjugates the brain. Nat Rev Neurosci, 9(1), 46–56.Google Scholar
Daut, R. A., & Fonken, L. K. (2019). Circadian regulation of depression: A role for serotonin. Front Neuroendocrinol, 54, 100746.Google Scholar
David, S., & Kroner, A. (2011). Repertoire of microglial and macrophage responses after spinal cord injury. Nat Rev Neurosci, 12(7), 388–399.CrossRefGoogle ScholarPubMed
Deboer, T. (2020). Circadian regulation of sleep in mammals. Curr Opin Physiol, 15, 7.Google Scholar
Engwall, M., Fridh, I., Johansson, L., Bergbom, I., & Lindahl, B. (2015). Lighting, sleep and circadian rhythm: An intervention study in the intensive care unit. Intensive Crit Care Nurs, 31(6), 325–335.CrossRefGoogle ScholarPubMed
Everson, C. A., & Toth, L. A. (2000). Systemic bacterial invasion induced by sleep deprivation. Am J Physiol Regul Integr Comp Physiol, 278(4), R905–916.Google Scholar
Fatima, G., Sharma, V. P., & Verma, N. S. (2016). Circadian variations in melatonin and cortisol in patients with cervical spinal cord injury. Spinal Cord, 54(5), 364–367.Google Scholar
Faulkner, J. R., Herrmann, J. E., Woo, M. J., Tansey, K. E., Doan, N. B., & Sofroniew, M. V. (2004). Reactive astrocytes protect tissue and preserve function after spinal cord injury. J Neurosci, 24(9), 2143–2155.Google Scholar
Fitch, M. T., Doller, C., Combs, C. K., Landreth, G. E., & Silver, J. (1999). Cellular and molecular mechanisms of glial scarring and progressive cavitation: In vivo and in vitro analysis of inflammation-induced secondary injury after CNS trauma. J Neurosci, 19(19), 8182–8198.Google Scholar
Fleshner, M., & Crane, C. R. (2017). Exosomes, DAMPs and miRNA: Features of stress physiology and immune homeostasis. Trends Immunol, 38(10), 768–776.Google Scholar
Fonken, L. K., Bedrosian, T. A., Zhang, N., Weil, Z. M., DeVries, A. C., & Nelson, R. J. (2019). Dim light at night impairs recovery from global cerebral ischemia. Exp Neurol, 317, 100–109.Google Scholar
Fonken, L. K., Frank, M. G., Gaudet, A. D., D’Angelo, H. M., Daut, R. A., Hampson, E. C., Ayala, M. T., Watkins, L. R., & Maier, S. F. (2018). Neuroinflammatory priming to stress is differentially regulated in male and female rats. Brain Behav Immun, 70, 257–267.Google Scholar
Fonken, L. K., Frank, M. G., Kitt, M. M., Barrientos, R. M., Watkins, L. R., & Maier, S. F. (2015). Microglia inflammatory responses are controlled by an intrinsic circadian clock. Brain Behav Immun, 45, 171–179.Google Scholar
Fonken, L. K., Kitt, M. M., Gaudet, A. D., Barrientos, R. M., Watkins, L. R., & Maier, S. F. (2016). Diminished circadian rhythms in hippocampal microglia may contribute to age-related neuroinflammatory sensitization. Neurobiol Aging, 47, 102–112.Google Scholar
Frank, M. G., Weber, M. D., Watkins, L. R., & Maier, S. F. (2015). Stress sounds the alarmin: The role of the danger-associated molecular pattern HMGB1 in stress-induced neuroinflammatory priming. Brain Behav Immun, 48, 1–7.CrossRefGoogle ScholarPubMed
Friese, R. S., Bruns, B., & Sinton, C. M. (2009). Sleep deprivation after septic insult increases mortality independent of age. J Trauma, 66(1), 50–54.Google Scholar
Gaudet, A. D., & Fonken, L. K. (2018). Glial cells shape pathology and repair after spinal cord injury. Neurotherapeutics, 15(3), 554–577.Google Scholar
Gaudet, A. D., Fonken, L. K., Ayala, M. T., Bateman, E. M., Schleicher, W. E., Smith, E. J., D’Angelo, H. M., Maier, S. F., & Watkins, L. R. (2018). Spinal cord injury in rats disrupts the circadian system. eNeuro, 5(6).CrossRefGoogle ScholarPubMed
Gaudet, A. D., Fonken, L. K., Ayala, M. T., Dangelo, H. M., Smith, E. J., Bateman, E. M., Schleicher, W. E., Maier, S. F., & Watkins, L. R. (2019). Spinal cord injury in rats dysregulates diurnal rhythms of fecal output and liver metabolic indicators. J Neurotrauma, 36(12), 1923–1934.CrossRefGoogle ScholarPubMed
Gaudet, A. D., Fonken, L. K., Watkins, L. R., Nelson, R. J., & Popovich, P. G. (2018). MicroRNAs: Roles in regulating neuroinflammation. Neuroscientist, 24(3), 221–245.Google Scholar
Gaudet, A. D., Mandrekar-Colucci, S., Hall, J. C., Sweet, D. R., Schmitt, P. J., Xu, X., Guan, Z., Mo, X., Guerau-de-Arellano, M., & Popovich, P. G. (2016). miR-155 deletion in mice overcomes neuron-intrinsic and neuron-extrinsic barriers to spinal cord repair. J Neurosci, 36(32), 8516–8532.Google Scholar
Gazendam, J. A. C., Van Dongen, H. P. A., Grant, D. A., Freedman, N. S., Zwaveling, J. H., & Schwab, R. J. (2013). Altered circadian rhythmicity in patients in the ICU. Chest, 144(2), 483–489.Google Scholar
Gensel, J. C., Nakamura, S., Guan, Z., van Rooijen, N., Ankeny, D. P., & Popovich, P. G. (2009). Macrophages promote axon regeneration with concurrent neurotoxicity. J Neurosci, 29(12), 3956–3968.CrossRefGoogle ScholarPubMed
Gibbs, J. E., Blaikley, J., Beesley, S., Matthews, L., Simpson, K. D., Boyce, S. H., Farrow, S. N., Else, K. J., Singh, D., Ray, D. W., & Loudon, A. S. (2012). The nuclear receptor REV-ERBalpha mediates circadian regulation of innate immunity through selective regulation of inflammatory cytokines. Proc Natl Acad Sci USA, 109(2), 582–587.Google Scholar
Goritz, C., Dias, D. O., Tomilin, N., Barbacid, M., Shupliakov, O., & Frisen, J. (2011). A pericyte origin of spinal cord scar tissue. Science, 333(6039), 238–242.Google Scholar
Greenhalgh, A. D., & David, S. (2014). Differences in the phagocytic response of microglia and peripheral macrophages after spinal cord injury and its effects on cell death. J Neurosci, 34(18), 6316–6322.CrossRefGoogle ScholarPubMed
Griffin, P., Dimitry, J. M., Sheehan, P. W., Lananna, B. V., Guo, C., Robinette, M. L., Hayes, M. E., Cedeño, M. R., Nadarajah, C. J., Ezerskiy, L. A., Colonna, M., Zhang, J., Bauer, A. Q., Burris, T. P., & Musiek, E. S. (2019). Circadian clock protein Rev-erbα regulates neuroinflammation. Proc Natl Acad Sci USA, 116(11), 5102–5107.CrossRefGoogle ScholarPubMed
Guillaumond, F., Dardente, H., Giguère, V., & Cermakian, N. (2005). Differential control of Bmal1 circadian transcription by REV-ERB and ROR nuclear receptors. J Biol Rhythms, 20(5), 391–403.Google Scholar
Habgood, M. D., Bye, N., Dziegielewska, K. M., Ek, C. J., Lane, M. A., Potter, A., Morganti-Kossmann, C., & Saunders, N. R. (2007). Changes in blood-brain barrier permeability to large and small molecules following traumatic brain injury in mice. Eur J Neurosci, 25(1), 231–238.Google Scholar
Hablitz, L. M., Plá, V., Giannetto, M., Vinitsky, H. S., Stæger, F. F., Metcalfe, T., Nguyen, R., Benrais, A., & Nedergaard, M. (2020). Circadian control of brain glymphatic and lymphatic fluid flow. Nat Commun, 11(1), 4411.Google Scholar
Halberg, F., Johnson, E. A., Brown, B. W., & Bittner, J. J. (1960). Susceptibility rhythm to E. coli endotoxin and bioassay. Proc Soc Exp Biol Med, 103, 142–144.Google Scholar
Hannon, M. J., Crowley, R. K., Behan, L. A., O’Sullivan, E. P., O’Brien, M. M. C., Sherlock, M., Rawluk, D., O’Dwyer, R., Tormey, W., & Thompson, C. J. (2013). Acute glucocorticoid deficiency and diabetes insipidus are common after acute traumatic brain injury and predict mortality. J Clin Endocrinol Metab, 98(8), 3229–3237.CrossRefGoogle ScholarPubMed
Hastings Hagenauer, M., Crodelle, J. A., Piltz, S. H., Toporikova, N., Ferguson, P., & Booth, V. (2017). The modulation of pain by circadian and sleep-dependent processes: A review of the experimental evidence. In Layton, A., & Miller, L. (eds.), Women in mathematical biology. Association for women in mathematics series (Vol. 8, pp. 1–22). Cham: Springer.Google Scholar
Hattar, S., Kumar, M., Park, A., Tong, P., Tung, J., Yau, K. W., & Berson, D. M. (2006). Central projections of melanopsin-expressing retinal ganglion cells in the mouse. J Comp Neurol, 497(3), 326–349.Google Scholar
He, W., Holtkamp, S., Hergenhan, S. M., Kraus, K., de Juan, A., Weber, J., Bradfield, P., Grenier, J. M. P., Pelletier, J., Drudz, D., Chen, C.-S., Ince, L. M., Bierschenk, S., Pick, R., Sperandio, M., Aurrand-Lions, M., & Scheiermann, C. (2018). Circadian expression of migratory factors establishes lineage-specific signatures that guide the homing of leukocyte subsets to tissues. Immunity, 49(6), 1175–1190.e1177.Google Scholar
Hilton, G. D., Stoica, B. A., Byrnes, K. R., & Faden, A. I. (2008). Roscovitine reduces neuronal loss, glial activation, and neurologic deficits after brain trauma. J Cereb Blood Flow Metab, 28(11), 1845–1859.CrossRefGoogle ScholarPubMed
Hou, J., Shen, Q., Wan, X., Zhao, B., Wu, Y., & Xia, Z. (2019). REM sleep deprivation-induced circadian clock gene abnormalities participate in hippocampal-dependent memory impairment by enhancing inflammation in rats undergoing sevoflurane inhalation. Behav Brain Res, 364, 167–176.Google Scholar
Huang, S., Choi, M. H., Huang, H., Wang, X., Chang, Y. C., & Kim, J. Y. (2020). Demyelination regulates the circadian transcription factor BMAL1 to signal adult neural stem cells to initiate oligodendrogenesis. Cell Rep, 33(7), 108394.Google Scholar
Hultén, V. D. T., Biering-Sørensen, F., Jørgensen, N. R., & Jennum, P. J. (2020). A review of sleep research in patients with spinal cord injury. J Spinal Cord Med, 43(6), 775–796.Google Scholar
Iliff, J. J., Wang, M., Zeppenfeld, D. M., Venkataraman, A., Plog, B. A., Liao, Y., Deane, R., & Nedergaard, M. (2013). Cerebral arterial pulsation drives paravascular CSF-interstitial fluid exchange in the murine brain. J Neurosci, 33(46), 18190–18199.Google Scholar
Irwin, M., Thompson, J., Miller, C., Gillin, J. C., & Ziegler, M. (1999). Effects of sleep and sleep deprivation on catecholamine and interleukin-2 levels in humans: Clinical implications. J Clin Endocrinol Metab, 84(6), 1979–1985.Google Scholar
Irwin, M. R. (2019). Sleep and inflammation: partners in sickness and in health. Nat Rev Immunol, 19(11), 702–715.CrossRefGoogle ScholarPubMed
Iwasaki, A., & Medzhitov, R. (2015). Control of adaptive immunity by the innate immune system. Nat Immunol, 16(4), 343–353.Google Scholar
Jang, H. J., Park, J., & Shin, H. I. (2011). Length of hospital stay in patients with spinal cord injury. Ann Rehabil Med, 35(6), 798–806.Google Scholar
Jensen, M. P., Hirsh, A. T., Molton, I. R., & Bamer, A. M. (2009). Sleep problems in individuals with spinal cord injury: frequency and age effects. Rehabil Psychol, 54(3), 323–331.CrossRefGoogle ScholarPubMed
Kierdorf, K., Masuda, T., Jordão, M. J. C., & Prinz, M. (2019). Macrophages at CNS interfaces: Ontogeny and function in health and disease. Nat Rev Neurosci, 20(9), 547–562.Google Scholar
Kigerl, K. A., de Rivero Vaccari, J. P., Dietrich, W. D., Popovich, P. G., & Keane, R. W. (2014). Pattern recognition receptors and central nervous system repair. Exp Neurol, 258, 5–16.Google Scholar
Kigerl, K. A., Gensel, J. C., Ankeny, D. P., Alexander, J. K., Donnelly, D. J., & Popovich, P. G. (2009). Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J Neurosci, 29(43), 13435–13444.Google Scholar
Kim, Y., Kim, J., Ahn, M., & Shin, T. (2017). Lithium ameliorates rat spinal cord injury by suppressing glycogen synthase kinase-3β and activating heme oxygenase-1. Anat Cell Biol, 50(3), 207–213.Google Scholar
Koch, C. E., Leinweber, B., Drengberg, B. C., Blaum, C., & Oster, H. (2017). Interaction between circadian rhythms and stress. Neurobiol Stress, 6, 57–67.CrossRefGoogle ScholarPubMed
Kojetin, D. J., & Burris, T. P. (2014). REV-ERB and ROR nuclear receptors as drug targets. Nat Rev Drug Discov, 13(3), 197–216.Google Scholar
Krassioukov, A., & Claydon, V. E. (2006). The clinical problems in cardiovascular control following spinal cord injury: An overview. Prog Brain Res, 152, 223–229.CrossRefGoogle ScholarPubMed
Lam, M. T., Cho, H., Lesch, H. P., Gosselin, D., Heinz, S., Tanaka-Oishi, Y., Benner, C., Kaikkonen, M. U., Kim, A. S., Kosaka, M., Lee, C. Y., Watt, A., Grossman, T. R., Rosenfeld, M. G., Evans, R. M., & Glass, C. K. (2013). Rev-Erbs repress macrophage gene expression by inhibiting enhancer-directed transcription. Nature, 498(7455), 511–515.Google Scholar
Lananna, B. V., Nadarajah, C. J., Izumo, M., Cedeño, M. R., Xiong, D. D., Dimitry, J., Tso, C. F., McKee, C. A., Griffin, P., Sheehan, P. W., Haspel, J. A., Barres, B. A., Liddelow, S. A., Takahashi, J. S., Karatsoreos, I. N., & Musiek, E. S. (2018). Cell-autonomous regulation of astrocyte activation by the circadian clock protein BMAL1. Cell Rep, 25(1), 1–9.e5.Google Scholar
Lange, T., Dimitrov, S., & Born, J. (2010). Effects of sleep and circadian rhythm on the human immune system. Ann NY Acad Sci, 1193, 48–59.CrossRefGoogle ScholarPubMed
Lee, K. Z. (2019). Impact of cervical spinal cord contusion on the breathing pattern across the sleep-wake cycle in the rat. J Appl Physiol, 126(1), 111–123.Google Scholar
Li, B., Li, D., Ni, H., Liu, C., Xiong, J., Liu, H., Gao, R., Zhang, L., & Chen, G. (2022). The circadian clock regulator Bmal1 affects traumatic brain injury in rats through the p38 MAPK signalling pathway. Brain Res Bull, 178, 17–28.CrossRefGoogle ScholarPubMed
Li, D., Ma, S., Guo, D., Cheng, T., Li, H., Tian, Y., Li, J., Guan, F., Yang, B., & Wang, J. (2016). Environmental circadian disruption worsens neurologic impairment and inhibits hippocampal neurogenesis in adult rats after traumatic brain injury. Cell Mol Neurobiol, 36(7), 1045–1055.CrossRefGoogle ScholarPubMed
Li, S. Y., Wang, T. J., Wu, S. F. V., Liang, S. Y., & Tung, H. H. (2011). Efficacy of controlling night-time noise and activities to improve patients’ sleep quality in a surgical intensive care unit. J Clin Nurs, 20(3–4), 396–407.Google Scholar
Loane, D. J., Stoica, B. A., & Faden, A. I. (2015). Neuroprotection for traumatic brain injury. Handb Clin Neurol, 127, 343–366.Google Scholar
Logan, R. W., & McClung, C. A. (2019). Rhythms of life: Circadian disruption and brain disorders across the lifespan. Nat Rev Neurosci, 20(1), 49–65.Google Scholar
Logan, R. W., & Sarkar, D. K. (2012). Circadian nature of immune function. Mol Cell Endocrinol, 349(1), 82–90.Google Scholar
Lucin, K. M., Sanders, V. M., Jones, T. B., Malarkey, W. B., & Popovich, P. G. (2007). Impaired antibody synthesis after spinal cord injury is level dependent and is due to sympathetic nervous system dysregulation. Exp Neurol, 207(1), 75–84.Google Scholar
Ma, H., Zhong, W., Jiang, Y., Fontaine, C., Li, S., Fu, J., Olkkonen, V. M., Staels, B., & Yan, D. (2013). Increased atherosclerotic lesions in LDL receptor deficient mice with hematopoietic nuclear receptor Rev-erbα knock-down. J Am Heart Assoc, 2(4), e000235.CrossRefGoogle ScholarPubMed
Marchetti, L., & Engelhardt, B. (2020). Immune cell trafficking across the blood–brain barrier in the absence and presence of neuroinflammation. Vasc Biol, 2(1), H1–H18.CrossRefGoogle ScholarPubMed
Marpegan, L., Swanstrom, A. E., Chung, K., Simon, T., Haydon, P. G., Khan, S. K., Liu, A. C., Herzog, E. D., & Beaulé, C. (2011). Circadian regulation of ATP release in astrocytes. J Neurosci, 31(23), 8342–8350.Google Scholar
Mathias, J. L., & Alvaro, P. K. (2012). Prevalence of sleep disturbances, disorders, and problems following traumatic brain injury: A meta-analysis. Sleep Med, 13(7), 898–905.CrossRefGoogle ScholarPubMed
Mavroudis, P. D., DuBois, D. C., Almon, R. R., & Jusko, W. J. (2018). Modeling circadian variability of core-clock and clock-controlled genes in four tissues of the rat. PLoS One, 13(6), e0197534.Google Scholar
McCreedy, D. A., Lee, S., Sontag, C. J., Weinstein, P., Olivas, A. D., Martinez, A. F., Fandel, T. M., Trivedi, A., Lowell, C. A., Rosen, S. D., & Noble-Haeusslein, L. J. (2018). Early targeting of L-selectin on leukocytes promotes recovery after spinal cord injury, implicating novel mechanisms of pathogenesis. eNeuro, 5(4): ENEURO.0101-18.2018.CrossRefGoogle ScholarPubMed
McKee, C. A., Lananna, B. V., & Musiek, E. S. (2020). Circadian regulation of astrocyte function: implications for Alzheimer’s disease. Cell Mol Life Sci, 77(6), 1049–1058.Google Scholar
Medzhitov, R., & Janeway, C. Jr. (2000). Innate immunity. N Engl J Med, 343(5), 338–344.Google Scholar
Milich, L. M., Choi, J. S., Ryan, C., Cerqueira, S. R., Benavides, S., Yahn, S. L., Tsoulfas, P., & Lee, J. K. (2021). Single-cell analysis of the cellular heterogeneity and interactions in the injured mouse spinal cord. J Exp Med, 218(8), e20210040.CrossRefGoogle ScholarPubMed
Milich, L. M., Ryan, C. B., & Lee, J. K. (2019). The origin, fate, and contribution of macrophages to spinal cord injury pathology. Acta Neuropathol, 137(5), 785–797.Google Scholar
Miron, V. E., Boyd, A., Zhao, J. W., Yuen, T. J., Ruckh, J. M., Shadrach, J. L., van Wijngaarden, P., Wagers, A. J., Williams, A., Franklin, R. J. M., & Ffrench-Constant, C. (2013). M2 microglia and macrophages drive oligodendrocyte differentiation during CNS remyelination. Nat Neurosci, 16(9), 1211–1218.CrossRefGoogle ScholarPubMed
Mogensen, F. L., Delle, C., & Nedergaard, M. (2021). The glymphatic system (en)during inflammation. Int J Mol Sci, 22(14), 7491.Google Scholar
Moon, J. H., Cho, C. H., Son, G. H., Geum, D., Chung, S., Kim, H., Kang, S.-G., Park, Y.-M., Yoon, H.-K., Kim, L., Jee, H.-J., An, H., Kripke, D. F., & Lee, H. J. (2016). Advanced circadian phase in mania and delayed circadian phase in mixed mania and depression returned to normal after treatment of bipolar disorder. EBioMedicine, 11, 285–295.Google Scholar
Moore, R. Y., & Qavi, H. B. (1971). Circadian rhythm in adrenal adenyl cyclase and corticosterone abolished by medial forebrain bundle transection in the rat. Experientia, 27(3), 249–250.Google Scholar
Musiek, E. S., Lim, M. M., Yang, G., Bauer, A. Q., Qi, L., Lee, Y., Roh, J. H., Ortiz-Gonzalez, X., Dearborn, J. T., Culver, J. P., Herzog, E. D., Hogenesch, J. B., Wozniak, D. F., Dikranian, K., Giasson, B. I., Weaver, D. R., Holtzman, D. M., & Fitzgerald, G. A. (2013). Circadian clock proteins regulate neuronal redox homeostasis and neurodegeneration. J Clin Invest, 123(12), 5389–5400.Google Scholar
Nimmerjahn, A., Kirchhoff, F., & Helmchen, F. (2005). Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science, 308(5726), 1314–1318.Google Scholar
Norton, L. (2010). Spinal cord injury, Australia 2007–08. (Cat. no. INJCAT 128). Canberra: AIHW.Google Scholar
NSCISC. (2021). National Spinal Cord Injury Statistical Center, facts and figures at a glance. Report, University of Alabama at Birmingham. Available at: www.nscisc.uab.edu/Public/Facts%20and%20Figures%202020.pdf.Google Scholar
Ooms, S., Overeem, S., Besse, K., Rikkert, M. O., Verbeek, M., & Claassen, J. A. (2014). Effect of 1 night of total sleep deprivation on cerebrospinal fluid β-amyloid 42 in healthy middle-aged men: A randomized clinical trial. JAMA Neurol, 71(8), 971–977.Google Scholar
Opp, M. R. (2005). Cytokines and sleep. Sleep Med Rev, 9(5), 355–364.Google Scholar
Perkes, I., Baguley, I. J., Nott, M. T., & Menon, D. K. (2010). A review of paroxysmal sympathetic hyperactivity after acquired brain injury. Ann Neurol, 68(2), 126–135.Google Scholar
Pineau, I., Sun, L., Bastien, D., & Lacroix, S. (2010). Astrocytes initiate inflammation in the injured mouse spinal cord by promoting the entry of neutrophils and inflammatory monocytes in an IL-1 receptor/MyD88-dependent fashion. Brain Behav Immun, 24(4), 540–553.Google Scholar
Plemel, J. R., Wee Yong, V., & Stirling, D. P. (2014). Immune modulatory therapies for spinal cord injury: Past, present and future. Exp Neurol, 258, 91–104.Google Scholar
Popovich, P. G., Guan, Z., Wei, P., Huitinga, I., van Rooijen, N., & Stokes, B. T. (1999). Depletion of hematogenous macrophages promotes partial hindlimb recovery and neuroanatomical repair after experimental spinal cord injury. Exp Neurol, 158(2), 351–365.CrossRefGoogle ScholarPubMed
Prolo, L. M., Takahashi, J. S., & Herzog, E. D. (2005). Circadian rhythm generation and entrainment in astrocytes. J Neurosci, 25(2), 404–408.Google Scholar
Provencio, I., Rollag, M. D., & Castrucci, A. M. (2002). Photoreceptive net in the mammalian retina. This mesh of cells may explain how some blind mice can still tell day from night. Nature, 415(6871), 493.Google Scholar
Purkayastha, S., Stokes, M., & Bell, K. R. (2019). Autonomic nervous system dysfunction in mild traumatic brain injury: A review of related pathophysiology and symptoms. Brain Inj, 33(9), 1129–1136.CrossRefGoogle ScholarPubMed
Ransohoff, R. M., & Brown, M. A. (2012). Innate immunity in the central nervous system. J Clin Invest, 122(4), 1164–1171.Google Scholar
Reddy, A. B., Maywood, E. S., Karp, N. A., King, V. M., Inoue, Y., Gonzalez, F. J., Lilley, K. S., Kyriacou, C. P., & Hastings, M. H. (2007). Glucocorticoid signaling synchronizes the liver circadian transcriptome. Hepatology, 45(6), 1478–1488.Google Scholar
Redwine, L., Hauger, R. L., Gillin, J. C., & Irwin, M. (2000). Effects of sleep and sleep deprivation on interleukin-6, growth hormone, cortisol, and melatonin levels in humans. J Clin Endocrinol Metab, 85(10), 3597–3603.Google Scholar
Reid, L.D., & Fingar, K.R. (2020). Healthcare Cost and Utilization Project (HCUP). Agency for Healthcare Research and Quality. Available at: www.hcup-us.ahrq.gov/reports/statbriefs/sb255-Traumatic-Brain-Injury-Hospitalizations-ED-Visits-2017.jsp (last accessed March 24, 2023).Google Scholar
Reitz, C. J., Alibhai, F. J., Khatua, T. N., Rasouli, M., Bridle, B. W., Burris, T. P., & Martino, T. A. (2019). SR9009 administered for one day after myocardial ischemia-reperfusion prevents heart failure in mice by targeting the cardiac inflammasome. Comm Biol, 2(1), 353.CrossRefGoogle ScholarPubMed
Ripperger, J. A. (2006). Mapping of binding regions for the circadian regulators BMAL1 and CLOCK within the mouse Rev-erbalpha gene. Chronobiol Int, 23(1–2), 135–142.Google Scholar
Roby, D. A., Ruiz, F., Kermath, B. A., Voorhees, J. R., Niehoff, M., Zhang, J., Morley, J. E., Musiek, E. S., Farr, S. A., & Burris, T. P. (2019). Pharmacological activation of the nuclear receptor REV-ERB reverses cognitive deficits and reduces amyloid-beta burden in a mouse model of Alzheimer’s disease. PLoS One, 14(4), e0215004.Google Scholar
Rowe, R. K., Harrison, J. L., O’Hara, B. F., & Lifshitz, J. (2014). Recovery of neurological function despite immediate sleep disruption following diffuse brain injury in the mouse: Clinical relevance to medically untreated concussion. Sleep, 37(4), 743–752.Google Scholar
Rowe, R. K., Rumney, B. M., May, H. G., Permana, P., Adelson, P. D., Harman, S. M., Lifshitz, J., & Thomas, T. C. (2016). Diffuse traumatic brain injury affects chronic corticosterone function in the rat. Endocr Connect, 5(4), 152–166.Google Scholar
Ruben, M. D., Francey, L. J., Guo, Y., Wu, G., Cooper, E. B., Shah, A. S., Hogenesch, J. B., & Smith, D. F. (2019). A large-scale study reveals 24-h operational rhythms in hospital treatment. Proc Natl Acad Sci USA, 116(42), 20953–20958.Google Scholar
Ruben, M. D., Smith, D. F., FitzGerald, G. A., & Hogenesch, J. B. (2019). Dosing time matters. Science, 365(6453), 547–549.Google Scholar
Saiwai, H., Ohkawa, Y., Yamada, H., Kumamaru, H., Harada, A., Okano, H., Yokomizo, T., Iwamoto, Y., & Okada, S. (2010). The LTB4-BLT1 axis mediates neutrophil infiltration and secondary injury in experimental spinal cord injury. Am J Pathol, 176(5), 2352–2366.Google Scholar
Sandsmark, D. K., Elliott, J. E., & Lim, M. M. (2017). Sleep–wake disturbances after traumatic brain injury: Synthesis of human and animal studies. Sleep, 40(5), zsx044.Google Scholar
Sankari, A., Badr, M. S., Martin, J. L., Ayas, N. T., & Berlowitz, D. J. (2019). Impact of spinal cord injury on sleep: Current perspectives. Nat Sci Sleep, 11, 219–229.Google Scholar
Scheer, F. A., Zeitzer, J. M., Ayas, N. T., Brown, R., Czeisler, C. A., & Shea, S. A. (2006). Reduced sleep efficiency in cervical spinal cord injury; association with abolished night time melatonin secretion. Spinal Cord, 44(2), 78–81.Google Scholar
Schibler, U., Gotic, I., Saini, C., Gos, P., Curie, T., Emmenegger, Y., Sinturel, F., Gosselin, P., Gerber, A., Fleury-Olela, F., Rando, G., Demarque, M., & Franken, P. (2015). Clock-talk: Interactions between central and peripheral circadian oscillators in mammals. Cold Spring Harb Symp Quant Biol, 80, 223–232.Google Scholar
Segal, J. P., Tresidder, K. A., Bhatt, C., Gilron, I., & Ghasemlou, N. (2018). Circadian control of pain and neuroinflammation. J Neurosci Res, 96(6), 1002–1020.Google Scholar
Sharma, K., Bisht, K., & Eyo, U. B. (2021). A comparative biology of microglia across species. Front Cell Dev Biol, 9, 652748.Google Scholar
Simpson, L. A., Eng, J. J., Hsieh, J. T., & Wolfe, D. L. (2012). The health and life priorities of individuals with spinal cord injury: A systematic review. J Neurotrauma, 29(8), 1548–1555.CrossRefGoogle ScholarPubMed
Slomnicki, L. P., Myers, S. A., Saraswat Ohri, S., Parsh, M. V., Andres, K. R., Chariker, J. H., Rouchka, E. C., Whittemore, S. R., & Hetman, M. (2020). Improved locomotor recovery after contusive spinal cord injury in Bmal1(-/-) mice is associated with protection of the blood spinal cord barrier. Sci Rep, 10(1), 14212.Google Scholar
Slovarp, L., Azuma, T., & Lapointe, L. (2012). The effect of traumatic brain injury on sustained attention and working memory. Brain Inj, 26(1), 48–57.Google Scholar
Sofroniew, M. V., & Vinters, H. V. (2010). Astrocytes: Biology and pathology. Acta Neuropathol, 119(1), 7–35.Google Scholar
Stubblefield, J. J., & Lechleiter, J. D. (2019). Time to target stroke: Examining the circadian system in stroke. Yale J Biol Med, 92(2), 349–357.Google Scholar
Tamburri, L. M., DiBrienza, R., Zozula, R., & Redeker, N. S. (2004). Nocturnal care interactions with patients in critical care units. Am J Crit Care, 13(2), 102–112.Google Scholar
Tardif, P. A., Moore, L., Boutin, A., Dufresne, P., Omar, M., Bourgeois, G., Bonaventure, P. L., Kuimi, B. L. B., & Turgeon, A. F. (2017). Hospital length of stay following admission for traumatic brain injury in a Canadian integrated trauma system: A retrospective multicenter cohort study. Injury, 48(1), 94–100.Google Scholar
Teo, W., Newton, M. J., & McGuigan, M. R. (2011). Circadian rhythms in exercise performance: Implications for hormonal and muscular adaptation. J Sports Sci Med, 10(4), 600–606.Google Scholar
Tripathi, R., & McTigue, D. M. (2007). Prominent oligodendrocyte genesis along the border of spinal contusion lesions. Glia, 55(7), 698–711.Google Scholar
Trivedi, A., Tercovich, K. G., Casbon, A. J., Raber, J., Lowell, C., & Noble-Haeusslein, L. J. (2021). Neutrophil-specific deletion of Syk results in recruitment-independent stabilization of the barrier and a long-term improvement in cognitive function after traumatic injury to the developing brain. Neurobiol Dis, 157, 105430.Google Scholar
Vethe, D., Scott, J., Engstrøm, M., Salvesen, Ø., Sand, T., Olsen, A., Morken, G., Heglum, H. S., Kjørstad, K., Faaland, P. M., Vestergaard, C. L., Langsrud, K., & Kallestad, H. (2021). The evening light environment in hospitals can be designed to produce less disruptive effects on the circadian system and improve sleep. Sleep, 44(3), zsaa194.Google Scholar
Wang, F., Chang, S., Li, J., Wang, D., Li, H., & He, X. (2021). Lithium alleviated spinal cord injury (SCI)-induced apoptosis and inflammation in rats via BDNF-AS/miR-9-5p axis. Cell Tissue Res, 384(2), 301–312.CrossRefGoogle ScholarPubMed
Webster, J. C., Oakley, R. H., Jewell, C. M., & Cidlowski, J. A. (2001). Proinflammatory cytokines regulate human glucocorticoid receptor gene expression and lead to the accumulation of the dominant negative beta isoform: A mechanism for the generation of glucocorticoid resistance. Proc Natl Acad Sci USA, 98(12), 6865–6870.CrossRefGoogle Scholar
Weil, Z. M., Fonken, L. K., Walker, W. H., 2nd, Bumgarner, J. R., Liu, J. A., Melendez-Fernandez, O. H., Zhang, N., DeVries, A. C., & Nelson, R. J. (2020). Dim light at night exacerbates stroke outcome. Eur J Neurosci, 52(9), 4139–4146.Google Scholar
Wickwire, E. M., Albrecht, J. S., Capaldi, V. F., 2nd, Jain, S. O., Gardner, R. C., Werner, J. K., Mukherjee, P., McKeon, A. B., Smith, M. T., Giacino, J. T., Nelson, L. D., Williams, S. G., Collen, J., Sun, X., Schnyer, D. M., Markowitz, A. J., Manley, G. T., Krystal, A. D., & Transforming Research and Clinical Knowledge in Traumatic Brain Injury (TRACK-TBI) Investigators. (2022). Trajectories of insomnia in adults after traumatic brain injury. JAMA Netw Open, 5(1), e2145310.Google Scholar
Yamakawa, G. R., Brady, R. D., Sun, M., McDonald, S. J., Shultz, S. R., & Mychasiuk, R. (2020). The interaction of the circadian and immune system: Desynchrony as a pathological outcome to traumatic brain injury. Neurobiol Sleep Circadian Rhythms, 9, 100058.Google Scholar
Yin, L., Wang, J., Klein, P. S., & Lazar, M. A. (2006). Nuclear receptor Rev-erbα is a critical lithium-sensitive component of the circadian clock. Science, 311(5763), 1002–1005.Google Scholar
Zeitzer, J. M., Ayas, N. T., Shea, S. A., Brown, R., & Czeisler, C. A. (2000). Absence of detectable melatonin and preservation of cortisol and thyrotropin rhythms in tetraplegia. J Clin Endocrinol Metab, 85(6), 2189–2196.Google Scholar
Zhang, E. E., & Kay, S. A. (2010). Clocks not winding down: Unravelling circadian networks. Nat Rev Mol Cell Biol, 11(11), 764–776.Google Scholar
Zhao, X., Hirota, T., Han, X., Cho, H., Chong, L. W., Lamia, K., Liu, S., Atkins, A. R., Banayo, E., Liddle, C., Yu, R. T., Yates, J. R., Kay, S. A., Downes, M., & Evans, R. M. (2016). Circadian amplitude regulation via FBXW7-targeted REV-ERBα degradation. Cell, 165(7), 1644–1657.Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×