Hostname: page-component-8448b6f56d-wq2xx Total loading time: 0 Render date: 2024-04-23T12:43:27.870Z Has data issue: false hasContentIssue false
  • English
  • Français

Sleep Deprivation Impairs Ca2+ Expression in the Hippocampus: Ionic Imaging Analysis for Cognitive Deficiency with TOF-SIMS

Published online by Cambridge University Press:  12 April 2012

Hung-Ming Chang ,
Wen-Chieh Liao ,
Ji-Nan Sheu ,
Chun-Chao Chang ,
Chyn-Tair Lan  and
Fu-Der Mai
Hung-Ming Chang
Affiliation:
Department of Anatomy, Faculty of Medicine, Chung Shan Medical University, Taichung 402, Taiwan Department of Pediatrics, Chung Shan Medical University Hospital, Taichung 402, Taiwan
Wen-Chieh Liao
Affiliation:
Department of Anatomy, Faculty of Medicine, Chung Shan Medical University, Taichung 402, Taiwan
Ji-Nan Sheu
Affiliation:
Department of Pediatrics, Chung Shan Medical University Hospital, Taichung 402, Taiwan
Chun-Chao Chang
Affiliation:
Department of Internal Medicine, Taipei Medical University Hospital, Taipei 110, Taiwan
Chyn-Tair Lan
Affiliation:
Department of Anatomy, Faculty of Medicine, Chung Shan Medical University, Taichung 402, Taiwan
Fu-Der Mai*
Affiliation:
Department of Biochemistry, School of Medicine, Taipei Medical University, Taipei 110, Taiwan Biomedical Mass Imaging Research Center, Taipei Medical University, Taipei 110, Taiwan
*
Corresponding author. E-mail: fordmai@tmu.edu.tw
Get access

Abstract

Sleep deprivation causes cognitive dysfunction in which impaired neuronal plasticity in hippocampus may underlie the molecular mechanisms of this deficiency. Considering calcium-mediated NMDA receptor subunit 1 (NMDAR1) and neuronal nitric oxide synthase (nNOS) activation plays an important role in the regulation of neuronal plasticity, the present study is aimed to determine whether total sleep deprivation (TSD) would impair calcium expression, together with injury of the neuronal plasticity in hippocampus. Adult rats subjected to TSD were processed for time-of-flight secondary ion mass spectrometry, NMDAR1 immunohistochemistry, nNOS biochemical assay, cytochrome oxidase histochemistry, and the Morris water maze learning test to detect ionic, neurochemical, bioenergetic as well as behavioral changes of neuronal plasticity, respectively. Results indicated that in normal rats, strong calcium signaling along with intense NMDAR1/nNOS expression were observed in hippocampal regions. Enhanced calcium imaging and neurochemical expressions corresponded well with strong bioenergetic activity and good performance of behavioral testing. However, following TSD, both calcium intensity and NMDAR1/nNOS expressions were significantly decreased. Behavioral testing also showed poor responses after TSD. As proper calcium expression is essential for maintaining hippocampal neuronal plasticity, impaired calcium expression would depress downstream NMDAR1-mediated nNOS activation, which might contribute to the initiation or development of TSD-related cognitive deficiency.

Keywords

cognitive functionlong-term potentiationionic imagingquantitative immunohistochemistrysleep deprivationTOF-SIMS
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 18 , Issue 3 , June 2012 , pp. 425 - 435
Copyright
Copyright © Microscopy Society of America 2012

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

Belu, A.M., Graham, D.J. & Castner, D.G. (2003). Time-of-flight secondary ion mass spectrometry: Techniques and applications for the characterization of biomaterial surfaces. Biomaterials 24, 3635–3653.CrossRefGoogle Scholar
Bergmann, B.M., Kushida, C.A., Everson, C.A., Gilliland, M.A., Obermeyer, W. & Rechtschaffen, A. (1989). Sleep deprivation in the rat: II. Methodology. Sleep 12, 5–12.Google Scholar
Billard, J.M. (2006). Ageing, hippocampal synaptic plasticity and magnesium. Magnesium Res 19, 199–215.Google Scholar
Carafoli, E. & Klee, C. (1999). Calcium as a Cellular Regulator. New York: Oxford University Press.Google Scholar
Chang, H.M., Chen, B.J., Wu, U.I., Huang, Y.L. & Mai, F.D. (2008a). Molecular imaging of enhanced Na+ expression in the liver of total sleep deprived rats by TOF-SIMS. Appl Surf Sci 255, 1131–1134.Google Scholar
Chang, H.M., Mai, F.D., Chen, B.J., Wu, U.I., Huang, Y.L., Lan, C.T. & Ling, Y.C. (2008b). Sleep deprivation predisposes liver to oxidative stress and phospholipid damage—A quantitative molecular imaging study. J Anat 212, 295–305.Google Scholar
Chang, H.M., Mai, F.D., Lei, S.L. & Ling, Y.C. (2010). Impaired sodium levels in the suprachiasmatic nucleus are associated with the formation of cardiovascular deficiency in sleep-deprived rats. J Anat 217, 694–704.Google Scholar
Chang, H.M., Tseng, C.Y., Wei, I.H., Lue, J.H., Wen, C.Y. & Shieh, J.Y. (2005). Melatonin restores the cytochrome oxidase reactivity in the nodose ganglia of acute hypoxic rats. J Pineal Res 39, 206–214.CrossRefGoogle ScholarPubMed
Chang, H.M., Wu, U.I. & Lan, C.T. (2009). Melatonin preserves longevity protein (sirtuin 1) expression in the hippocampus of total sleep-deprived rats. J Pineal Res 47, 211–220.CrossRefGoogle ScholarPubMed
Chang, H.M., Wu, U.I., Lin, T.B., Lan, C.T., Chien, W.C., Huang, W.L. & Shieh, J.Y. (2006). Total sleep deprivation inhibits the neuronal nitric oxide synthase and cytochrome oxidase reactivities in the nodose ganglion of adult rats. J Anat 209, 239–250.Google Scholar
Chee, M.W. & Chuah, L.Y. (2008). Functional neuroimaging insights into how sleep and sleep deprivation affect memory and cognition. Curr Opin Neurol 21, 417–423.Google Scholar
Chee, M.W., Chuah, L.Y., Venkatraman, V., Chan, W.Y., Philip, P. & Dinges, D.F. (2006). Functional imaging of working memory following normal sleep and after 24 and 35 h of sleep deprivation: Correlations of fronto-parietal activation with performance. Neuroimage 31, 419–428.Google Scholar
Chen, C., Hardy, M., Zhang, J., LaHoste, G.J. & Bazan, N.G. (2006). Altered NMDA receptor trafficking contributes to sleep deprivation-induced hippocampal synaptic and cognitive impairments. Biochem Biophys Res Commun 340, 435–440.Google Scholar
Colrain, I.M. (2011). Sleep and the brain. Neuropsychol Rev 21, 1–4.Google Scholar
Copinschi, G. (2005). Metabolic and endocrine effects of sleep deprivation. Essent Psychopharmacol 6, 341–347.Google Scholar
D'almeida, V., Hipólide, D.C., Raymond, R., Barlow, K.B., Parkes, J.H., Pedrazzoli, M., Tufik, S. & Nobrega, J.N. (2005). Opposite effects of sleep rebound on orexin OX1 and OX2 receptor expression in rat brain. Brain Res Mol Brain Res 136, 148–157.Google Scholar
Easom, R.A., Tarpley, J.L., Filler, N.R. & Bhatt, H. (1998). Dephosphorylation and deactivation of Ca2+/calmodulin-dependent protein kinase II in betaTC3-cells is mediated by Mg2+ and okadaic-acid-sensitive protein phosphatases. Biochem J 329, 283–288.Google Scholar
Forest, G. & Godbout, R. (2000). Effects of sleep deprivation on performance and EEG spectral analysis in young adults. Brain Cogn 43, 195–200.Google Scholar
Hawkins, R.D., Son, H. & Arancio, O. (1998). Nitric oxide as a retrograde messenger during long-term potentiation in hippocampus. Prog Brain Res 118, 155–172.Google Scholar
Hsu, K.S., Ho, W.C., Huang, C. & Tsai, J.J. (2000). Transient removal of extracellular Mg2+ elicits persistent suppression of LTP at hippocampal CA1 synapses via PKC activation. J Neurophysiol 84, 1279–1288.Google Scholar
Iannuzzelli, P.G., Wang, X.H., Wang, Y. & Murphy, E.H. (1994). Axotomy-induced changes in cytochrome oxidase activity in the cat trochlear nucleus. Brain Res 637, 267–272.CrossRefGoogle ScholarPubMed
Ichikawa, H. & Helke, C.J. (1992). Cytochrome oxidase activity in vagal and glossopharyngeal visceral sensory neurons of the rat: Effect of peripheral axotomy. Brain Res 578, 311–316.Google Scholar
Ikegami, K., Ogyu, S., Arakomo, Y., Suzuki, K., Mafune, K., Hiro, H. & Nagata, S. (2009). Recovery of cognitive performance and fatigue after one night of sleep deprivation. J Occup Health 51, 412–422.CrossRefGoogle ScholarPubMed
Killgore, W.D. (2010). Effects of sleep deprivation on cognition. Prog Brain Res 185, 105–129.Google Scholar
Kim, J.H., Kim, J.H., Ahn, B.J., Park, J.H., Shon, H.K., Yu, Y.S., Moon, D.W., Lee, T.G. & Kim, K.W. (2008). Label-free calcium imaging in ischemic retinal tissue by TOF-SIMS. Biophys J 94, 4095–4102.Google Scholar
Kopp, C., Longordo, F., Nicholson, J.R. & Lüthi, A. (2006). Insufficient sleep reversibly alters bidirectional synaptic plasticity and NMDA receptor function. J Neurosci 26, 12456–12465.Google Scholar
LaManna, J.C., Kutina-Nelson, K.L., Hritz, M.A., Huang, Z. & Wong-Riley, M.T.T. (1996). Decreased rat brain cytochrome oxidase activity after prolonged hypoxia. Brain Res 720, 1–6.CrossRefGoogle ScholarPubMed
Landfield, P.W. & Morgan, G.A. (1984). Chronically elevating plasma Mg2+ improves hippocampal frequency potentiation and reversal learning in aged and young rats. Brain Res 322, 167–171.CrossRefGoogle ScholarPubMed
Louin, G., Besson, V.C., Royo, N.C., Bonnefont-Rousselot, D., Marchand-Verrecchia, C., Plotkine, M. & Jafarian-Tehrani, M. (2004). Cortical calcium increase following traumatic brain injury represents a pitfall in the evaluation of Ca2+-independent NOS activity. J Neurosci Methods 138, 73–79.CrossRefGoogle ScholarPubMed
MacDonald, J.F., Jackson, M.F. & Beazely, M.A. (2006). Hippocampal long-term synaptic plasticity and signal amplification of NMDA receptors. Crit Rev Neurobiol 18, 71–84.Google Scholar
Mai, F.D., Chen, L.Y., Ling, Y.C., Chen, B.J., Wu, U.I. & Chang, H.M. (2010). Molecular imaging of in vivo calcium ion expression in area postrema of total sleep deprived rats: Implications for cardiovascular regulation by TOF-SIMS analysis. Appl Surf Sci 256, 4456–4461.Google Scholar
Malmberg, P., Jennische, E., Nilsson, D. & Nygren, H. (2011). High-resolution, imaging TOF-SIMS: Novel applications in medical research. Anal Bioanal Chem 399, 2711–2718.Google Scholar
Matynia, A., Kushner, S.A. & Silva, A.J. (2002). Genetic approaches to molecular and cellular cognition: A focus on LTP and learning and memory. Annu Rev Genet 36, 687–720.Google Scholar
McEwen, B.S. (2006). Sleep deprivation as a neurobiological and physiological stressor: Allostasis and allostatic load. Metabolism 55, S20–S23.Google Scholar
McGown, A.D., Makker, H., Elwell, C., Al Rawi, P.G., Valipour, A. & Spiro, S.G. (2003). Measurement of changes in cytochrome oxidase redox state during obstructive sleep apnea using near-infrared spectroscopy. Sleep 26, 710–716.CrossRefGoogle ScholarPubMed
Miyamoto, E. (2006). Molecular mechanism of neuronal plasticity: Induction and maintenance of long-term potentiation in the hippocampus. J Pharmacol Sci 100, 433–442.Google Scholar
Morris, R.G., Garrud, P., Rawlins, J.N. & O'Keefe, J. (1982). Place navigation impaired in rats with hippocampal lesions. Nature 297, 681–683.Google Scholar
NIH (1985). Guide for the Care and Use of Laboratory Animals. NIH Pub. No. 86-23. Bethesda, MD: National Institutes of Health.Google Scholar
Peigneux, P., Laureys, S., Delbeuck, X. & Maquet, P. (2001). Sleeping brain, learning brain. The role of sleep for memory systems. Neuroreport 12, A111–A124.Google Scholar
Potier, B., Jouvenceau, A., Poindessous-Jazat, F., Dutar, P. & Billard, J.M. (1999). Modulation of the NMDA receptor by magnesium: Comparison in young and aged rats. Soc Neurosci Abst 25, 68220.Google Scholar
Rechtschaffen, A. (1998). Current perspectives on the function of sleep. Perspect Biol Med 41, 359–390.Google Scholar
Smolen, A.J. (1990). Image analytic techniques for quantification of immuno-histochemical staining in the nervous system. In Methods in Neuroscience: Quantitative and Qualitative Microscopy, Conn, P.M. (Ed.), pp. 208–229. San Diego, CA: Academic Press.Google Scholar
Süer, C., Dolu, N., Artis, A.S., Sahin, L., Yilmaz, A. & Cetin, A. (2011). The effects of long-term sleep deprivation on the long-term potentiation in the dentate gyrus and brain oxidation status in rats. Neurosci Res 70, 71–77.Google Scholar
Tartar, J.L., Ward, C.P., McKenna, J.T., Thakkar, M., Arrigoni, E., McCarley, R.W., Brown, R.E. & Strecker, R.E. (2006). Hippocampal synaptic plasticity and spatial learning are impaired in a rat model of sleep fragmentation. Eur J Neurosci 23, 2739–2748.Google Scholar
Vandewalle, G., Archer, S.N., Wuillaume, C., Balteau, E., Degueldre, C., Luxen, A., Maquet, P. & Dijk, D.J. (2009). Functional magnetic resonance imaging-assessed brain responses during an executive task depend on interaction of sleep homeostasis, circadian phase, and PER3 genotype. J Neurosci 29, 7948–7956.Google Scholar
Vogel, D.D. (2005). A neural network model of memory and higher cognitive functions. Int J Psychophysiol 55, 3–21.Google Scholar
Walker, M.P. (2008). Cognitive consequences of sleep and sleep loss. Sleep Med 9(Suppl 1), S29–S34.Google Scholar
Walker, M.P. & Stickgold, R. (2004). Sleep-dependent learning and memory consolidation. Neuron 44, 121–133.Google Scholar
Wang, S.H. & Morris, R.G. (2010). Hippocampal-neocortical interactions in memory formation, consolidation, and reconsolidation. Annu Rev Psychol 61, 49–79.CrossRefGoogle ScholarPubMed
Wong-Riley, M.T.T. (1989). Cytochrome oxidase: An endogenous metabolic marker for neuronal activity. Trends Neurosci 12, 94–101.Google Scholar
Wong-Riley, M.T.T. & Welt, C. (1980). Histochemical changes in cytochrome oxidase of cortical barrels after vibrissal removal in neonatal and adult mice. Proc Natl Acad Sci USA 77, 2333–2337.Google Scholar
Wu, U.I., Mai, F.D., Sheu, J.N., Chen, L.Y., Liu, Y.T., Huang, H.C. & Chang, H.M. (2011). Melatonin inhibits microglial activation, reduces pro-inflammatory cytokine levels, and rescues hippocampal neurons of adult rats with acute Klebsiella pneumoniae meningitis. J Pineal Res 50, 159–170.CrossRefGoogle ScholarPubMed
Yang, R.H., Hou, X.H., Xu, X.N., Zhang, L., Shi, J.N., Wang, F., Hu, S.J. & Chen, J.Y. (2011). Sleep deprivation impairs spatial learning and modifies the hippocampal theta rhythm in rats. Neuroscience 173, 116–123.Google Scholar