Selective deprivation of rapid eye movement (REM) sleep for 24 h does not modify the c-Fos immunoreactivity in the Ventral Respiratory Column (VRC) of rat
Resumen
La generación y modulación de la respiración es controlada por la columna respiratoria ventral (VRC), la cual incluye: el grupo respiratorio parafacial/núcleo retrotrapezoide (pFRG/RTN), el complejo Bötzinger (BötC) y el complejo preBötzinger (preBötC). Una correlación entre el sueño y la respiración es particularmente clara en condiciones como la apnea obstructiva del sueño y el síndrome de hipoventilación central congénita. En este trabajo, mediante la inmunoreactividad contra c-Fos como un marcador indirecto de la actividad neuronal, se estudió el efecto de la privación selectiva de sueño MOR a corto plazo sobre la actividad de las neuronas en la VRC. Ratas macho Wistar fueron divididas en dos grupos: control (n=6) y 24 h de privación selectiva de sueño MOR utilizando la técnica de florero invertido (n=11). La frecuencia respiratoria, la frecuencia cardíaca, la temperatura y la saturación de oxígeno (SpO2) se midieron antes y durante la privación de sueño MOR. El grupo de privación de sueño MOR no mostró diferencias estadísticamente significativas con respecto al grupo control. Sin embargo, la frecuencia cardíaca del grupo de privación de sueño MOR aumentó y la SpO2 disminuyó significativamente en comparación con los valores basales. Estos datos sugieren que, en ausencia de sueño MOR, la actividad de las neuronas respiratorias en la VRC está altamente regulada para asegurar la homeostasis de gases y una tasa de respiración estable y que los cambios fisiológicos encontrados probablemente están regulados por núcleos no relacionados con la generación del ritmo respiratorio.
Abstract
Breathing generation and modulation is controlled by several regions in the ventral respiratory column (VRC), such as the parafacial respiratory group/retrotrapezoid nucleus (pFRG/RTN), the Bötzinger Complex (BötC) and the preBötzinger Complex (preBötC). A correlation between sleep and breathing is particularly clear in conditions such as obstructive sleep apnea and congenital central hypoventilation syndrome. Here, by using c-Fos immunoreactivity as an indirect marker of neuronal activity, we aimed to study the effect of short-term selective REM sleep deprivation on the activity of neurons along the VRC. Male Wistar rats were divided in two groups: control (n=6) and 24 h selective REM sleep deprivation using the flowerpot technique (n=11). Respiratory rate, heart rate, temperature and oxygen saturation (SpO2) were measured before and during REM sleep deprivation. When comparing the REM sleep-deprived to the control group, not statistically significant differences were found in the number of c-Fos positive neurons in the pFRG/RTN and VRC or in the respiratory rate, heart rate, temperature and SpO2. Interestingly, in the REM sleep-deprived group the heart rate increased and SpO2 decreased statistically significantly compared to baseline values. These data suggest that, in the absence of REM sleep, activity of respiratory neurons in the VRC is highly regulated to ensure a stable breathing rate and gas homeostasis, and that physiological changes may result from modulation on nuclei not involved in the generation of respiratory rate.
Keywords: Ventral respiratory column, preBötzinger complex; respiratory rhythm; c-Fos; sleep deprivation; REM sleep.
Palabras clave
Texto completo:
PDF (English)Referencias
Deak MC, Kirsch DB, MD. Sleep-Disordered Breathing in Neurologic Conditions. Clin Chest Med. 2014; 35:547–56.
Bhat S, Gupta D, Chokroverty S. Sleep Disorders in Neuromuscular Neurol Clin. 2012; 30:1359-87.
Smith JC, Abdala AP, Rybak IA, Paton JF. Structural and functional architecture of respiratory networks in the mammalian brainstem. Philos Trans R Soc Lond B Biol Sci. 2009; 364:2577–87.
Alheid GF, McCrimmon DR. The chemical neuroanatomy of breathing. Respir Physiol Neurobiol. 2008; 164:3-11.
Smith JC, Abdala AP, Koizumi H, Rybak IA, Paton JF. Spatial and functional architecture of the mammalian brain stem respiratory network: a hierarchy of three oscillatory mechanisms. J Neurophysiol. 2007; 98:3370-87.
Feldman JL, Mitchell GS, Nattie EE. Breathing: rhythmicity, plasticity, chemosensitivity. Annu Rev Neurosci. 2003; 26:239–66.
Smith JC, Ellenberger HH, Ballanyi K, Richter DW, Feldman JL. Pre-Bötzinger complex: a brainstem region that may generate respiratory rhythm in mammals. Science. 1991; 254:726-9.
McKay LC, Janczewski WA, Feldman JL. Sleep-disordered breathing after targeted ablation of preBötzinger complex neurons. Nat Neurosci. 2005; 8:1142-44.
Guyenet PG, Stornetta RL, Bayliss DA. Central respiratory chemoreception. J Comp Neurol. 2010; 518:3883–906.
Guyenet PG, Stornetta RL, Bayliss DA. Retrotrapezoid nucleus and central chemoreception. J Physiol. 2008; 586:2043-48.
Grace KP, Horner RL. Evaluating the evidence surrounding pontinecholinergic involvement in REM sleep generation. Front Neurol. 2015; 6:190.
Szymusiak R, McGinty D. Hypothalamic regulation of sleep and arousal. Ann N Y Acad Sci. 2008; 1129:275–86.
Snyder F, Hobson JA, Morrison DF, Goldfrank F. Changes in respiration, heart rate, and systolic blood pressure in human sleep. J Appl Physiol. 1964; 19:417–22.
Mendelson WB, Martin JV, Perlis M, Giesen H, Wagner R, Rapoport SI, Periodic cessation of respiratory effort during sleep in adult rats. Physiol Behav. 1988; 43: 229–34.
Krieger J, Turlot JC, Mangin P, Kurtz D. Breathing during sleep in normal young and elderly subjects: hypopneas, apneas, and correlated factors. Sleep. 1983; 6:108–20.
Mendelson WB, Guthrie RD, Frederick G, Wyatt RJ. The flower pot technique of rapid eye movement (REM) sleep deprivation. Pharmacol Biochem Behav. 1974; 2:553–56.
Paxinos G, Watson C, The Rat Brain in Stereotaxic Coordinates, 5th Edition, Elsevier Academic Press, San Diego California; 2005.
McKay LC, Feldman JL. Unilateral ablation of pre-Botzinger complex disrupts breathing during sleep but not wakefulness. Am J Respir Crit Care Med. 2008; 178:89–95.
Rasband, WS. ImageJ, U. S. National Institutes of Health, Bethesda, Maryland, USA, https://imagej.nih.gov/ij/, 1997-2016.
Radulovacki M, Trbovic SM, Carley DW. Cardiopulmonary interactions following REM sleep deprivation in Sprague-Dawley rats. Exp Neurol. 1997;145(2 Pt 1):371-5.
Shiromani PJ, Malik M, Winston S, McCarley RW. Time course of Fos-like immunoreactivity associated with cholinergically induced REM sleep. J Neurosci. 1995; 15:3500-8.
Cirelli C, Pompeiano M, Tononi G. Sleep deprivation and c-fos expression in the rat brain. J Sleep Res. 1995; 4:92-106.
García-García F, Beltrán-Parrazal L, Jiménez-Anguiano A, Vega-González A, Drucker-Colín R. Manipulations during forced wakefulness have differential impact on sleep architecture, EEG power spectrum, and Fos induction. Brain Res Bull. 1998; 47:317-24.
Morgan JI, Cohen DR, Hempstead JL, Curran T. Mapping patterns of c-fos expression in the central nervous system after seizure. Science. 1987; 237:192-7.
Semba K1, Pastorius J, Wilkinson M, Rusak B. Sleep deprivation-induced c-fos and junB expression in the rat brain: effects of duration and timing. Behav Brain Res. 2001; 120: 75–86.
Jeddi S, Asl AN, Asgari A, Ghasemi A. The Effect of Sleep Deprivation on Cardiac Function and Tolerance to Ischemia-Reperfusion Injury in Male Rats. Arq Bras Cardiol. 2016; 106:41-8.
Kovalzon VM, Tsibulsky VL. REM-sleep deprivation, stress and emotional behavior in rats. Behav Brain Res. 1984; 14:235-245.
Rechtschaffen A, Bergmann BM. Sleep deprivation in the rat by the disk-over-water method. Behav Brain Res.1995; 69:55-63.
Guzman-Marin R., Suntsova N, Bashir T, Nienhuis R. Szymusiak R, McGinty D, Rapid eye movement sleep deprivation contributes to reduction of neurogenesis in the hippocampal dentate gyrus of the adult rat. Sleep. 2008; 31:167-75.
Gip P, Hagiwara G, Sapolsky RM, Cao VH, Heller HC, Ruby NF. Glucocorticoids influence brain glycogen levels during sleep deprivation. Am J Physiol Regul Integr Comp Physiol. 2004; 286(6):R1057-62.
Mueller AD, Pollock MS, Lieblich SE, Epp JR, Galea LA, Mistlberger RE. Sleep deprivation can inhibit adult hippocampal neurogenesis independent of adrenal stress hormones. Am J Physiol Regul Integr Comp Physiol. 2008; 294(5):R1693-703.
Guzmán-Marín R, Suntsova N, Stewart DR, Gong H, Szymusiak R, McGinty D. Sleep deprivation reduces proliferation of cells in the dentate gyrus of the hippocampus in rats. J Physiol. 2003; 549(Pt 2):563-71.
Joseph V, Pequignot JM, Van Reeth O. Neurochemical perspectives on the control of breathing during sleep. Respir Physiol Neurobiol. 2002; 130:253- 263.
Orem J. Medullary respiratory neuron activity: relationship to tonic and phasic REM sleep. J Appl Physiol Respir Environ Exerc Physiol. 1980; 48: 54-65.
Guyanet PG and Mulkey DK. Retrotrapezoid nucleus and parafacial respiratory group. Respir Physiol Neurobiol. 2010; 173(3):244–55.
Burke PG, Kanbar R, Basting TM, Hodges WM, Viar KE, Stornetta RL, Guyenet PG. State-dependent control of breathing by the retrotrapezoid nucleus. J Physiol. 2015; 593:2909-26.
Cohen MI, Shaw CF. Role in the inspiratory off-switch of vagal inputs to rostral pontine inspiratory-modulated neurons. Respir Physiol Neurobiol. 2004; 143:127–140.
DOI: https://doi.org/10.25009/eb.v8i18.2526
Enlaces refback
- No hay ningún enlace refback.
eNeurobiología es una publicación cuatrimestral editada por el Instituto de Investigaciones Cerebrales de la Universidad Veracruzana. Estamos ubicados en Av. Dr. Luis Castelazo Ayala, s/n, colonia Industrial Ánimas, C.P. 91190, Xalapa-Enríquez, Veracruz, México. Teléfono: 8418900 ext. 13062, www.iice.uv.mx; eneurobiologia@uv.mx. Reserva de Derechos al Uso Exclusivo 04-2023-061314100600-102, otorgada por el Instituto Nacional de Derechos de Autor. ISSN: 2007-3054. Esta obra está bajo una Licencia Creative Commons Attribution 4.0 International.