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Published in: Fluids and Barriers of the CNS 1/2009

Open Access 01-12-2009 | Research

Turnover rate of cerebrospinal fluid in female sheep: changes related to different light-dark cycles

Authors: Jean-Claude Thiéry, Didier Lomet, Sylvain Bougoin, Benoit Malpaux

Published in: Fluids and Barriers of the CNS | Issue 1/2009

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Abstract

Background

Sheep are seasonal breeders. The key factor governing seasonal changes in the reproductive activity of the ewe is increased negative feedback of estradiol at the level of the hypothalamus under long-day conditions. It has previously been demonstrated that when gonadotropin secretions are inhibited during long days, there is a higher concentration of estradiol in the cerebrospinal fluid (CSF) than during short days. This suggests an involvement of the CSF and choroid plexus in the neuroendocrine regulatory loop, but the mechanisms underlying this phenomenon remain unknown. One possible explanation of this difference in hormonal content is an effect of concentration or dilution caused by variations in CSF secretion rate. The aim of this study was thus to investigate changes in the CSF turnover rate related to light-dark cycles.

Methods

The turnover rate of the CSF was estimated by measuring the time taken for the recovery of intraventricular pressure (IVP) after removal of a moderate volume (0.5 to 2 ml) of CSF (slope in mmHg/min). The turnover rate was estimated three times in the same group of sheep: during a natural period of decreasing day-length corresponding to the initial period when gonadotropin activity is stimulated (SG1), during a long-day inhibitory period (IG), and finally during a short-day stimulatory period (SG2).

Results

The time taken and the speed of recovery of initial IVP differed between groups: 8 min 30 sec, 0.63 ± 0.07 mmHg/min(SG1), 11 min 1 sec, 0.38 ± 0.06 mmHg/min (IG) and 9 min 0 sec, 0.72 ± 0.15 mmHg/min (SG2). Time changes of IVP differed between groups (ANOVA, p < 0.005, SG1 different from IG, p < 0.05). The turnover rate in SG2: 183.16 ± 23.82 μl/min was not significantly different from SG1: 169. 23 ± 51.58 μl/min (Mann-Whitney test, p = 0.41), but was significantly different from IG: 71.33 ± 16.59 μl/min (p = 0.016).

Conclusion

This study shows that the turnover rate of CSF in ewes changes according to the light-dark cycle; it is increased during short day periods and reduced in long day periods. This phenomenon could account for differences in hormonal concentrations in the CSF in this seasonal species.
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Literature
1.
go back to reference Speake T, Whitwell C, Kajita H, Majid A, Brown PD: Mechanisms of CSF secretion by the choroid plexus. Microsc Res Techn. 2001, 52: 49-59. 10.1002/1097-0029(20010101)52:1<49::AID-JEMT7>3.0.CO;2-C.CrossRef Speake T, Whitwell C, Kajita H, Majid A, Brown PD: Mechanisms of CSF secretion by the choroid plexus. Microsc Res Techn. 2001, 52: 49-59. 10.1002/1097-0029(20010101)52:1<49::AID-JEMT7>3.0.CO;2-C.CrossRef
2.
go back to reference Brown PD, Davies SL, Speake T, Millar ID: Molecular mechanisms of cerebrospinal fluid production. Neuroscience. 2004, 129: 957-970. 10.1016/j.neuroscience.2004.07.003.PubMedCentralCrossRefPubMed Brown PD, Davies SL, Speake T, Millar ID: Molecular mechanisms of cerebrospinal fluid production. Neuroscience. 2004, 129: 957-970. 10.1016/j.neuroscience.2004.07.003.PubMedCentralCrossRefPubMed
3.
go back to reference Ghersi-Egea JF, Strazielle N: Choroid plexus transporters for drugs and other xenobiotics. J Drug Target. 2002, 10: 353-357. 10.1080/10611860290031859.CrossRefPubMed Ghersi-Egea JF, Strazielle N: Choroid plexus transporters for drugs and other xenobiotics. J Drug Target. 2002, 10: 353-357. 10.1080/10611860290031859.CrossRefPubMed
4.
go back to reference Miller DS: Confocal imaging of xenobiotic transport across the choroid plexus. Adv Drug Deliv Rev. 2004, 56: 1811-1824. 10.1016/j.addr.2004.07.010.CrossRefPubMed Miller DS: Confocal imaging of xenobiotic transport across the choroid plexus. Adv Drug Deliv Rev. 2004, 56: 1811-1824. 10.1016/j.addr.2004.07.010.CrossRefPubMed
5.
go back to reference Shen DD, Artru AA, Adkison KK: Principles and applicability of CSF sampling for the assessment of CNS drug delivery and pharmacodynamics. Adv Drug Deliv Rev. 2004, 56: 1825-1857. 10.1016/j.addr.2004.07.011.CrossRefPubMed Shen DD, Artru AA, Adkison KK: Principles and applicability of CSF sampling for the assessment of CNS drug delivery and pharmacodynamics. Adv Drug Deliv Rev. 2004, 56: 1825-1857. 10.1016/j.addr.2004.07.011.CrossRefPubMed
6.
go back to reference Kurtcuoglu V, Soellinger M, Summers P, Boomsma K, Poulikakos D, Boesiger P, Ventikos J: Computational investigation of subject-specific cerebrospinal fluid flow in the third ventricle and aqueduct of Sylvius. J Biomech. 2007, 40: 1235-1245. 10.1016/j.jbiomech.2006.05.031.CrossRefPubMed Kurtcuoglu V, Soellinger M, Summers P, Boomsma K, Poulikakos D, Boesiger P, Ventikos J: Computational investigation of subject-specific cerebrospinal fluid flow in the third ventricle and aqueduct of Sylvius. J Biomech. 2007, 40: 1235-1245. 10.1016/j.jbiomech.2006.05.031.CrossRefPubMed
7.
go back to reference Schreiber G, Aldred AR, Jaworowski A, Nilsson C, Achen MG, Segal MB: Thyroxine transport from blood to brain via transthyretin synthesis in choroid plexus. Am J Physiol. 1990, 258: R338-R345.PubMed Schreiber G, Aldred AR, Jaworowski A, Nilsson C, Achen MG, Segal MB: Thyroxine transport from blood to brain via transthyretin synthesis in choroid plexus. Am J Physiol. 1990, 258: R338-R345.PubMed
9.
go back to reference Tricoire H, Locatelli A, Chemineau P, Malpaux B: Melatonin Enters the Cerebrospinal Fluid through the Pineal Recess. Endocrinology. 2002, 143: 84-90. 10.1210/en.143.1.84.CrossRefPubMed Tricoire H, Locatelli A, Chemineau P, Malpaux B: Melatonin Enters the Cerebrospinal Fluid through the Pineal Recess. Endocrinology. 2002, 143: 84-90. 10.1210/en.143.1.84.CrossRefPubMed
10.
go back to reference Chodobski A, Szmydynger-Chodobska J: Choroid plexus: target for polypeptides and sites of their synthesis. Microsc Res Techn. 2001, 52: 65-82. 10.1002/1097-0029(20010101)52:1<65::AID-JEMT9>3.0.CO;2-4.CrossRef Chodobski A, Szmydynger-Chodobska J: Choroid plexus: target for polypeptides and sites of their synthesis. Microsc Res Techn. 2001, 52: 65-82. 10.1002/1097-0029(20010101)52:1<65::AID-JEMT9>3.0.CO;2-4.CrossRef
11.
go back to reference Lehman M, Silver R: CSF signaling in physiology and behavior. Prog Brain Res. 2000, 125: 415-433. full_text.CrossRefPubMed Lehman M, Silver R: CSF signaling in physiology and behavior. Prog Brain Res. 2000, 125: 415-433. full_text.CrossRefPubMed
12.
go back to reference Johanson CE, Duncan JA, Klinge PM, Brinker T, Stopa EG, Silverberg GD: Multiplicity of cerebrospinal fluid functions: New challenges in health and disease. Cerebrospinal Fluid Res. 2008, 5: 10-10.1186/1743-8454-5-10.PubMedCentralCrossRefPubMed Johanson CE, Duncan JA, Klinge PM, Brinker T, Stopa EG, Silverberg GD: Multiplicity of cerebrospinal fluid functions: New challenges in health and disease. Cerebrospinal Fluid Res. 2008, 5: 10-10.1186/1743-8454-5-10.PubMedCentralCrossRefPubMed
13.
go back to reference Goodman RL, Bittman EL, Foster DL, Karsch FJ: Alterations in the control of luteinizing hormone pulse frequency underlie the seasonal variation in estradiol negative feedback in the ewe. Biol reprod. 1982, 27: 580-589. 10.1095/biolreprod27.3.580.CrossRefPubMed Goodman RL, Bittman EL, Foster DL, Karsch FJ: Alterations in the control of luteinizing hormone pulse frequency underlie the seasonal variation in estradiol negative feedback in the ewe. Biol reprod. 1982, 27: 580-589. 10.1095/biolreprod27.3.580.CrossRefPubMed
14.
go back to reference Thiéry JC, Robel P, Canepa S, Delaleu B, Gayrard V, Picard-Hagen N, Malpaux B: Passage of progesterone into the brain changes with photoperiod in ewe. Eur J Neurosci. 2003, 18: 895-901. 10.1046/j.1460-9568.2003.02796.x.CrossRefPubMed Thiéry JC, Robel P, Canepa S, Delaleu B, Gayrard V, Picard-Hagen N, Malpaux B: Passage of progesterone into the brain changes with photoperiod in ewe. Eur J Neurosci. 2003, 18: 895-901. 10.1046/j.1460-9568.2003.02796.x.CrossRefPubMed
15.
go back to reference Thiéry JC, Lomet D, Schumacher M, Liere P, Tricoire H, Locatelli A, Delagrange P, Malpaux B: Concentrations of estradiol in ewe cerebrospinal fluid are modulated by photoperiod through pineal-dependent mechanisms. J Pineal Res. 2006, 41: 306-312. 10.1111/j.1600-079X.2006.00370.x.CrossRefPubMed Thiéry JC, Lomet D, Schumacher M, Liere P, Tricoire H, Locatelli A, Delagrange P, Malpaux B: Concentrations of estradiol in ewe cerebrospinal fluid are modulated by photoperiod through pineal-dependent mechanisms. J Pineal Res. 2006, 41: 306-312. 10.1111/j.1600-079X.2006.00370.x.CrossRefPubMed
16.
go back to reference Adam CL, Findlay PA, Miller DW: Blood-brain leptin transport and appetite and reproductive neuroendocrine responses to intracerebroventricular leptin injection in sheep: influence of photoperiod. Endocrinology. 2006, 147: 4589-4598. 10.1210/en.2006-0576.CrossRefPubMed Adam CL, Findlay PA, Miller DW: Blood-brain leptin transport and appetite and reproductive neuroendocrine responses to intracerebroventricular leptin injection in sheep: influence of photoperiod. Endocrinology. 2006, 147: 4589-4598. 10.1210/en.2006-0576.CrossRefPubMed
17.
go back to reference Nilsson C, Stahlberg F, Thomsen C, Henriksen O, Herning M, Owman C: Circadian variation in human cerebrospinal fluid production measured by magnetic resonance imaging. Am J Physiol. 1992, 262: R20-R24.PubMed Nilsson C, Stahlberg F, Thomsen C, Henriksen O, Herning M, Owman C: Circadian variation in human cerebrospinal fluid production measured by magnetic resonance imaging. Am J Physiol. 1992, 262: R20-R24.PubMed
18.
go back to reference May C, Kaye JA, Atack JR, Schapiro MB, Friedland RP, Rapoport SI: Cerebrospinal fluid production is reduced in healthy aging. Neurology. 1990, 40: 500-503.CrossRefPubMed May C, Kaye JA, Atack JR, Schapiro MB, Friedland RP, Rapoport SI: Cerebrospinal fluid production is reduced in healthy aging. Neurology. 1990, 40: 500-503.CrossRefPubMed
19.
go back to reference Preston JE: Ageing choroid plexus-cerebrospinal fluid system. Microsc Res Techn. 2001, 52: 31-37. 10.1002/1097-0029(20010101)52:1<31::AID-JEMT5>3.0.CO;2-T.CrossRef Preston JE: Ageing choroid plexus-cerebrospinal fluid system. Microsc Res Techn. 2001, 52: 31-37. 10.1002/1097-0029(20010101)52:1<31::AID-JEMT5>3.0.CO;2-T.CrossRef
20.
go back to reference Silverberg GD, Heit G, Huhn S, Jaffe RA, Chang SD, Bronte-Stewart H, Rubenstein E, Possin K, Saul TA: The cerebrospinal fluid production rate is reduced in dementia of the Alzheimer's type. Neurology. 2001, 57: 1763-1766.CrossRefPubMed Silverberg GD, Heit G, Huhn S, Jaffe RA, Chang SD, Bronte-Stewart H, Rubenstein E, Possin K, Saul TA: The cerebrospinal fluid production rate is reduced in dementia of the Alzheimer's type. Neurology. 2001, 57: 1763-1766.CrossRefPubMed
21.
go back to reference Masserman JH: Cerebrospinal fluid hydrodynamics. Arch Neurol Psychiat. 1934, 32: 524-553.CrossRef Masserman JH: Cerebrospinal fluid hydrodynamics. Arch Neurol Psychiat. 1934, 32: 524-553.CrossRef
22.
go back to reference Karsch FJ, Bittman EL, Foster DL, Goodman RL, Legan SJ, Robinson JE: Neuroendocrine basis of seasonal reproduction. Recent Prog Horm Res. 1984, 40: 185-232.PubMed Karsch FJ, Bittman EL, Foster DL, Goodman RL, Legan SJ, Robinson JE: Neuroendocrine basis of seasonal reproduction. Recent Prog Horm Res. 1984, 40: 185-232.PubMed
23.
go back to reference Skinner DC, Malpaux B, Delaleu B, Caraty A: Luteinizing hormone (LH)-releasing hormone in third ventricular cerebrospinal fluid of the ewe: correlation with LH pulses and the LH surge. Endocrinology. 1995, 136: 3230-3237. 10.1210/en.136.8.3230.PubMed Skinner DC, Malpaux B, Delaleu B, Caraty A: Luteinizing hormone (LH)-releasing hormone in third ventricular cerebrospinal fluid of the ewe: correlation with LH pulses and the LH surge. Endocrinology. 1995, 136: 3230-3237. 10.1210/en.136.8.3230.PubMed
24.
go back to reference Chen RL, Kassem NA, Redzic ZB, Chen CP, Segal MB, Preston JE: Age-related changes in choroid plexus and blood-cerebrospinal fluid barrier function in the sheep. Exp Gerontol. 2009, 44: 289-96. 10.1016/j.exger.2008.12.004.CrossRefPubMed Chen RL, Kassem NA, Redzic ZB, Chen CP, Segal MB, Preston JE: Age-related changes in choroid plexus and blood-cerebrospinal fluid barrier function in the sheep. Exp Gerontol. 2009, 44: 289-96. 10.1016/j.exger.2008.12.004.CrossRefPubMed
25.
go back to reference Masseguin C, LePanse S, Corman B, Verbavatz JM, Gabrion J: Aging affects choroidal proteins involved in CSF production in Sprague-Dawley rats. Neurobiol Aging. 2005, 26: 917-927. 10.1016/j.neurobiolaging.2004.07.013.CrossRefPubMed Masseguin C, LePanse S, Corman B, Verbavatz JM, Gabrion J: Aging affects choroidal proteins involved in CSF production in Sprague-Dawley rats. Neurobiol Aging. 2005, 26: 917-927. 10.1016/j.neurobiolaging.2004.07.013.CrossRefPubMed
26.
go back to reference Skinner DC, Herbison AE: Effects of photoperiod on estrogen receptor, tyrosine hydroxylase, neuropeptide Y, and beta-endorphin immunoreactivity in the ewe hypothalamus. Endocrinology. 1997, 138: 2585-2595. 10.1210/en.138.6.2585.PubMed Skinner DC, Herbison AE: Effects of photoperiod on estrogen receptor, tyrosine hydroxylase, neuropeptide Y, and beta-endorphin immunoreactivity in the ewe hypothalamus. Endocrinology. 1997, 138: 2585-2595. 10.1210/en.138.6.2585.PubMed
27.
go back to reference Stefanovic I, Adrian B, Jansen HT, Lehman MN, Goodman RL: The ability of estradiol to induce fos expression in a subset of estrogen receptor-α containing neurons in the preoptic area of the ewe depends on reproductive status. Endocrinology. 2000, 141: 190-196. 10.1210/en.141.1.190.PubMed Stefanovic I, Adrian B, Jansen HT, Lehman MN, Goodman RL: The ability of estradiol to induce fos expression in a subset of estrogen receptor-α containing neurons in the preoptic area of the ewe depends on reproductive status. Endocrinology. 2000, 141: 190-196. 10.1210/en.141.1.190.PubMed
28.
go back to reference Dziegielewska KM, Evans CA, Fossan G, Lorscheider FL, Malinowska DH, Mollgard K, Reynolds ML, Saunders NR, Wilkinson S: Proteins in cerebrospinal fluid and plasma of fetal sheep during development. J Physiol. 1980, 300: 457-465.PubMedCentralCrossRefPubMed Dziegielewska KM, Evans CA, Fossan G, Lorscheider FL, Malinowska DH, Mollgard K, Reynolds ML, Saunders NR, Wilkinson S: Proteins in cerebrospinal fluid and plasma of fetal sheep during development. J Physiol. 1980, 300: 457-465.PubMedCentralCrossRefPubMed
29.
go back to reference Chodobski A, Szmydynger-Chodobska J, Cooper E, McKinley MJ: Atrial natriuretic peptide does not alter cerebrospinal fluid formation in sheep. Am J Physiol. 1992, 262: R860-R864.PubMed Chodobski A, Szmydynger-Chodobska J, Cooper E, McKinley MJ: Atrial natriuretic peptide does not alter cerebrospinal fluid formation in sheep. Am J Physiol. 1992, 262: R860-R864.PubMed
30.
go back to reference Heisey SR, Held D, Pappenheimer JR: Bulk flow and diffusion in the cerebrospinal fluid system of the goat. Am J Physiol. 1962, 203: 775-781.PubMed Heisey SR, Held D, Pappenheimer JR: Bulk flow and diffusion in the cerebrospinal fluid system of the goat. Am J Physiol. 1962, 203: 775-781.PubMed
31.
go back to reference Artru AA, Momota T: Rate of CSF formation and resistance to reabsorption of CSF during sevoflurane or remifentanil in rabbits. J Neurosurg Anesthesiol. 2000, 12: 37-43. 10.1097/00008506-200001000-00008.CrossRefPubMed Artru AA, Momota T: Rate of CSF formation and resistance to reabsorption of CSF during sevoflurane or remifentanil in rabbits. J Neurosurg Anesthesiol. 2000, 12: 37-43. 10.1097/00008506-200001000-00008.CrossRefPubMed
32.
go back to reference Tetrault S, Chever O, Sik A, Amzica F: Opening of the blood-brain barrier during isoflurane anaesthesia. Eur J Neurosci. 2008, 28: 1330-1341. 10.1111/j.1460-9568.2008.06443.x.CrossRefPubMed Tetrault S, Chever O, Sik A, Amzica F: Opening of the blood-brain barrier during isoflurane anaesthesia. Eur J Neurosci. 2008, 28: 1330-1341. 10.1111/j.1460-9568.2008.06443.x.CrossRefPubMed
33.
go back to reference Nilsson C, Stahlberg F, Gideon P, Thomsen C, Henriksen O: The nocturnal increase in human cerebrospinal fluid production is inhibited by β1-receptor antagonist. Am J Physiol. 1994, 267: R1445-R1448.PubMed Nilsson C, Stahlberg F, Gideon P, Thomsen C, Henriksen O: The nocturnal increase in human cerebrospinal fluid production is inhibited by β1-receptor antagonist. Am J Physiol. 1994, 267: R1445-R1448.PubMed
34.
go back to reference Thiery JC, Chemineau P, Hernandez X, Migaud M, Malpaux B: Neuroendocrine interactions and seasonality. Dom Anim Endocrinol. 2002, 23: 87-100. 10.1016/S0739-7240(02)00148-0.CrossRef Thiery JC, Chemineau P, Hernandez X, Migaud M, Malpaux B: Neuroendocrine interactions and seasonality. Dom Anim Endocrinol. 2002, 23: 87-100. 10.1016/S0739-7240(02)00148-0.CrossRef
35.
go back to reference Skinner DC, Malpaux B: High melatonin concentrations in third ventricular cerebrospinal fluid are not due to Galen vein blood recirculating through the choroid plexus. Endocrinology. 1999, 140: 4399-4405. 10.1210/en.140.10.4399.PubMed Skinner DC, Malpaux B: High melatonin concentrations in third ventricular cerebrospinal fluid are not due to Galen vein blood recirculating through the choroid plexus. Endocrinology. 1999, 140: 4399-4405. 10.1210/en.140.10.4399.PubMed
36.
go back to reference Stankov B, Capsoni S, Lucini V, Fauteck J, Gatti S, Gridelli B, Biella G, Cozzi B, Fraschini F: Autoradiographic localization of putative melatonin receptors in the brains of two Old World primates: Cercopithecus aethiops and Papio ursinus. Neuroscience. 1993, 52: 459-468. 10.1016/0306-4522(93)90172-C.CrossRefPubMed Stankov B, Capsoni S, Lucini V, Fauteck J, Gatti S, Gridelli B, Biella G, Cozzi B, Fraschini F: Autoradiographic localization of putative melatonin receptors in the brains of two Old World primates: Cercopithecus aethiops and Papio ursinus. Neuroscience. 1993, 52: 459-468. 10.1016/0306-4522(93)90172-C.CrossRefPubMed
37.
go back to reference Williams LM, Hannah LT, Bassett JM: Melatonin receptors in neonatal pig brain and pituitary gland. J Pineal Res. 1999, 26: 43-49. 10.1111/j.1600-079X.1999.tb00565.x.CrossRefPubMed Williams LM, Hannah LT, Bassett JM: Melatonin receptors in neonatal pig brain and pituitary gland. J Pineal Res. 1999, 26: 43-49. 10.1111/j.1600-079X.1999.tb00565.x.CrossRefPubMed
38.
go back to reference Williams LM, Hannah LT, Kyle CE, Adam CL: Central melatonin receptors in red deer (Cervus elaphus). Gen Comp Endocrino. 1996, 104: 1-106. 10.1006/gcen.1996.0134.CrossRef Williams LM, Hannah LT, Kyle CE, Adam CL: Central melatonin receptors in red deer (Cervus elaphus). Gen Comp Endocrino. 1996, 104: 1-106. 10.1006/gcen.1996.0134.CrossRef
39.
go back to reference Decker JF, Quay WB: Stimulatory effects of melatonin on ependymal epithelium of choroid plexuses in golden hamsters. J Neural Transm. 1982, 55: 53-67. 10.1007/BF01243341.CrossRefPubMed Decker JF, Quay WB: Stimulatory effects of melatonin on ependymal epithelium of choroid plexuses in golden hamsters. J Neural Transm. 1982, 55: 53-67. 10.1007/BF01243341.CrossRefPubMed
40.
go back to reference Vitte PA, Brun J, Lestage P, Claustrat B, Bobillier P: The effects of melatonin and pinealectomy upon local cerebral glucose utilization in awake unrestrained rats are restricted to a few specific regions. Brain Res. 1989, 489: 273-282. 10.1016/0006-8993(89)90860-3.CrossRefPubMed Vitte PA, Brun J, Lestage P, Claustrat B, Bobillier P: The effects of melatonin and pinealectomy upon local cerebral glucose utilization in awake unrestrained rats are restricted to a few specific regions. Brain Res. 1989, 489: 273-282. 10.1016/0006-8993(89)90860-3.CrossRefPubMed
41.
go back to reference Kondo N, Sekijima T, Kondo J, Takamatsu N, Tohya K, Ohtsu T: Circannual control of hibernation by HP complex in the brain. Cell. 2006, 125: 161-172. 10.1016/j.cell.2006.03.017.CrossRefPubMed Kondo N, Sekijima T, Kondo J, Takamatsu N, Tohya K, Ohtsu T: Circannual control of hibernation by HP complex in the brain. Cell. 2006, 125: 161-172. 10.1016/j.cell.2006.03.017.CrossRefPubMed
42.
go back to reference Skipor J, Thiery JC: The choroid plexus – cerebrospinal fluid system: undervaluated pathway of neuroendocrine signaling into the brain. Acta Neurobiol Exp (Wars). 2008, 68: 414-428. Skipor J, Thiery JC: The choroid plexus – cerebrospinal fluid system: undervaluated pathway of neuroendocrine signaling into the brain. Acta Neurobiol Exp (Wars). 2008, 68: 414-428.
43.
go back to reference Ramírez-Rodríguez G, Meza I, Hernández ME, Castillo A, Benítez-King G: Melatonin induced cyclic modulation of vectorial water transport in kidney-derived MDCK cells. Kidney Int. 2003, 63: 1356-1364. 10.1046/j.1523-1755.2003.00872.x.CrossRefPubMed Ramírez-Rodríguez G, Meza I, Hernández ME, Castillo A, Benítez-King G: Melatonin induced cyclic modulation of vectorial water transport in kidney-derived MDCK cells. Kidney Int. 2003, 63: 1356-1364. 10.1046/j.1523-1755.2003.00872.x.CrossRefPubMed
Metadata
Title
Turnover rate of cerebrospinal fluid in female sheep: changes related to different light-dark cycles
Authors
Jean-Claude Thiéry
Didier Lomet
Sylvain Bougoin
Benoit Malpaux
Publication date
01-12-2009
Publisher
BioMed Central
Published in
Fluids and Barriers of the CNS / Issue 1/2009
Electronic ISSN: 2045-8118
DOI
https://doi.org/10.1186/1743-8454-6-9

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