Projections of the suprachiasmatic nucleus to stress-related areas in the rat hypothalamus: A light and electron microscopic study
Open accessAbstract
The purpose of the present study was to investigate the sites in the hypothalamus where the suprachiasmatic nucleus (SCN) may influence corticosteroid secretion. In spite of the well established, SCN-mediated, daily rhythms in adrenocorticotrophic hormone (ACTH) and corticosteroid secretion, previous studies determining the projections of the suprachiasmatic nucleus failed to illustrate direct connections with corticotrophin-releasing hormone neurons (CRH). In order to identify where in the central nervous system the SCN may influence corticosteroid secretion, areas were selected that contained SCN efferents contacting neurons involved in the stress response. To achieve this in the present study, SCN efferents were visualized by Pha-L tract-tracing, together with the neurons involved in the stress response by immunocytochemical staining for c-fos protein. The sites where these efferents contacted c-fos-positive neurons were established by light microscopic double staining and electron microscopic immunocytochemical studies. It appeared that apart from the medial parvocellular area of the paraventricular nucleus (PVN) of the hypothalamus, many more regions showed fos-positive neurons. Sites where SCN efferents contacted such neurons are limited only to areas immediately adjacent to these putative CRH neurons but are not concentrated on these neurons themselves. These areas consist of the periventricular and rostral PVN together with the dorsomedial hypothalamus: all three regions are known to project into the PVN. Therefore, it is concluded that the SCN transmits its information related to corticosteroid secretion via interneurons in and around the PVN to the CRH-containing neurons, rather than by a direct interaction with these neurons themselves.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The SCN may modulate cardiovascular functioning, as suggested by multisynaptic projections from the SCN to the heart and organs that regulate cardiovascular function through hormones and blood volume regulation.
“That the SCN may modulate cardiovascular functioning is suggested by the presence of multisynaptic projections from the SCN to the heart and organs that regulate cardiovascular function through hormones and blood volume regulation (e.g., adrenal cortex, adrenal medulla, and kidneys”
From The impact of the circadian timing system on cardiovascular and metabolic function (2012) · cites this paper as Buijs et al., 1993
Vasopressinergic neurons from the SCN have an inhibitory effect on CRH neurons in the PVN.
“The vasopressinergic neurons from the SCN have an inhibitory effect on CRH neurons in the PVN (Buijs et al., 1993; Hermes et al., 1996).”
From The impact of the circadian timing system on cardiovascular and metabolic function (2012) · cites this paper as Buijs et al., 1993
Cites
Morgan, J., & Curran, T. (1991) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.14.030191.002225 · Cited by 2,689 · see citing works
Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat
Moore, R. Y., & Eichler, V. B. (1972) · Brain Research · doi:10.1016/0006-8993(72)90054-6 · Cited by 2,135 · see citing works
Swanson, L. W., Sawchenko, P. E., Rivier, J., & Vale, W. W. (2008) · Neuroendocrinology · doi:10.1159/000123454 · Cited by 1,953 · see citing works
Expression of c- <i>fos</i> Protein in Brain: Metabolic Mapping at the Cellular Level
Sagar, S. M., Sharp, F. R., & Curran, T. (1988) · Science · doi:10.1126/science.3131879 · Cited by 1,925 · see citing works
Watts, A. G., Swanson, L. W., & Sanchez‐Watts, G. (1987) · The Journal of Comparative Neurology · doi:10.1002/cne.902580204 · Cited by 678 · see citing works
The projections of the dorsomedial hypothalamic nucleus in the rat
Horst, G. J. T., & Luiten, P. G. M. (1986) · Brain Research Bulletin · doi:10.1016/0361-9230(86)90038-9 · Cited by 269 · see citing works
The magnocellular and parvocellular paraventricular nucleus of rat: intrinsic organization
Van Den Pol, A. N. (1982) · Journal of Comparative Neurology · doi:10.1002/cne.902060402 · Cited by 228 · see citing works
Vasopressin-containing neurons of the suprachiasmatic nuclei inhibit corticosterone release
Kalsbeek, A., Buijs, R. M., van Heerikhuize, J. J., Arts, M., & van der Woude, T. P. (1992) · Brain Research · doi:10.1016/0006-8993(92)90927-2 · Cited by 226 · see citing works
Self-citationGallyas, F., Görcs, T. J., & Merchenthaler, I. J. (1982) · Journal of Histochemistry & Cytochemistry · doi:10.1177/30.2.7061820 · Cited by 221 · see citing works
Efferent connections of the rat suprachiasmatic nucleus
Stephan, F. K., Berkley, K. J., & Moss, R. L. (1981) · Neuroscience · doi:10.1016/0306-4522(81)90108-1 · Cited by 216 · see citing works
Vasopressin fiber pathways in the rat brain following suprachiasmatic nucleus lesioning
Hoorneman, E. M. D., & Buijs, R. M. (1982) · Brain Research · doi:10.1016/0006-8993(82)90246-3 · Cited by 211 · see citing works
Self-citationAdrenal Sensitivity to Adrenocorticotropin Varies Diurnally*
KANEKO, M., Kaneko, K., Shinsako, J., & Dallman, M. F. (1981) · Endocrinology · doi:10.1210/endo-109-1-70 · Cited by 207 · see citing works
Berk, M. L., & Finkelstein, J. A. (1981) · Brain Research · doi:10.1016/0006-8993(81)91079-9 · Cited by 193 · see citing works
Suprachiasmatic nucleus lesion increases corticosterone secretion
Buijs, R. M., Kalsbeek, A., van der Woude, T. P., van Heerikhuize, J. J., & Shinn, S. (1993) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1993.264.6.r1186 · Cited by 149 · see citing works
Self-citationCircadian variation in stress-evoked increases in plasma corticosterone
Dunn, J. D., Scheving, L. E., & Millet, P. (1972) · American Journal of Physiology-Legacy Content · doi:10.1152/ajplegacy.1972.223.2.402 · Cited by 143 · see citing works
BRADBURY, M. J., Cascio, C. S., Scribner, K. A., & Dallman, M. F. (1991) · Endocrinology · doi:10.1210/endo-128-2-680 · Cited by 139 · see citing works
Kant, J., Mougey, E. H., & Meyerhoff, J. L. (2008) · Neuroendocrinology · doi:10.1159/000124553 · Cited by 138 · see citing works
Whitnall, M. H., Smyth, D. G., & Gainer, H. (2008) · Neuroendocrinology · doi:10.1159/000124768 · Cited by 121 · see citing works
Jacobson, L., Sharp, F. R., & Dallman, M. F. (1990) · Endocrinology · doi:10.1210/endo-126-3-1709 · Cited by 112 · see citing works
The suprachiasmatic nuclei stimulate evening ACTH secretion in the rat
Cascio, C. S., Shinsako, J., & Dallman, M. F. (1987) · Brain Research · doi:10.1016/0006-8993(87)90837-7 · Cited by 109 · see citing works
Bernardis, L. L. (1973) · Physiology & Behavior · doi:10.1016/0031-9384(73)90054-1 · Cited by 101 · see citing works
Effect of Ventromedial and Dorsomedial Hypothalamic Lesions on Circadian Corticosterone Rhythms
Bellinger, L. L., Bernardis, L. L., & Mendel, V. E. (2008) · Neuroendocrinology · doi:10.1159/000122628 · Cited by 85 · see citing works
Buijs, R. M., Pool, C. W., van Heerikhuize, J. J., Sluiter, A. A., van der Sluis, P. J., Ramkema, M., van der Woude, T. P., & van der Beek, E. M. (1989) · Data Archiving and Networked Services (DANS) · Cited by 82 · see citing works
Self-citationKalsbeek, A., & Buijs, R. M. (1992) · Progress in brain research · doi:10.1016/s0079-6123(08)61186-3 · Cited by 50 · see citing works
Self-citationYamamoto, H., Nagai, K., & Nakagawa, H. (1984) · Brain Research · doi:10.1016/0006-8993(84)90326-3 · Cited by 46 · see citing works
Plasma hormone levels in growth-retarded rats with dorsomedial hypothalamic lesions
Bellinger, L. L., Bernardis, L. L., McCusker, R. H., & Campion, D. R. (1985) · Physiology & Behavior · doi:10.1016/0031-9384(85)90378-6 · Cited by 33 · see citing works
Buijs, R. M., van der Beek, E. M., Renaud, L. P., Day, T. A., & Jhamandas, J. H. (1990) · Neuroscience · doi:10.1016/0306-4522(90)90255-3 · Cited by 29 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Herman, J. P., Figueiredo, H., Mueller, N. K., Ulrich-Lai, Y., Ostrander, M. M., Choi, D. C., & Cullinan, W. E. (2003) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2003.07.001 · Cited by 1,586 · see citing works
Interacting Appetite-Regulating Pathways in the Hypothalamic Regulation of Body Weight
Kalra, S. P., Dube, M. G., Pu, S., Xu, B., Horváth, T. L., & Kalra, P. S. (1999) · Endocrine Reviews · doi:10.1210/edrv.20.1.0357 · Cited by 1,556 · see citing works
Russell, G., & Lightman, S. (2019) · Nature Reviews Endocrinology · doi:10.1038/s41574-019-0228-0 · Cited by 1,032 · see citing works
Glucocorticoids and the circadian clock
Dickmeis, T. (2009) · Journal of Endocrinology · doi:10.1677/joe-08-0415 · Cited by 494 · see citing works
Buijs, R. M., Wortel, J., Van Heerikhuize, J. J., Feenstra, M. G. P., Ter Horst, G. J., Romijn, H. J., & Kalsbeek, A. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00575.x · Cited by 485 · see citing works
Self-citationCircadian system, sleep and endocrinology
Morris, C. J., Aeschbach, D., & Scheer, F. A. J. L. (2012) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2011.09.003 · Cited by 403 · see citing works
Buijs, R. M., van Eden, C. G., Goncharuk, V. D., & Kalsbeek, A. (2003) · Journal of Endocrinology · doi:10.1677/joe.0.1770017 · Cited by 387 · see citing works
Self-citationLowry, C. A. (2002) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2002.00861.x · Cited by 362 · see citing works
Guilding, C., & Piggins, H. D. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05581.x · Cited by 348 · see citing works
Dendritic Release of Vasopressin and Oxytocin
Ludwig (1998) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.1998.00279.x · Cited by 342 · see citing works
Neurotransmitter Switching in the Adult Brain Regulates Behavior
Dulcis, D., Jamshidi, P., Leutgeb, S., & Spitzer, N. C. (2013) · Science · doi:10.1126/science.1234152 · Cited by 317 · see citing works
Haamedi, S. N., Karten, H. J., & Djamgoz, M. B. A. (2001) · The Journal of Comparative Neurology · doi:10.1002/1096-9861(20010319)431:4 · Cited by 8 · see citing works
Self-citationTopographic organization of suprachiasmatic nucleus projection neurons
Leak, R. K., & Moore, R. Y. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.1142 · Cited by 295 · see citing works
Kalsbeek, A., van Heerikhuize, J. J., Wortel, J., & Buijs, R. M. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-17-05555.1996 · Cited by 274 · see citing works
Self-citationKalsbeek, A., & Buijs, R. M. (2002) · Cell and Tissue Research · doi:10.1007/s00441-002-0577-0 · Cited by 261 · see citing works
Self-citationL�pez-Mart�n, E., Caruncho, H. J., Rodríguez‐Pallares, J., Guerra, M. J., & Labandeira-García, J. L. (1999) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19990405)406:2 · Cited by 40 · see citing works
Self-citationBowers, G., Cullinan, W. E., & Herman, J. P. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-15-05938.1998 · Cited by 250 · see citing works
Thompson, R. H. (1998) · Brain Research Reviews · doi:10.1016/s0165-0173(98)00010-1 · Cited by 247 · see citing works
Kalsbeek, A., La Fleur, S., Van Heijningen, C., & Buijs, R. M. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.5328-03.2004 · Cited by 244 · see citing works
Self-citationWotjak, C. T., Kubota, M., Liebsch, G., Montkowski, A., Holsboer, F., Neumann, I. D., & Landgraf, R. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-23-07725.1996 · Cited by 231 · see citing works
Chapter 8 Entrainment pathways and the functional organization of the circadian system
Moore, R. Y. (1996) · Progress in brain research · doi:10.1016/s0079-6123(08)60403-3 · Cited by 226 · see citing works
The impact of the circadian timing system on cardiovascular and metabolic function
Morris, C. J., Yang, J. N., & Scheer, F. A. J. L. (2012) · Progress in Brain Research · doi:10.1016/b978-0-444-59427-3.00019-8 · Cited by 215 · see citing works
Structural characterization of a hypothalamic visceromotor pattern generator network
Thompson, R. H. (2003) · Brain Research Reviews · doi:10.1016/s0165-0173(02)00232-1 · Cited by 208 · see citing works
Sexual dimorphism in the mammalian limbic system
Madeira, M. D., & Lieberman, A. R. (1995) · Progress in Neurobiology · doi:10.1016/0301-0082(94)00052-j · Cited by 202 · see citing works
Neurochemical organization of circadian rhythm in the suprachiasmatic nucleus
Inouye, S. T., & Shibata, S. (1994) · Neuroscience Research · doi:10.1016/0168-0102(94)90029-9 · Cited by 195 · see citing works
Larsen, Enquist, & Card (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00003.x · Cited by 192 · see citing works
Organization of circadian functions: interaction with the body
Buijs, R. M., Scheer, F. A. J. L., Kreier, F., Yi, C., Bos, N. P. A., Goncharuk, V. D., & Kalsbeek, A. (2006) · Progress in brain research · doi:10.1016/s0079-6123(06)53020-1 · Cited by 189 · see citing works
Self-citationYi, C., van der Vliet, J., Dai, J., Guangfu, Y., Li-qiang, R., & Buijs, R. M. (2005) · Endocrinology · doi:10.1210/en.2005-1051 · Cited by 184 · see citing works
Self-citationAcosta-Galvan, G., Yi, C., van der Vliet, J., Jhamandas, J. H., Panula, P., Castellanos, A., Basualdo, M. D. C., Escobar, C., & Buijs, R. M. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1015551108 · Cited by 179 · see citing works
Self-citationNeural Circuitry in the Regulation of Adrenal Corticosterone Rhythmicity
Engeland, W. C., & Arnhold, M. M. (2005) · Endocrine · doi:10.1385/endo:28:3:325 · Cited by 178 · see citing works
Buijs, R. M., & van Eden, C. G. (2000) · Progress in brain research · doi:10.1016/s0079-6123(00)26011-1 · Cited by 176 · see citing works
Self-citationSuprachiasmatic pacemaker organization analyzed by viral transynaptic transport
Leak, R. K., Card, J. P., & Moore, R. Y. (1999) · Brain Research · doi:10.1016/s0006-8993(98)01317-1 · Cited by 164 · see citing works
la Fleur, S. E., Kalsbeek, A., Wortel, J., & Buijs, R. M. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02423-9 · Cited by 160 · see citing works
Self-citationThe regulation of neuroendocrine function: Timing is everything
Kriegsfeld, L. J., & Silver, R. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.12.011 · Cited by 146 · see citing works
Circadian Control of Insulin Secretion Is Independent of the Temporal Distribution of Feeding
Kalsbeek, A., & Strubbe, J. H. (1998) · Physiology & Behavior · doi:10.1016/s0031-9384(97)00493-9 · Cited by 142 · see citing works
Kriegsfeld, L. J., Leak, R. K., Yackulic, C. B., LeSauter, J., & Silver, R. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10995 · Cited by 137 · see citing works
Buijs, R. M., Hou, Y., Shinn, S., & Renaud, L. P. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903400308 · Cited by 134 · see citing works
Self-citationPickard, G. E., Smeraski, C. A., Tomlinson, C. C., Banfield, B. W., Kaufman, J. D., Wilcox, C. L., Enquist, L. W., & Sollars, P. J. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-07-02701.2002 · Cited by 133 · see citing works
The Biological Clock: The Bodyguard of Temporal Homeostasis
Perreau‐Lenz, S., Pévet, P., Buijs, R., & Kalsbeek, A. (2004) · Chronobiology International · doi:10.1081/cbi-120027984 · Cited by 140 · see citing works
Self-citationKalsbeek, A., Buijs, R. M., Engelmann, M., Wotjak, C., & Landgraf, R. (1995) · Brain Research · doi:10.1016/0006-8993(95)00324-j · Cited by 131 · see citing works
Self-citationVrang, N., Larsen, P. J., & Mikkelsen, J. D. (1995) · Brain Research · doi:10.1016/0006-8993(95)00425-p · Cited by 123 · see citing works
Topographical organization of the rat suprachiasmatic‐paraventriocular projection
Vrang, N., Larsen, P. J., Møller, M., & Mikkelsen, J. D. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903530409 · Cited by 119 · see citing works
Buijs, R., Hermes, M., & Kalsbeek, A. (1998) · Progress in Brain Research · doi:10.1016/s0079-6123(08)61581-2 · Cited by 118 · see citing works
Self-citationKruijver, F. P. M., Balesar, R. A., Espila, A. M., Unmehopa, U. A., & Swaab, D. F. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10899 · Cited by 116 · see citing works
A Network of (Autonomic) Clock Outputs
Kalsbeek, A., Perreau‐Lenz, S., & Buijs, R. (2006) · Chronobiology International · doi:10.1080/07420520500464528 · Cited by 114 · see citing works
Self-citationWatts, A. G., Tanimura, S. M., & Sanchez‐Watts, G. (2003) · Endocrinology · doi:10.1210/en.2003-0394 · Cited by 109 · see citing works
Teclemariam‐Mesbah, R., Kalsbeek, A., Pévet, P., & Buijs, R. M. (1997) · Brain Research · doi:10.1016/s0006-8993(96)01246-2 · Cited by 104 · see citing works
Self-citationBuijs, R. M., Wortel, J., van Heerikhuize, J. J., & Kalsbeek, A. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00234-5 · Cited by 103 · see citing works
Self-citationThe circadian system and the balance of the autonomic nervous system
Buijs, R. M., Escobar, C., & Swaab, D. F. (2013) · Handbook of clinical neurology · doi:10.1016/b978-0-444-53491-0.00015-8 · Cited by 100 · see citing works
Self-citationShekhar, A., Keim, S. R., Simon, J. R., & McBride, W. J. (1996) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(96)00077-9 · Cited by 100 · see citing works
Castel, M., & Morris, J. F. (2000) · Journal of Anatomy · doi:10.1046/j.1469-7580.2000.19610001.x · Cited by 100 · see citing works
Goncharuk, V. D., Van Heerikhuize, J., Swaab, D. F., & Buijs, R. M. (2002) · Journal of Comparative Neurology · doi:10.1002/cne.10124 · Cited by 97 · see citing works
Self-citationBuijs, R. M., Wortel, J., & Hou, Y. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903580304 · Cited by 93 · see citing works
Self-citationA Network of (Autonomic) Clock Outputs
Kalsbeek, A., Perreau‐Lenz, S., & Buijs, R. (2006) · Chronobiology International · doi:10.1080/07420520600651073 · Cited by 35 · see citing works
Self-citationDai, J., Swaab, D. F., & Buijs, R. M. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970714)383:4 · Cited by 91 · see citing works
Self-citationHermes, M. L. H. J., Ruijter, J. M., Klop, A., Buijs, R. M., & Renaud, L. P. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.83.2.705 · Cited by 89 · see citing works
Self-citationEgli, M., Bertram, R., Sellix, M. T., & Freeman, M. E. (2004) · Endocrinology · doi:10.1210/en.2003-1710 · Cited by 88 · see citing works
Entrainment to Feeding but Not to Light: Circadian Phenotype of VPAC2Receptor-Null Mice
Sheward, W. J., Maywood, E. S., French, K. L., Horn, J. M., Hastings, M. H., Seckl, J. R., Holmes, M. C., & Harmar, A. J. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.4843-06.2007 · Cited by 86 · see citing works
Jiang, W., Li, S., Zhou, S., Sun, Y., Shi, J., & Lü, L. (2011) · Brain Research · doi:10.1016/j.brainres.2011.05.001 · Cited by 83 · see citing works
Human retinohypothalamic tract as revealed by in vitro postmortem tracing
Dai, J., van der Vliet, J., Swaab, D. F., & Buijs, R. M. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19980803)397:3 · Cited by 83 · see citing works
Self-citationThe Retinohypothalamic tract: Comparison of axonal projection patterns from four major targets
Canteras, N. S., Ribeiro-Barbosa, É. R., Goto, M., Cipolla‐Neto, J., & Swanson, L. W. (2010) · Brain Research Reviews · doi:10.1016/j.brainresrev.2010.09.006 · Cited by 79 · see citing works
Gillette, M. U., Abbott, S. M., & Arnold, J. M. (2012) · Sleep Medicine Clinics · doi:10.1016/j.jsmc.2012.06.001 · Cited by 79 · see citing works
Kriegsfeld, L. J., Korets, R., & Silver, R. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02431.x · Cited by 75 · see citing works
The Diurnal Modulation of Hormonal Responses in the Rat Varies with Different Stimuli
Kalsbeek, A., Ruiter, M., la Fleur, S. E., Heijningen, C. L. V., & Buijs, R. M. (2003) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2003.01112.x · Cited by 73 · see citing works
Self-citationThe Concept of Coupling in the Mammalian Circadian Clock Network
Pilorz, V., Astiz, M., Heinen, K. O., Rawashdeh, O., & Oster, H. (2020) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.12.037 · Cited by 70 · see citing works
Russo, K. A., La, J. L., Stephens, S. B. Z., Poling, M. C., Padgaonkar, N. A., Jennings, K. J., Piekarski, D. J., Kauffman, A. S., & Kriegsfeld, L. J. (2015) · Endocrinology · doi:10.1210/en.2014-1762 · Cited by 70 · see citing works
Κalamatianos, T., Kalló, I., Piggins, H. D., & Coen, C. W. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20168 · Cited by 70 · see citing works
Effect of lesioning the suprachiasmatic nuclei on behavioral despair in rats
Tataroğlu, Ö., Aksoy, A., Yılmaz, A., & Canbeyli, R. (2004) · Brain Research · doi:10.1016/j.brainres.2003.11.063 · Cited by 69 · see citing works
Russell, G., Kalafatakis, K., & Lightman, S. (2015) · Journal of neuroendocrinology · doi:10.1111/jne.12247 · Cited by 64 · see citing works
Tonsfeldt, K. J., & Chappell, P. E. (2011) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2011.07.003 · Cited by 66 · see citing works
Cai, A., Scarbrough, K., Hinkle, D. A., & Wise, P. M. (1997) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1997.273.5.r1764 · Cited by 66 · see citing works
Rhythmicity matters: Circadian and ultradian patterns of HPA axis activity.
Focke, C. M. B., & Iremonger, K. J. (2019) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2019.110652 · Cited by 57 · see citing works
Keim, S. R., & Shekhar, A. (1996) · Brain Research · doi:10.1016/s0006-8993(96)00810-4 · Cited by 63 · see citing works
Guerrero‐Vargas, N. N., Salgado‐Delgado, R., Basualdo, M. D. C., García, J., Guzmán‐Ruiz, M. A., Carrero, J. C., Escobar, C., & Buijs, R. M. (2014) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2014.05.012 · Cited by 62 · see citing works
Self-citationBuijs, R. M. (1996) · Progress in brain research · doi:10.1016/s0079-6123(08)60411-2 · Cited by 62 · see citing works
Self-citationMeng, D., Li, H.-Q., Deisseroth, K. A., Leutgeb, S., & Spitzer, N. C. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1801598115 · Cited by 61 · see citing works
Effects of alcohol on the synthesis and expression of hypothalamic peptides
Madeira, M. D., & Paula-Barbosa, M. M. (1999) · Brain Research Bulletin · doi:10.1016/s0361-9230(98)00131-2 · Cited by 60 · see citing works
The suprachiasmatic nucleus is part of a neural feedback circuit adapting blood pressure response
Buijs, F. N., Cázarez‐Márquez, F., Basualdo, M. C., Scheer, F. A. J. L., Perusquı́a, M., Centurión, D., & Buijs, R. M. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.02.018 · Cited by 53 · see citing works
Self-citationRestricted Daytime Feeding Modifies Suprachiasmatic Nucleus Vasopressin Release in Rats
Kalsbeek, A., van Heerikhuize, J. J., Wortel, J., & Buijs, R. M. (1998) · Journal of Biological Rhythms · doi:10.1177/074873098128999880 · Cited by 53 · see citing works
Self-citationHippocampal spine changes across the sleep–wake cycle: corticosterone and kinases
Ikeda, M., Hojo, Y., Komatsuzaki, Y., Okamoto, M., Kato, A., Takeda, T., & Kawato, S. (2015) · Journal of Endocrinology · doi:10.1530/joe-15-0078 · Cited by 49 · see citing works
Moore, R. Y., & Leak, R. K. (2001) · Handbook of behavioral neurobiology · doi:10.1007/978-1-4615-1201-1_7 · Cited by 49 · see citing works
Douglas, A. J. (2005) · Techniques in the behavioral and neural sciences · doi:10.1016/s0921-0709(05)80014-8 · Cited by 48 · see citing works
Munch, I. C., Møller, M., Larsen, P. J., & Vrang, N. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.1421 · Cited by 47 · see citing works
Jiang, W., Li, S., Liu, J.-F., Sun, Y., Zhou, S., Zhu, W., Shi, J., & Lü, L. (2012) · Psychopharmacology · doi:10.1007/s00213-012-2941-4 · Cited by 45 · see citing works
Girotti, M., Weinberg, M., & Spencer, R. L. (2007) · Endocrinology · doi:10.1210/en.2006-1304 · Cited by 40 · see citing works
Vrang, N., Mikkelsen, J. D., & Larsen, P. J. (1997) · Brain Research Bulletin · doi:10.1016/s0361-9230(97)00138-x · Cited by 44 · see citing works
Immunohistochemical localization of caffeine-induced c-Fos protein expression in the rat brain
Bennett, H. J., & Semba, K. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19981109)401:1 · Cited by 41 · see citing works
Self-citationZaretskaia, M. V., Zaretsky, D. V., Sarkar, S., Shekhar, A., & DiMicco, J. A. (2008) · Brain Research · doi:10.1016/j.brainres.2008.01.018 · Cited by 41 · see citing works
Lakhdar‐Ghazal, N., Dubois‐Dauphin, M., Hermes, M. L. H. J., Buijs, R. M., Bengelloun, W. A., & Pévet, P. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903580404 · Cited by 41 · see citing works
Self-citationAge-related changes in the diurnal rhythm of CRH gene expression in the paraventricular nuclei
Cai, A., & Wise, P. M. (1996) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1996.270.2.e238 · Cited by 41 · see citing works
Aydin, A., Selvi, Y., Besiroglu, L., Boysan, M., Atli, A., Ozdemir, O., Kilic, S., & Balaharoglu, R. (2013) · Journal of Affective Disorders · doi:10.1016/j.jad.2013.04.007 · Cited by 40 · see citing works
Probst, J. C., Skutella, T., Müller-Schmid, A., Jirikowski, G. F., & Hoffmann, W. (1995) · Molecular Brain Research · doi:10.1016/0169-328x(95)00137-h · Cited by 39 · see citing works
Kalsbeek, A., & Buijs, R. M. (1996) · Progress in brain research · doi:10.1016/s0079-6123(08)60414-8 · Cited by 37 · see citing works
Self-citationAhn, R. S., Choi, J. H., Choi, B. C., Kim, J., Lee, S. H., & Sung, S. S. (2011) · Journal of Endocrinology · doi:10.1530/joe-11-0247 · Cited by 35 · see citing works
Circadian Regulation of Cortisol Release in Behaviorally Split Golden Hamsters
Lilley, T. R., Wotus, C., Taylor, D. J., Lee, J. M., & de la Iglesia, H. O. (2011) · Endocrinology · doi:10.1210/en.2011-1624 · Cited by 32 · see citing works
Mitome, M., Honma, S., Yoshihara, T., & Honma, K. (1994) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1994.266.4.e606 · Cited by 32 · see citing works
Chun, S.-J., Niijima, A., Nagai, N., & Nagai, K. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00854-3 · Cited by 31 · see citing works
Nakaya, M., Sanada, K., & Fukada, Y. (2003) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(03)00791-5 · Cited by 29 · see citing works
Mattson, M. P., & Guo, Q. (1997) · Journal of Neuroscience Research · doi:10.1002/(sici)1097-4547(19971115)50:4 · Cited by 52 · see citing works
Organization of the neuroendocrine and autonomic hypothalamic paraventricular nucleus
Kalsbeek, A., & Buijs, R. M. (2021) · Handbook of clinical neurology · doi:10.1016/b978-0-12-820107-7.00004-5 · Cited by 27 · see citing works
Self-citation
- Authors
- Buijs, R. M., Markman, M., Nunes‐Cardoso, B., Hou, Y., & Shinn, S.
- Corresponding author
- Buijs, Ruud M.
- ORCID
- Buijs, Ruud M.
- Venue
- Journal of Comparative Neurology
- Publisher
- Wiley
- Published
- 1993-09
- Volume
- 335
- Issue
- 1
- Pages
- 42-54
- ISSN
- 0021-9967 (ISSN-L)
- 1096-9861
- OpenAlex
- W2026488175
- Cited by
- 153
- References
- 27
- Citations by year
- 2026: 2 · 2023: 1 · 2022: 4 · 2021: 3 · 2020: 1 · 2019: 3 · 2018: 1 · 2017: 1 · 2015: 4 · 2014: 5 · 2013: 5 · 2012: 5
- FWCI
- 3.69
- Type
- journal article
- Language
- en
- Open access
- green
- pure.knaw.nl
- Licence
- Locations
- The Journal of Comparative Neurology (publishedVersion)
- PubMed (publishedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- KNAW Research Portal (The Royal Netherlands Academy of Arts and Sciences) (submittedVersion)
- Funders
- Medical Research Council
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Keywords
- suprachiasmatic nucleus, hypothalamus, corticosteroid secretion, c-fos, paraventricular nucleus, dorsomedial hypothalamus, stress response, daily rhythms, ACTH, interneurons
- MeSH terms
- Adrenal Cortex Hormones, Adrenocorticotropic Hormone, Animals, Efferent Pathways, Immunohistochemistry, Male, Microscopy, Microscopy, Electron, Neurons, Phytohemagglutinins, Staining and Labeling, Stress, Physiological, Suprachiasmatic Nucleus, Vasoactive Intestinal Peptide, Vasopressins, Proto-Oncogene Proteins c-fos, Rats, Wistar, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review