Advertisement

Action of Light on the Neuroendocrine Axis

Chapter
  • 65 Downloads
Part of the Masterclass in Neuroendocrinology book series (MANEURO, volume 10)

Abstract

Photoentrainment of the circadian clock located in the hypothalamic suprachiasmatic nucleus (SCN) is fundamental for the stable regulation of neuroendocrine function underlying physiological functions such as metabolism, sleep, immune responses, and reproduction. Masking by light directly suppresses melatonin secretion independent of the circadian system, with impact on several neuroendocrine axes. This chapter describes recent findings in anatomy and physiology on how light mediates its effects on SCN-regulated timing of the neuroendocrine system, including the hypothalamic-pituitary-adrenal (HPA) axis, the hypothalamic-pituitary-thyroid (HPT) axis, the hypothalamic-pituitary-gonadal (HPG) axis, and melatonin and arginine-vasopressin (AVP) secretion. In modern societies, artificial light at night (ALAN) seems to affect circadian and neuroendocrine systems, and should be considered in the understanding the health problems of the industrialized human population.

Keywords

Photoreceptors Neurotransmitters Neuroendocrine Circadian Seasonal 

Notes

Acknowledgments

This work was supported by the Danish Biotechnology Center for Cellular Communication.

References

  1. Arendt J (2009) Melatonin. In: Binder MD, Hirokawa N, Windhorst U (eds) Encyclopedia of neuroscience. Springer, Berlin, pp 2297–2302CrossRefGoogle Scholar
  2. Bechtold DA, Brown TM, Luckman SM, Piggins HD (2008) Metabolic rhythm abnormalities in mice lacking VIP-VPAC2 signaling. Am J Physiol Regul Integr Comp Physiol 294(2):R344–RR51PubMedCrossRefGoogle Scholar
  3. Berson DM, Dunn FA, Takao M (2002) Phototransduction by retinal ganglion cells that set the circadian clock. Science 295(5557):1070–1073PubMedCrossRefGoogle Scholar
  4. Binder MD, Hirokawa N, Windhorst U (2009) Neuroendocrine axis. In: Binder MD, Hirokawa N, Windhorst U (eds) Encyclopedia of neuroscience. Springer, BerlinCrossRefGoogle Scholar
  5. Bunger MK, Wilsbacher LD, Moran SM, Clendenin C, Radcliffe LA, Hogenesch JB et al (2000) Mop3 is an essential component of the master circadian pacemaker in mammals. Cell 103(7):1009–1017PubMedPubMedCentralCrossRefGoogle Scholar
  6. Challet E (2015) Keeping circadian time with hormones. Diabetes Obes Metab 17(Suppl 1):76–83.  https://doi.org/10.1111/dom.12516CrossRefPubMedGoogle Scholar
  7. Chen D, Buchanan GF, Ding JM, Hannibal J, Gillette MU (1999) PACAP: a pivotal modulator of glutamatergic regulation of the suprachiasmatic circadian clock. Proc Natl Acad Sci U S A 96(23):13409–13414CrossRefGoogle Scholar
  8. Cinzano PFF, Elvidge CD (2001) The first world atlas of the artificial night sky brightness. Mon Not R Astron Soc 328:689–707CrossRefGoogle Scholar
  9. Czeisler CA, Shanahan TL, Klerman EB, Martens H, Brotman DJ, Emens JS et al (1995) Suppression of melatonin secretion in some blind patients by exposure to bright light. N Engl J Med 332(1):6–11PubMedCrossRefPubMedCentralGoogle Scholar
  10. Czeisler CA, Duffy JF, Shanahan TL, Brown EN, Mitchell JF, Rimmer DW et al (1999) Stability, precision, and near-24-hour period of the human circadian pacemaker. Science 284(5423):2177–2181PubMedCrossRefPubMedCentralGoogle Scholar
  11. Daan S, Aschoff J (2001) The entrainment of circadian systems. In: Takahashi JS, Turek FW, Moore RY (eds) Circadian clocks. Handbook of behavioral neurobiology. Kluwer Academic/Plenum Publisher, New York, pp 7–43CrossRefGoogle Scholar
  12. Daan S, Pittendrigh CS (1976a) A functional analysis of circadian pacemakers in nocturnal rodents. II. The variability of phase response curves. J Comp Physiol 106:253–266CrossRefGoogle Scholar
  13. Daan S, Pittendrigh CS (1976b) A functional analysis of the circadian pacemakers in nocturnal rodents. IV. Entrainment: pacemaker and clock. J Comp Physiol 106:253–266CrossRefGoogle Scholar
  14. Dacey DM, Liao HW, Peterson BB, Robinson FR, Smith VC, Pokorny J et al (2005) Melanopsin-expressing ganglion cells in primate retina signal color and irradiance and project to the LGN. Nature 433(7027):749–754PubMedCrossRefPubMedCentralGoogle Scholar
  15. Do MT, Yau KW (2010) Intrinsically photosensitive retinal ganglion cells. Physiol Rev 90(4):1547–1581PubMedPubMedCentralCrossRefGoogle Scholar
  16. Duffy JF, Czeisler CA (2009) Effect of light on human circadian physiology. Sleep Med Clin 4(2):165–177PubMedPubMedCentralCrossRefGoogle Scholar
  17. Ecker JL, Dumitrescu ON, Wong KY, Alam NM, Chen SK, LeGates T et al (2010) Melanopsin-expressing retinal ganglion-cell photoreceptors: cellular diversity and role in pattern vision. Neuron 67(1):49–60PubMedPubMedCentralCrossRefGoogle Scholar
  18. Engelmann M, Landgraf R (1997) Intracerebral release of vasopressin and oxytocin: new aspects of the old concept of neurosecretion. In: Korf H-W, Usadel K-H (eds) Neuroendocrinology Retrospect and perspectives. Springer, Berlin, pp 87–97Google Scholar
  19. Fonken LK, Workman JL, Walton JC, Weil ZM, Morris JS, Haim A et al (2010) Light at night increases body mass by shifting the time of food intake. Proc Natl Acad Sci U S A 107(43):18664–18669PubMedPubMedCentralCrossRefGoogle Scholar
  20. Foster RG, Provencio I, Hudson D, Fiske S, De Grip W, Menaker M (1991) Circadian photoreception in the retinally degenerate mouse (rd/rd). J Comp Physiol A 169(1):39–50PubMedCrossRefPubMedCentralGoogle Scholar
  21. Freedman MS, Lucas RJ, Soni B, von Schantz M, Muñoz M, David-Gray Z et al (1999) Regulation of mammalian circadian behavior by non-rod, non-cone, ocular photoreceptors. Science 284:502–504PubMedCrossRefPubMedCentralGoogle Scholar
  22. Golombek DA, Rosenstein RE (2010) Physiology of circadian entrainment. Physiol Rev 90(3):1063–1102PubMedCrossRefPubMedCentralGoogle Scholar
  23. Gooley JJ, Lu J, Chou TC, Scammell TE, Saper CB (2001) Melanopsin in cells of origin of the retinohypothalamic tract. Nat Neurosci 12:1165CrossRefGoogle Scholar
  24. Grattan DR (2015) 60 years of neuroendocrinology: the hypothalamo-prolactin axis. J Endocrinol 226(2):T101–T122PubMedPubMedCentralCrossRefGoogle Scholar
  25. Guler AD, Ecker JL, Lall GS, Haq S, Altimus CM, Liao HW et al (2008) Melanopsin cells are the principal conduits for rod-cone input to non-image-forming vision. Nature 453(7191):102–105PubMedPubMedCentralCrossRefGoogle Scholar
  26. Hannibal J (2002) Neurotransmitters of the retino-hypothalamic tract. Cell Tissue Res 309(1):73–88PubMedCrossRefPubMedCentralGoogle Scholar
  27. Hannibal J (2006) Roles of PACAP-containing retinal ganglion cells in circadian timing. Int Rev Cytol 251:1–39PubMedCrossRefPubMedCentralGoogle Scholar
  28. Hannibal J (2016) PACAP in the circadian timing system: learning from knockout models. Pituitary adenylate activating polypeptide—PACAP. Current topics in neurotoxicity. Springer, Switzerland, pp 227–237CrossRefGoogle Scholar
  29. Hannibal J, Fahrenkrug J (2004) Target areas innervated by PACAP immunoreactive retinal ganglion cells. Cell Tissue Res 316(1):99–113PubMedCrossRefPubMedCentralGoogle Scholar
  30. Hannibal J, Moller M, Ottersen OP, Fahrenkrug J (2000) PACAP and glutamate are co-stored in the retinohypothalamic tract. J Comp Neurol 418:147–155PubMedCrossRefGoogle Scholar
  31. Hannibal J, Brabet P, Jamen F, Nielsen HS, Journot L, Fahrenkrug J (2001) Dissociation between light induced phase shift of the circadian rhythm and clock gene expression in mice lacking the PACAP type 1 receptor (PAC1). J Neurosci 21(13):4883–4890PubMedPubMedCentralCrossRefGoogle Scholar
  32. Hannibal J, Hindersson P, Knudsen SM, Georg B, Fahrenkrug J (2002) The photopigment melanopsin is exclusively present in PACAP containing retinal ganglion cells of the retinohypothalamic tract. J Neurosci 22:RC191:1–7CrossRefGoogle Scholar
  33. Hannibal J, Brabet P, Fahrenkrug J (2008) Mice lacking the PACAP type I receptor have impaired photic entrainment and negative masking. Am J Physiol Regul Integr Comp Physiol 295(6):R2050–R20R8PubMedCrossRefGoogle Scholar
  34. Hannibal J, Hsiung HM, Fahrenkrug J (2011) Temporal phasing of locomotor activity, heart rate rhythmicity, and core body temperature is disrupted in VIP receptor 2-deficient mice. Am J Physiol Regul Integr Comp Physiol 300(3):R519–R530.  https://doi.org/10.1152/ajpregu.00599.2010CrossRefPubMedGoogle Scholar
  35. Hannibal J, Kankipati L, Strang CE, Peterson BB, Dacey D, Gamlin PD (2014) Central projections of intrinsically photosensitive retinal ganglion cells in the macaque monkey. J Comp Neurol 522(10):2231–2248PubMedCrossRefGoogle Scholar
  36. Hannibal J, Christiansen AT, Heegaard S, Fahrenkrug J, Kiilgaard JF (2017) Melanopsin expressing human retinal ganglion cells: subtypes, distribution, and intraretinal connectivity. J Comp Neurol 525(8):1934–1961.  https://doi.org/10.1002/cne.24181CrossRefPubMedGoogle Scholar
  37. Hansen J (2001) Light at night, shiftwork, and breast cancer risk. J Natl Cancer Inst 93(20):1513–1515PubMedCrossRefPubMedCentralGoogle Scholar
  38. Hatori M, Le H, Vollmers C, Keding SR, Tanaka N, Schmedt C et al (2008) Inducible ablation of melanopsin-expressing retinal ganglion cells reveals their central role in non-image forming visual responses. PLoS One 3(6):e2451PubMedPubMedCentralCrossRefGoogle Scholar
  39. Hattar S, Liao HW, Takao M, Berson DM, Yau KW (2002) Melanopsin-containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science 295(5557):1065–1070PubMedPubMedCentralCrossRefGoogle Scholar
  40. Hattar S, Lucas RJ, Mrosovsky N, Thompson S, Douglas RH, Hankins MW et al (2003) Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice. Nature 424(6944):76–81PubMedPubMedCentralCrossRefGoogle Scholar
  41. Hattar S, Kumar M, Park A, Tong P, Tung J, Yau KW et al (2006) Central projections of melanopsin-expressing retinal ganglion cells in the mouse. J Comp Neurol 497(3):326–349PubMedPubMedCentralCrossRefGoogle Scholar
  42. Hazlerigg D, Loudon A (2008) New insights into ancient seasonal life timers. Curr Biol 18(17):R795–R804.  https://doi.org/10.1016/j.cub.2008.07.040CrossRefPubMedGoogle Scholar
  43. Hughes S, Watson TS, Foster RG, Peirson SN, Hankins MW (2013) Nonuniform distribution and spectral tuning of photosensitive retinal ganglion cells of the mouse retina. Curr Biol 23(17):1696–1701PubMedPubMedCentralCrossRefGoogle Scholar
  44. Hughes S, Jagannath A, Hankins MW, Foster RG, Peirson SN (2015) Photic regulation of clock systems. Methods Enzymol 552:125–143.  https://doi.org/10.1016/bs.mie.2014.10.018CrossRefPubMedGoogle Scholar
  45. Husse J, Leliavski A, Tsang AH, Oster H, Eichele G (2014) The light-dark cycle controls peripheral rhythmicity in mice with a genetically ablated suprachiasmatic nucleus clock. FASEB J 28(11):4950–4960.  https://doi.org/10.1096/fj.14-256594CrossRefPubMedGoogle Scholar
  46. Hut RA (2011) Photoperiodism: shall EYA compare thee to a summer’s day? Curr Biol 21(1):R22–R25.  https://doi.org/10.1016/j.cub.2010.11.060CrossRefPubMedGoogle Scholar
  47. Kalsbeek A, Buijs RM (2002) Output pathways of the mammalian suprachiasmatic nucleus: coding circadian time by transmitter selection and specific targeting. Cell Tissue Res 309(1):109–118.  https://doi.org/10.1007/s00441-002-0577-0CrossRefPubMedGoogle Scholar
  48. Kalsbeek A, Palm IF, La Fleur SE, Scheer FA, Perreau-Lenz S, Ruiter M et al (2006) SCN outputs and the hypothalamic balance of life. J Biol Rhythms 21(6):458–469.  https://doi.org/10.1177/0748730406293854CrossRefPubMedGoogle Scholar
  49. Keenan WT, Rupp AC, Ross RA, Somasundaram P, Hiriyanna S, Wu Z et al (2016) A visual circuit uses complementary mechanisms to support transient and sustained pupil constriction. Elife 5:e15392PubMedPubMedCentralCrossRefGoogle Scholar
  50. Kennett JE, Poletini MO, Freeman ME (2008) Vasoactive intestinal polypeptide modulates the estradiol-induced prolactin surge by entraining oxytocin neuronal activity. Brain Res 1196:65–73PubMedPubMedCentralCrossRefGoogle Scholar
  51. Kiessling S, Sollars PJ, Pickard GE (2014) Light stimulates the mouse adrenal through a retinohypothalamic pathway independent of an effect on the clock in the suprachiasmatic nucleus. PLoS One 9(3):e92959PubMedPubMedCentralCrossRefGoogle Scholar
  52. Klein DC, Moore RY, Reppert SM (1991) Suprachiasmatic nucleus. The mind’s clock. Oxford University Press, New YorkGoogle Scholar
  53. Klerman EB, Shanahan TL, Brotman DJ, Rimmer DW, Emens JS, Rizzo JF III et al (2002) Photic resetting of the human circadian pacemaker in the absence of conscious vision. J Biol Rhythms 17(6):548–555PubMedCrossRefPubMedCentralGoogle Scholar
  54. Kloog I, Stevens RG, Haim A, Portnov BA (2010) Nighttime light level co-distributes with breast cancer incidence worldwide. Cancer Causes Control 21(12):2059–2068.  https://doi.org/10.1007/s10552-010-9624-4CrossRefPubMedPubMedCentralGoogle Scholar
  55. Larsen PJ, Enquist LW, Card JP (1998) Characterization of the multisynaptic neuronal control of the rat pineal gland using viral transneuronal tracing. Eur J Neurosci 10(1):128–145PubMedCrossRefPubMedCentralGoogle Scholar
  56. Liao HW, Ren X, Peterson BB, Marshak DW, Yau KW, Gamlin PD et al (2016) Melanopsin-expressing ganglion cells in macaque and human retinas form two morphologically distinct populations. J Comp Neurol 524(14):2845–2872.  https://doi.org/10.1002/cne.23995CrossRefPubMedPubMedCentralGoogle Scholar
  57. Lincoln GA, Clarke IJ, Hut RA, Hazlerigg DG (2006) Characterizing a mammalian circannual pacemaker. Science 314(5807):1941–1944.  https://doi.org/10.1126/science.1132009CrossRefGoogle Scholar
  58. Lucas RJ, Peirson SN, Berson DM, Brown TM, Cooper HM, Czeisler CA et al (2014) Measuring and using light in the melanopsin age. Trends Neurosci 37(1):1–9PubMedCrossRefPubMedCentralGoogle Scholar
  59. Mohawk JA, Takahashi JS (2011) Cell autonomy and synchrony of suprachiasmatic nucleus circadian oscillators. Trends Neurosci 34(7):349–358PubMedPubMedCentralCrossRefGoogle Scholar
  60. Moore RY (1995) Organization of the mammalian circadian system. Ciba Found Symp 183:88–99PubMedPubMedCentralGoogle Scholar
  61. Moore RY, Lenn NJ (1972) A retinohypothalamic projection in the rat. J Comp Neurol 146:1–14PubMedCrossRefPubMedCentralGoogle Scholar
  62. Moore RY, Speh JC, Card JP (1995) The retinohypothalamic tract originates from a distinct subset of retinal ganglion cells. J Comp Neurol 352:351–366PubMedCrossRefPubMedCentralGoogle Scholar
  63. Morin LP, Allen CN (2005) The circadian visual system, 2005. Brain Res Rev 51(1):1–60PubMedCrossRefPubMedCentralGoogle Scholar
  64. Mrosovsky N (1999) Masking: history, definitions, and measurement. Chronobiol Int 16(4):415–429PubMedCrossRefPubMedCentralGoogle Scholar
  65. Navara KJ, Nelson RJ (2007) The dark side of light at night: physiological, epidemiological, and ecological consequences. J Pineal Res 43(3):215–224.  https://doi.org/10.1111/j.1600-079X.2007.00473.xCrossRefPubMedPubMedCentralGoogle Scholar
  66. Nelson RJ, Zucker I (1981) Absence of extraocular photoreception in diurnal and nocturnal rodents exposed to direct sunlight. Comp Biochem Physiol 69A:145–148CrossRefGoogle Scholar
  67. Ouyang JQ, Davies S, Dominoni D (2018) Hormonally mediated effects of artificial light at night on behavior and fitness: linking endocrine mechanisms with function. J Exp Biol 221(Pt 6):jeb156893PubMedPubMedCentralCrossRefGoogle Scholar
  68. Panda S, Provencio I, Tu DC, Pires SS, Rollag MD, Castrucci AM et al (2003) Melanopsin is required for non-image-forming photic responses in blind mice. Science 301(5632):525–527PubMedCrossRefPubMedCentralGoogle Scholar
  69. Pevet P, Challet E (2011) Melatonin: both master clock output and internal time-giver in the circadian clocks network. J Physiol Paris 105(4–6):170–182.  https://doi.org/10.1016/j.jphysparis.2011.07.001CrossRefPubMedPubMedCentralGoogle Scholar
  70. Pickard GE (1985) Bifurcating axons of retinal ganglion cells terminate in the hypothalamic suprachiasmatic nucleus and the intergeniculate leaflet of the thalamus. Neurosci Lett 55:211–217PubMedCrossRefGoogle Scholar
  71. Provencio I, Jiang G, De Grip WJ, Hayes WP, Rollag MD (1998) Melanopsin: an opsin in melanophores, brain, and eye. Proc Natl Acad Sci U S A 95(1):340–345PubMedPubMedCentralCrossRefGoogle Scholar
  72. Provencio I, Rodriguez IR, Jiang G, Hayes WP, Moreira EF, Rollag MD (2000) A novel human opsin in the inner retina. J Neurosci 20(0270-6474):600–605PubMedPubMedCentralCrossRefGoogle Scholar
  73. Redlin U, Mrosovsky N (1999) Masking by light in hamsters with SCN lesions. J Comp Physiol A 184(4):439–448PubMedCrossRefGoogle Scholar
  74. Reiter RJ, Tan DX, Galano A (2014) Melatonin: exceeding expectations. Physiology (Bethesda) 29(5):325–333.  https://doi.org/10.1152/physiol.00011.2014CrossRefGoogle Scholar
  75. Roenneberg T, Foster RG (1997) Twilight times: light and the circadian system. Photochem Photobiol 66(5):549–561PubMedCrossRefGoogle Scholar
  76. Saper CB, Cano G, Scammell TE (2005a) Homeostatic, circadian, and emotional regulation of sleep. J Comp Neurol 493(1):92–98PubMedCrossRefGoogle Scholar
  77. Saper CB, Scammell TE, Lu J (2005b) Hypothalamic regulation of sleep and circadian rhythms. Nature 437(7063):1257–1263PubMedCrossRefGoogle Scholar
  78. Schmidt TM, Kofuji P (2009) Functional and morphological differences among intrinsically photosensitive retinal ganglion cells. J Neurosci 29(2):476–482PubMedPubMedCentralCrossRefGoogle Scholar
  79. Shivers BD, Gorcs TJ, Gottschall PE, Arimura A (1991) Two high affinity binding sites for pituitary adenylate cyclase- activating polypeptide have different tissue distributions. Endocrinology 128:3055–3065PubMedCrossRefGoogle Scholar
  80. Van Dycke KC, Rodenburg W, van Oostrom CT, van Kerkhof LW, Pennings JL, Roenneberg T et al (2015) Chronically alternating light cycles increase breast cancer risk in mice. Curr Biol 25(14):1932–1937.  https://doi.org/10.1016/j.cub.2015.06.012CrossRefPubMedPubMedCentralGoogle Scholar
  81. Vosko AM, Schroeder A, Loh DH, Colwell CS (2007) Vasoactive intestinal peptide and the mammalian circadian system. Gen Comp Endocrinol 152(2–3):165–175PubMedPubMedCentralCrossRefGoogle Scholar

Recommended Further Reading

  1. Do MT, Yau KW (2010) Intrinsically photosensitive retinal ganglion cells. Physiol Rev 90(4):1547–1581. A small population of retinal ganglion cells in the mammalian eye that express a unique visual pigment called melanopsin. This review describes the anatomy and physiology of this remarkable system.Google Scholar
  2. Golombek DA, Rosenstein RE (2010) Physiology of circadian entrainment. Physiol Rev 90(3):1063–1102. This paper reviews the anatomy and physiology of the circadian timing system in mammals.Google Scholar
  3. Kalsbeek A, Palm IF, La Fleur SE, Scheer FA, Perreau-Lenz S, Ruiter M et al (2006) SCN outputs and the hypothalamic balance of life. J Biol Rhythms 21(6):458–469. This review considers the anatomical connections and neurotransmitters used by the SCN to control the daily rhythms in hormone release.Google Scholar

Copyright information

© The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Department of Clinical BiochemistryBispebjerg Frederiksberg Hospital, University of CopenhagenCopenhagenDenmark

Personalised recommendations