Anatomical demonstration of the suprachiasmatic nucleus–pineal pathway

A polysynaptic pathway is proposed to transmit light information from the retina through the suprachiasmatic nucleus of the hypothalamus (SCN) to the pineal. In the present study, the powerful transneuronal tracer, pseudorabies virus (PRV), was used to provide a detailed description of this pathway. PRV injected into the pineal subsequently labeled the superior cervical ganglion, the intermediolateral column of the upper thoracic cord, the autonomic division of the paraventricular nucleus of the hypothalamus (PVN), and the SCN. Neurons in the autonomic division of the PVN were the only PRV‐labeled neurons in the hypothalamus shown to receive input from the SCN as demonstrated by the presence of vasoactive intestinal polypeptide axonal contacts. This observation concurred with the presence of ventrally placed neurons in the SCN that could only be observed a day after the appearance of PVN‐labeled neurons. Nevertheless the majority of the neurons were found in the dorsomedial position of the SCN, associated with the vasopressin‐containing population of SCN neurons. Confocal laser scanning microscopy showed double‐labeled neurons containing PRV and vasopressin or PRV and vasoactive intestinal polypeptide. Specificity of tracing was also established by prior removal of the superior cervical ganglion, resulting in a complete absence of the tracer but in the pineal. Thus, the present study provides the anatomical basis for circadian control of melatonin secretion. J. Comp. Neurol. 406:171–182, 1999. © 1999 Wiley‐Liss, Inc.

[1]  Larsen,et al.  Characterization of the multisynaptic neuronal control of the rat pineal gland using viral transneuronal tracing , 1998, The European journal of neuroscience.

[2]  K. Mckenna,et al.  Central nervous system innervation of the penis as revealed by the transneuronal transport of pseudorabies virus , 1993, Neuroscience.

[3]  K. Chihara,et al.  Suprachiasmatic nucleus neurons immunoreactive for vasoactive intestinal polypeptide have synaptic contacts with axons immunoreactive for neuropeptide Y: An immunoelectron microscopic study in the rat , 1988, Neuroscience Letters.

[4]  J. Card.  Pseudorabies Virus Replication and Assembly in the Rodent Central Nervous System , 1995 .

[5]  M. Schwab,et al.  Binding, uptake and retrograde axonal transport of herpes virus suis in sympathetic neurons , 1986, Brain Research.

[6]  A. Loewy,et al.  Central Command Neurons of the Sympathetic Nervous System: Basis of the Fight-or-Flight Response , 1995, Science.

[7]  A. Kalsbeek,et al.  Efferent projections of the suprachiasmatic nucleus in the golden hamster (Mesocricetus auratus) , 1993, The Journal of comparative neurology.

[8]  R. F. Johnson,et al.  Paraventricular nucleus efferents mediating photoperiodism in male golden hamsters , 1989, Neuroscience Letters.

[9]  H. Romijn,et al.  Anatomical and functional demonstration of a multisynaptic suprachiasmatic nucleus adrenal (cortex) pathway , 1999, The European journal of neuroscience.

[10]  L. P. Morin,et al.  Projections of the suprachiasmatic nuclei, subparaventricular zone and retrochiasmatic area in the golden hamster , 1994, Neuroscience.

[11]  A. Kalsbeek,et al.  Direct vasoactive intestinal polypeptide-containing projection from the suprachiasmatic nucleus to spinal projecting hypothalamic paraventricular neurons , 1997, Brain Research.

[12]  J. Mikkelsen,et al.  A direct neural projection from the intergeniculate leaflet of the lateral geniculate nucleus to the deep pineal gland of the rat, demonstrated withPhaseolus vulgaris leucoagglutinin , 1990, Brain Research.

[13]  M. Møller.  Fine structure of the pinealopetal innervation of the mammalian pineal gland , 1992, Microscopy research and technique.

[14]  A. Kalsbeek,et al.  A Diurnal Rhythm of Stimulatory Input to the Hypothalamo–Pituitary–Adrenal System as Revealed by Timed Intrahypothalamic Administration of the Vasopressin V1Antagonist , 1996, The Journal of Neuroscience.

[15]  J. Mikkelsen,et al.  Histamine-immunoreactive nerve fibers in the rat pineal gland: evidence for a histaminergic central innervation , 1992, Brain Research.

[16]  J. Korf,et al.  Neuroanatomy of Cardiac Activity‐regulating Circuitry: A Transneuronal Retrograde Viral Labelling Study in the Rat , 1996, The European journal of neuroscience.

[17]  S. Reuss,et al.  Neuropeptide Y‐Containing Neurons in the Rat Superior Cervical Ganglion , 1989, Journal of pineal research.

[18]  A. Strack,et al.  Pseudorabies virus: a highly specific transneuronal cell body marker in the sympathetic nervous system , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  H. Okamura,et al.  Vasoactive intestinal peptide (VIP)-like immunoreactive neurons located in the rat suprachiasmatic nucleus receive a direct retinal projection , 1989, Neuroscience Letters.

[20]  H. Kuypers,et al.  The paraventricular nucleus of the hypothalamus: Cytoarchitectonic subdivisions and organization of projections to the pituitary, dorsal vagal complex, and spinal cord as demonstrated by retrograde fluorescence double‐labeling methods , 1980, The Journal of comparative neurology.

[21]  R. Moore.  Neural control of the pineal gland , 1995, Behavioural Brain Research.

[22]  T. Nishikawa,et al.  N-Methyl-d-aspartate , quisqualate and kainate receptors are all involved in transmission of photic stimulation in the suprachiasmatic nucleus in rats , 1991, Brain Research.

[23]  L W Swanson,et al.  Efferent projections of the suprachiasmatic nucleus: I. Studies using anterograde transport of Phaseolus vulgaris leucoagglutinin in the rat , 1987, The Journal of comparative neurology.

[24]  H. Romijn,et al.  Differences in colocalization between Fos and PHI, GRP, VIP and VP in neurons of the rat suprachiasmatic nucleus after a light stimulus during the phase delay versus the phase advance period of the night , 1996, The Journal of comparative neurology.

[25]  L. Renaud,et al.  Ultrastructural evidence for intra‐ and extranuclear projections of GABAergic neurons of the suprachiasmatic nucleus , 1994, The Journal of comparative neurology.

[26]  J. Roppolo,et al.  Transneuronal labeling of neurons in the adult rat brainstem and spinal cord after injection of pseudorabies virus into the urethra , 1995, The Journal of comparative neurology.

[27]  L. Renaud,et al.  GABA and glutamate mediate rapid neurotransmission from suprachiasmatic nucleus to hypothalamic paraventricular nucleus in rat. , 1996, The Journal of physiology.

[28]  A. Loewy,et al.  CNS innervation of airway-related parasympathetic preganglionic neurons: a transneuronal labeling study using pseudorabies virus , 1993, Brain Research.

[29]  A. Loewy,et al.  Specificity of pseudorabies virus as a retrograde marker of sympathetic preganglionic neurons: implications for transneuronal labeling studies , 1993, Brain Research.

[30]  L W Swanson,et al.  Efferent projections of the suprachiasmatic nucleus: II. Studies using retrograde transport of fluorescent dyes and simultaneous peptide immunohistochemistry in the rat , 1987, The Journal of comparative neurology.

[31]  T. Nishikawa,et al.  N-methyl-D-aspartate receptor participates in neuronal transmission of photic information through the retinohypothalamic tract. , 1991, Neuroendocrinology.

[32]  D. Klein.  Photoneural regulation of the mammalian pineal gland. , 1985, Ciba Foundation symposium.

[33]  B. Roland,et al.  Local origins of some GABAergic projections to the paraventricular and supraoptic nuclei of the hypothalamus in the rat , 1993, The Journal of comparative neurology.

[34]  D. Klein,et al.  Pinealocyte projections into the mammalian brain revealed with S-antigen antiserum. , 1986, Science.

[35]  L. Schramm,et al.  Peripheral and central pathways regulating the kidney: a study using pseudorabies virus , 1993, Brain Research.

[36]  P. J. Larsen,et al.  Topographical organization of the rat suprachiasmatic‐paraventriocular projection , 1995, The Journal of comparative neurology.

[37]  A. Loewy,et al.  CNS cell groups regulating the sympathetic outflow to adrenal gland as revealed by transneuronal cell body labelling with pseudorabies virus , 1989, Brain Research.

[38]  A. Kalsbeek,et al.  GABA receptors in the region of the dorsomedial hypothalamus of rats are implicated in the control of melatonin and corticosterone release. , 1996, Neuroendocrinology.

[39]  R. Miselis,et al.  Central nervous system neurons labelled following the injection of pseudorabies virus into the rat urinary bladder , 1992, Neuroscience Letters.

[40]  A. Kalsbeek,et al.  Oxytocin innervation of spinal preganglionic neurons projecting to the superior cervical ganglion in the rat , 1997, Cell and Tissue Research.

[41]  A. Kalsbeek,et al.  In vivo measurement of a diurnal variation in vasopressin release in the rat suprachiasmatic nucleus , 1995, Brain Research.

[42]  M. Markman,et al.  Projections of the suprachiasmatic nucleus to stress‐related areas in the rat hypothalamus: A light and electron microscopic study , 1993, The Journal of comparative neurology.

[43]  C. Bowers,et al.  The number and distribution of sympathetic neurons that innervate the rat pineal gland , 1984, Neuroscience.

[44]  J. Luebke,et al.  Characterization of superior cervical ganglion neurons that project to the submandibular glands, the eyes, and the pineal gland in rats , 1992, Brain Research.

[45]  S. Honma,et al.  Light suppression of nocturnal pineal and plasma melatonin in rats depends on wavelength and time of day , 1992, Neuroscience Letters.

[46]  P. J. Larsen,et al.  Direct Link From the Suprachiasmatic Nucleus to Hypothalamic Neurons Projecting to the Spinal Cord: A Combined Tracing Study Using Cholera Toxin Subunit B and Phaseolus vulgaris-Leucoagglutinin , 1997, Brain Research Bulletin.