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The thalamic paraventricular nucleus relays information from the suprachiasmatic nucleus to the amygdala: A combined anterograde and retrograde tracing study in the rat at the light and electron microscopic levels

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Journal of Neurocytology

Abstract

The relationship between efferents of the hypothalamic suprachiasmatic nucleus (SCN) and neurons of the thalamic paraventricular nucleus (PVT) projecting to the amygdala was investigated in the rat using tract tracing in light and electron microscopy. Biotinylated dextran amine was used to label anterogradely SCN efferents. These fibers were found to reach the thalamic midline, terminating in PVT, through three pathways: anterodorsally through the preoptic region, dorsally through the periventricular hypothalamus, and through the contralateral medial hypothalamic and preoptic areas after crossing the midline in the optic chiasm. Preterminal and terminal-like elements labeled from the SCN were distributed throughout the rostrocaudal extent of PVT, with an anteroposterior gradient of density. Labeled terminal elements were densest in the dorsal portion of PVT beneath the ependymal lining and some of them entered the ependyma. Anterograde tracing of SCN fibers was combined with injections of retrograde tracers in the amygdala. Numerous retrogradely labeled cell bodies were seen throughout PVT, with a prevalence in its anterodorsal portion. Overlap was detected between puncta labeled from the SCN and retrogradely labeled neurons, especially in the anterodorsal sector of PVT, where numerous puncta were in close apposition to thalamo-amygdaloid cells. Electron microscopy revealed that boutons labeled from the SCN established synaptic contacts with dendritic profiles of PVT neurons labeled from the amygdala. The findings demonstrate that information processed in the biological clock is conveyed to the amygdala through PVT, indicating that this nucleus plays a role in the transfer of circadian timing information to the limbic system.

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References

  • ARAI, R., KOJIMA, Y., GEFFARD, M., KITAHAMA, K. & MAEDA, T. (1992) Combined use of silver staining of the retrograde tracer WGAapoHRP-Au and pre-embedding immunocytochemistry for electron microscopy: Demonstration of dopaminergic terminals in synaptic contact with striatal neurons projecting to the substantia nigra in the rat. Journal of Histochemistry and Cytochemistry 40, 889-892.

    Google Scholar 

  • BALERCIA, G., BENTIVOGLIO, M. & KRUGER, L. (1992) Fine structural organization of the ependymal region of the paraventricular nucleus of the rat thalamus and its relation with projection neurons. Journal of Neurocytology 21, 105-119.

    Google Scholar 

  • BASBAUM, A. I. & MÉNÉTREY, D. (1987) Wheat germ agglutinin-apoHRP gold: A new retrograde tracer for light-and electron-microscopic single-and double-label studies. Journal of Comparative Neurology 261, 306-318.

    Google Scholar 

  • BENTIVOGLIO, M., BALERCIA, G. & KRUGER, L. (1991) The specificity of the nonspecific thalamus: The midline nuclei. Progress in Brain Research 87, 53-80.

    Google Scholar 

  • BENTIVOGLIO, M., KULTAS-ILINSKY, K. & ILINSKY, I. A. (1993) Limbic thalamus: Structure, intrinsic organization, and connections. In Neurobiology of the Cingulate Cortex and Limbic Thalamus (edited by VOGT, B. A. & GABRIEL, M.) pp. 71-122. Boston: Birkhäuser.

    Google Scholar 

  • BENTIVOGLIO, M. & GRASSI-ZUCCONI, G. (1998) Immediate early gene expression in sleep and wakefulness. In Handbook of Behavioral State Control (edited by LYDIC, R. & BAGHDOYAN, H.) pp. 235-253. Boca Raton, FL: CRC Press.

    Google Scholar 

  • BHATNAGAR, S. & DALLMAN, M. F. (1999) The paraventricular nucleus of the thalamus alters rhythms in core temperature and energy balance in a state dependent manner. Brain Research 851, 66-75.

    Google Scholar 

  • BITTMAN, E. L. & WEAVER, D. R. (1990) The distribution of melatonin binding sites in neuroendocrine tissues of the ewe. Biology of Reproduction 43, 986-993.

    Google Scholar 

  • BOTCHKINA, G. I., LYUBSKY, S. & HAGAG, N. G. (1996) Transient expression of neuropeptide Y (NPY) immunoreactivity in the developing hamster paraventricular thalamic area is due to apoptosis. Cellular and Molecular Neurobiology 16, 649-659.

    Google Scholar 

  • BRANDT, K. M. & APKARIAN, A. V. (1992) Biotin-dextran: A sensitive anterograde tracer for neuroanatomic studies in rat and monkey. Journal of Neuroscience Methods 45, 35-40.

    Google Scholar 

  • BUIJS, R. M. (1996) The anatomical basis for the expression of circadian rhythms: The efferent projections of the suprachiasmatic nucleus. Progress in Brain Research 111, 229-240.

    Google Scholar 

  • CHANG, H. T., KUO, H., WHITTAKER, J. A. & COOPER, N. G. F. (1990) Light and electron microscopic analysis of projection neurons retrogradely labeled with Fluoro-Gold: Notes on the application of antibodies to Fluoro-Gold. Journal of Neuroscience Methods 35, 31-37.

    Google Scholar 

  • CHEN, S. & SU, H. S. (1990) Afferent connections of the thalamic paraventricular and parataenial nuclei in the rat:A retrograde tracing study with iontophoretic application of Fluoro-Gold. Brain Research 522, 1-6.

    Google Scholar 

  • CIRELLI, C., POMPEIANO, M. & TONONI, G. (1993) Fos like immunoreactivity in the rat brain in spontaneous wakefulness and sleep. Archives Italiens de Biologie 131, 327-330.

    Google Scholar 

  • DAI, J., SWAAB, D. F., VAN DER VLIET, J. & BJIS, R. M. (1998) Postmortem tracing reveals the organization of hypothalamic projections of the suprachiasmatic nucleus in the human brain. Journal of Comparative Neurology 400, 87-102.

    Google Scholar 

  • DING, S. L. & ELBERGER, J. (1995) A modification of biotinylated dextran amine histochemistry for labeling the developing mammalian brain. Journal of Neuroscience Methods 57, 67-75.

    Google Scholar 

  • EBLING, F. J. P., MAYWOOD, E. S., HUMBY, T. & HASTINGS, M. H. (1992) Circadian and photoperiodic time measurement in male Syrian hamsters following lesions of the melatonin-binding sites of the paraventricular thalamus. Journal of Biological Rhythms 7, 241-254.

    Google Scholar 

  • FRASSONI, C., SPREAFICO, R. & BENTIVOGLIO, M. (1997) Glutamate, aspartate and co-localization with calbindin in the medial thalamus: An immunohistochemical study in the rat. Experimental Brain Research 115, 95-104.

    Google Scholar 

  • HASTINGS, M. H. (1998) The vertebrate clock: Localisation, connection and entrainment. In Physiology and Pharmacology of Biological Rhythms (edited by REDFERN, P. H. & LEMMER, B.) pp. 1-28. Berlin: Springer.

    Google Scholar 

  • HEREIDA, R., REAL, M. A., SUAREZ, J., GUIRADO, S. & DAVILA, J. C. (2002) A proposed homology between the reptilian dorsomedial thalamic nucleus and the mammalian paraventricular thalamic nucleus. Brain Research Bulletin 57, 443-445.

    Google Scholar 

  • JEPSON, T. L., ERNST, M. E. & KELLY. M. W. (1999) Current perspectives on the management of seasonal affective disorder. Journal of American Pharmacology Association 39, 822-829.

    Google Scholar 

  • JONES, S. H. (2001) Circadian rhythms, multilevel models of emotion and bipolar disorder—an initial step towards integration? Clinical Psychology Reviews 21, 1193-1209.

    Google Scholar 

  • KALSBEEK, A., TECLEMARIAM-MESBAH, R. & PÉVET, P. (1993) Efferent projections of the suprachiasmatic nucleus in the golden hamster (Mesocricetus auratus). Journal of Comparative Neurology 332, 293-314.

    Google Scholar 

  • KAWANO, J., KROUT, K. E. & LOEWY, A. D. (2001) Suprachiasmatic nucleus projections to the paraventricular thalamic nucleus of the rat. Thalamus and Related Systems 1, 197-202.

    Google Scholar 

  • KROUT, K. E., KAWANO, J., METTENLEITER, T. C. & LOEWY, A. D. (2002) CNS inputs to the suprachiasmatic nucleus of the rat. Neuroscience 110, 73-92.

    Google Scholar 

  • KULLER, R. (2002) The influence of light on circadian rhythms in humans. Journal of Physiology, Anthropology and Applied Human Sciences 21, 87-91.

    Google Scholar 

  • LEAK, R. K. & MOORE, R. Y. (2001) Topographic organization of suprachiasmatic nucleus projection neurons. Journal of Comparative Neurology 433, 312-334.

    Google Scholar 

  • LIU, C., WEAVER, D. R., JIN, X., SHEARMAN, L. P., PIESCHL, R. L., GRIBKOFF, V. K. & REPPERT, M. (1997) Molecular dissection of two distinct actions of melatonin on the suprachiasmatic circadian clock. Neuron 19, 91-102.

    Google Scholar 

  • MOGA, M. M. & MOORE, R. Y. (1997) Organization of neural inputs to the suprachiasmatic nucleus in the rat. Journal of Comparative Neurology 389, 508-534.

    Google Scholar 

  • MOGA, M. M., WEIS, R. P. & MOORE, R. Y. (1995) Efferent projections of the paraventricular thalamic nucleus in the rat. Journal of Comparative Neurology 359, 221-238.

    Google Scholar 

  • MOORE, R. Y. (1996) Entrainment pathways and the functional organization of the circadian system. Progress in Brain Research 111, 103-118.

    Google Scholar 

  • NOVAK, C. M. & NUNEZ, A. A. (1998) Daily rhythms in Fos activity in the rat ventrolateral preoptic area and midline thalamic nuclei. American Journal of Physiology 275, R1620-1626.

    Google Scholar 

  • NOVAK, C. M., HARRIS, J. A., SMALE, L. & NUNEZ, A. A. (2000) Suprachiasmatic nucleus projections to the paraventricular thalamic nucleus in nocturnal rats (Rattus norvegicus) and diurnal Nile grass rats (Arviacanthis niloticus). Brain Research 874, 147-157.

    Google Scholar 

  • PAPPAS, G. D., COHEN, E. B. & PURPURA D. P. (1966) Fine structure of synaptic and nonsynaptic neuronal relations in the thalamus of the cat. In The Thalamus (edited by PURPURA, D. P. & YAHR, M. D.) pp. 47-75. New York: Columbia University Press.

    Google Scholar 

  • PAXINOS, G. & WATSON, C. (1986) The Rat Brain in Stereotaxic Coordinates. Sydney: Academic Press.

    Google Scholar 

  • PENG, Z. C., GRASSI-ZUCCONI, G. & BENTIVOGLIO, M. (1995) Fos-related protein expression in the midline paraventricular nucleus of the rat thalamus: Basal oscillation and relationship with limbic efferents. Experimental Brain Research 104, 21-29.

    Google Scholar 

  • PINTO, A., JANKOWSKI, M. & SESACK, S. R. (2003) Projections from the paraventricular nucleus of the thalamus to the rat prefrontal cortex and nucleus accumbens shell: Ultrastructural characteristics and spatial relationships with dopamine afferents. Journal of Comparative Neurology 459, 142-155.

    Google Scholar 

  • POMPEIANO, M., CIRELLI, C. & TONONI, G. (1994) Immediate-early genes in spontaneous wakefulness and sleep: Expression of c-fos and NGFI-A mRNA and protein. Journal of Sleep Research 3, 80-96.

    Google Scholar 

  • PURVIS, C. C. & DUNCAN, M. J. (1997) Discrete thalamic lesions attenuate winter adaptations and increase body weight. American Journal of Physiology 273, R226-235.

    Google Scholar 

  • SAEB-PARSY, K., LOMBARDELLI, S., KHAN, F. Z., MCDOWALL, K., AU-YONG, I. T. & DYBALL, R. E. (2000) Neural connections of hypothalamic neuroendocrine nuclei in the rat. Journal of Neuroendocrinology 12, 635-648.

    Google Scholar 

  • SEWARDS, T. V. & SEWARDS, M. A. (2003) Representations of motivational drives in mesial cortex, medial thalamus, hypothalamus and midbrain. Brain Research Bulletin 61, 25-49.

    Google Scholar 

  • SILVER, R., LESAUTER, J., TRESCO, P. A. & LEHMAN, M. N. (1996) A diffusible coupling signal from the transplanted suprachiasmatic nucleus controlling circadian locomotor rhythms. Nature 382, 810-813.

    Google Scholar 

  • STERIADE, M., JONES, E. G. & MCCORMICK, D. A. (1997) Thalamus Vol. 1. Amsterdam: Elsevier.

    Google Scholar 

  • SU, H. S. & BENTIVOGLIO, M. (1990) Thalamic midline cell populations projecting to the nucleus accumbens, amygdala, and hippocampus in the rat. Journal of Comparative Neurology 297, 582-593.

    Google Scholar 

  • SUN, X., WHITEFIELD, S., RUSAK, B. & SEMBA, K. (2001) Electrophysiological analysis of suprachiasmatic nucleus projections to the ventrolateral preoptic area in the rat. European Journal of Neuroscience 14, 1257-1274.

    Google Scholar 

  • SWANSON, L. W. (1992) Brain Maps. Amsterdam: Elsevier.

    Google Scholar 

  • TURNER, B. H. & HERKENHAM, M. (1991) Thalamoamygdaloid projections in the rat: A test of the amygdala's role in sensory processing. Journal of Comparative Neurology 313, 295-325.

    Google Scholar 

  • WATTS, A. G. & SWANSON, L. W. (1987) Efferent projections of the suprachiasmatic nucleus: II. Studies using retrograde transport of fluorescent dyes and simultaneous peptide immunohistochemistry in the rat. Journal of Comparative Neurology 258, 230-252.

    Google Scholar 

  • WATTS, A. G., SWANSON, L. W. & SANCHEZ-WATTS, G. (1987) Efferent projections of the suprachiasmatic nucleus: I. Studies using anterograde transport of Phaseolus vulgaris leucoagglutinin in the rat. Journal of Comparative Neurology 258, 204-229.

    Google Scholar 

  • WEAVER, D. R., RIVKEES, S. A. & REPPERT, S. M. (1989) Localization and characterization of melatonin receptors in rodent brain by in vitro autoradiography. Journal of Neuroscience 9, 2581-2590.

    Google Scholar 

  • WOUTERLOOD, F. G. & JORRITSMA-BYHAM, B. (1993) The anterograde neuroanatomical tracer biotinylated dextran-amine: Comparison with the tracer Phaseolus vulgaris-leucoagglutinin in preparations for electron microscopy. Journal of Neuroscience Methods 48, 75-87.

    Google Scholar 

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Correspondence to Marina Bentivoglio.

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Peng, ZC., Bentivoglio, M. The thalamic paraventricular nucleus relays information from the suprachiasmatic nucleus to the amygdala: A combined anterograde and retrograde tracing study in the rat at the light and electron microscopic levels. J Neurocytol 33, 101–116 (2004). https://doi.org/10.1023/B:NEUR.0000029651.51195.f9

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  • DOI: https://doi.org/10.1023/B:NEUR.0000029651.51195.f9

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