Dil tracing of the hypothalamic projection systems during perinatal development

Frontiers in Neuroanatomy

Volumn 8, Issue DEC, 2014, Pages

  Makarenko, Irina G ^a  

^a KOL TSOV INSTITUTE OF DEVELOPMENTAL BIOLOGY   (Russian Federation)

Author keywords

Dil; Hypothalamus; Intrahypothalamic; Mammillary; Mammillotegmental; Mammillothalamic; Rat; Septal

Indexed keywords

1, 1' DIOCTADECYL 3, 3, 3', 3' TETRAMETHYLINDOCARBOCYANINE; CARBOCYANINE; NEUROHORMONE; UNCLASSIFIED DRUG; VASOPRESSIN;

ANTIBODY LABELING; ARCUATE NUCLEUS; BRAIN DEVELOPMENT; FLUORESCENCE MICROSCOPY; HUMAN; HYPOPHYSIS INTERMEDIATE LOBE; HYPOTHALAMUS; HYPOTHALAMUS PERIVENTRICULAR NUCLEUS; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; MAGNOCELLULAR NUCLEUS; MAMMILLARY BODY; MAMMILLARY PENDUCLE; MAMMILLOTHALMIC TRACT; NERVE CELL NETWORK; NERVE FIBER GROWTH; NERVE PROJECTION; NEUROHYPOPHYSIS; NONHUMAN; PERINATAL DEVELOPMENT; REVIEW; SUPRACHIASMATIC NUCLEUS; SYNAPTIC POTENTIAL; THALAMUS POSTERIOR NUCLEUS;

EID: 84934313497     PISSN: None     EISSN: 16625129     Source Type: Journal    
DOI: 10.3389/fnana.2014.00144     Document Type: Review

References (83)

1. Allen, G. V., and Hopkins, D. A. (1989). Mammillary body in the rat: topography and synaptology of projections from the subicular complex, prefrontal cortex and midbrain tegmentum. J. Comp. Neurol. 286, 311-336. doi: 10.1002/cne.902860303
2. Allen, G. V., and Hopkins, D. A. (1990). Topography and synaptology of mammil- larybodyprojections to the mesencephalon andponsin the rat. J. Comp. Neurol. 301,214-231. doi: 10.1002/cne.903010206
3. Alpeeva, E. V., and Makarenko, I. G. (2007). Perinatal development of the mammillo-tegmental connections in rats. Russ. J. Dev. Biol. 38, 58-65. doi: 10.1134/s1062360407020026
4. Alpeeva, E. V., and Makarenko, I. G. (2009). Perinatal development of the mam- millothalamic tract and innervation of the anterior thalamic nuclei. Brain Res. 1248, 1-13. doi: 10.1016/j.brainres.2008.10.060
5. Altman, J., and Bayer, S. A. (1980). Development of the brain stem in the rat. IV. Thymidine-radiographic study of the time of origin of neurons in the pontine region. J. Comp. Neurol. 194, 905-929. doi: 10.1002/cne.901940411
6. Altman, J., and Bayer, S.A. (1986). The development of the rat hypothalamus. Adv. Anat. Embryol Cell Biol. 100, 1-178. doi: 10.1007/978-3-642-71301-91
7. Alvarez-Bolado, G., Zhou, X., Voss, A. K., Thomas, T., and Gruss, P. (2000).Winged helix transcription factor Foxb1 is essential for access of mammillothalamic axons to the thalamus. Development 127, 1029-1038.
8. Arai, R., Onteniente, B., Trembleau, A., Landry, M., and Calas, A. (1990). Hypotha­lamic galanin-immunoreactive neurons projecting to the posterior lobe of the rat pituitary: a combined retrograde tracing and immunocytochemical study. J. Comp. Neurol. 229,405-420. doi: 10.1002/cne.902990403
9. Bader, A., Klein, B., Breer, H., and Strotmann, J. (2012). Connectivity from OR37expressing olfactory sensory neurons to distinct cell types in the hypotha­lamus. Front. Neural Circuits 6:84. doi: 10.3389/fncir.2012.00084
10. Balthazart, J., Dupiereux, V., Aste, N., Viglietti-Panzica, C., Barrese, M., and Panz- ica, G. C. (1994). Afferent and efferent connections of the sexually dimorphic medial preoptic nucleus of the male quail revealed by in vitro transport of DiI. Cell Tissue Res. 276, 455-475. doi: 10.1007/bf00343944
11. Bayer, A., and Altman, J. (1995). “Neurogenesis and neuronal migration," in The Rat Nervous System. 2nd Edn., ed G. Paxinos (San Diego: Academic Press), 1041-1078.
12. Bouret, S. G. (2010). Neurodevelopmental actions of leptin. Brain res. 1350, 2-9. doi: 10.1016/j.brainres.2010.04.011
13. Bouret, S. G., Draper, S. J., and Simerly, R. B. (2004). Formation of projection pathways from the arcuate nucleus of the hypothalamus to hypothalamic regions implicated in the neural control of feeding behavior in mice. J. Neurosci. 24, 2797-2805. doi: 10.1523/jneurosci.5369-03.2004
14. Buchanan, K. L., and Yellon, S. M. (1993). Developmental study of GnRH neuronal projections to the medial basal hypothalamus of the male Djungarian hamster. J. Comp. Neurol. 333, 236-245. doi: 10.1002/cne.903330209
15. Buijs, R. M. (1992). “The development of vasopressin and oxytocin systems in the brain," in Handbook of Chemical Neuroanatomy Vol 10: Ontogeny of Transmitters and Peptide in the CNS, eds A. Björklund and N. Hökfelt (Amsterdam: Elsevier), 547-569.
16. Caqueret, A., Yang, C., Duplan, S., Boucher, F., and Michaud, J. L. (2005). Looking for trouble: a search for developmental defects of the hypothalamus. Horm. Res. 64, 222-230. doi: 10.1159/000088977
17. Castejon, O. J., Fuller, L., and Dailey, M. E. (2004). Localization of synapsin-I and PSD-95 in developing postnatal rat cerebellar cortex. Brain Res. Dev. Brain Res. 151, 25-32. doi: 10.1016/j.devbrainres.2004.03.019
18. Coggeshall, R. E. (1964). A study of diencephalic development in the Albino rat. J. Comp. Neurol. 122,241-270. doi: 10.1002/cne.901220208
19. Cruce, J. A. (1977). An autoradiographic study of the descending connections of the mammillary nuclei of the rat. J. Comp. Neurol. 176, 631-644. doi: 10.1002/cne.901760411
20. Daikoku, S., Kawano, H., Okamura, Y., Tokuzen, M., and Nagatsu, I. (1986). Ontogenesis of immunoreactive tyrosine hydroxylase-containing neurons in rat hypothalamus. Brain Res. 393, 85-98. doi: 10.1016/0165-3806(86)90068-4
21. Easter, S. S. Jr., Ross, L. S., and Frankfurter, A. (1993). Initial tract formation in the mouse brain. J. Neurosci. 13, 285-299.
22. Falke, N. (1991). Modulation of oxytocin and vasopressin release at the level of the neurohypophysis. Prog. Neurobiol. 36, 465-484. doi: 10.1016/0301-0082(91)90013-q
23. Gary, K. A., and Chronwall, B. M. (1992). The onset of dopaminergic inner­vation during ontogeny decreases melanotrope proliferation in the IL of the rat pituitary. Int. J. Dev. Neurosci. 10, 131-142. doi: 10.1016/0736-5748(92)90041-w
24. Godement, P., Vanselow, J., Thanos, S., and Bonhoeffer, F. (1987). A study in developing visual systems with a new method of staining neurons and their processes in fixed tissue. Development 101, 697-713.
25. Gonzalo-Ruiz, A., Morte, L., and Sanz, J. M. (1998). Glutamate/aspartate and leu- enkephalin immunoreactivity in mammillothalamic projection neurons of the rat. Brain Res. Bull. 47, 565-574. doi: 10.1016/s0361-9230(98)00077-x
26. Gonzalo-Ruiz, A., Romero, J. C., Sanz, J. M., and Morte, L. (1999). Localization of amino acids, neuropeptides and cholinergic neurotransmitter markers in identified projections from the mesencephalic tegmentum to the mammillary nuclei of the rat. J. Chem. Neuroanat. 16, 117-133. doi: 10.1016/s0891-0618(98)00063-5
27. Goudreau, J. L., Lindley, S. E., Lookingland, K. J., and Moore, K. E. (1992). Evidence that hypothalamic periventricular dopamine neurons innervate the IL of the rat pituitary. Neuroendocrinology 56, 100-105. doi: 10.1159/000126214
28. Grayson, B. E., Allen, S. E., Billes, S. K., Williams, S. M., Smith, M. S., and Grove, K. L. (2006). Prenatal development of hypothalamic neuropeptide systems in the nonhuman primate. Neuroscience 143, 975-986. doi: 10.1016/j.neuroscience.2006.08.055
29. Grinevich, V. V., and Polenov, A. L. (1994). Evolution of nonapeptidergic neurose­cretory hypothalamic formations in vertebrates. Zh. Evol. Biokhim. Fiziol. 30, 270-292.
30. Grove, K. L., Grayson, B. E., Glavas, M. M., Xiao, X. Q., and Smith, M. S. (2005). Development of metabolic systems. Physiol. Behav. 86, 646-660. doi: 10.1016/j.physbeh.2005.08.063
31. Guison, N. G., Ahmed, A. K., Dong, K., Yamadori, T., and Kobe, D. (1995). Projections from the lateral mammillary nucleus to the anterodorsal thalamic nucleus in the rat. Kobe J. Med. Sci. 41, 213-220. doi: 10.1016/0891-0618(95)00078-x
32. Hatton, G. I. (1990). Emerging concepts of structure-function dynamics in adult brain: the hypothalamo-neurohypophysial system. Prog. Neurobiol. 34, 437-504. doi: 10.1016/0301-0082(90)90017-b
33. Hayakawa, T., and Zyo, K. (1989). Retrograde double-labeling study of the mam- millothalamic and the mammillotegmental projections in the rat. J. Comp. Neurol. 284, 1-11. doi: 10.1002/cne.902840102
34. Hayakawa, T., and Zyo, K. (1990). Ultrastructure of the mammillotegmental projections to the ventral tegmental nucleus of Gudden in the rat. J. Comp. Neurol. 298, 466-475. doi: 10.1002/cne.902930309
35. Hayakawa, T., andZyo, K. (1991). Quantitative and ultrastructural studyofascend- ing projections to the medial mammillary nucleus in the rat. Anat. Embryol. (Berl) 184, 611-622. doi: 10.1007/bf00942583
36. Herman, J. P., Tasker, J. G., Ziegler, D. R., and Cullinan, W. E. (2002). Local circuit regulation of paraventricular nucleus stress integration: glutamate-GABA connections. Pharmacol. Biochem. Behav. 71, 457-468. doi: 10.1016/s0091-3057(01)00681-5
37. Hoffman, G. E., Phelps, C. J., Khachaturian, H., and Sladek, J. R. (1986). Neuroen­docrine projections to the median eminence. Curr. Top. Neuroendocrinol. 7, 161­317. doi: 10.1007/978-3-642-71461-05
38. Honig, M. G., and Hume, R. I. (1986). Fluorescent carbocyanine dyes allow living neurons of identified origin to be studied in long-term cultures. J. Cell Biol. 103, 171-187. doi: 10.1083/jcb.103.1.171
39. Honig, M. G., and Hume, R. I. (1989). DiI and DiO: versatile fluorescent dyes for neuronal labeling and pathway tracing. Trends Neurosci. 12, 333-341. doi: 10.1016/0166-2236(89)90040-4
40. Hutton, L. A., Gu, G., and Simerly, R. B. (1998). Development ofasexually dimor­phic projection from the bed nuclei of the stria terminalis to the anteroventral periventricular nucleus in the rat. J. Neurosci. 18, 3003-3013.
41. Ishikawa, K., Katakami, H., Jansson, J., and Frohman, L. A. (1986). Ontogenesis of growth hormone-releasing hormone neurons in the rat hypothalamus. Neu­roendocrinology 43, 537-542. doi: 10.1159/000124579
42. Jaeger, C. B. (1986). Aromatic l-amino acid decarboxylase in the rat brain: immunocytochemical localization during prenatal development. Neuroscience 8, 121-150. doi: 10.1016/0306-4522(86)90183-1
43. Ju, G., Liu, S., and Tao, J. (1986). Projections from the hypothalamus and its adjacent areas to the posterior pituitary in the rat. Neuroscience 19, 803-828. doi: 10.1016/0306-4522(86)90300-3
44. Kawano, H., and Daikoku, S. (1987). Functional topography of the rat hypothalamic dopamine neuron systems: retrograde tracing and immuno- histochemical study. J. Comp. Neurol. 265, 242-253. doi: 10.1002/cne.902650208
45. Keshavan, M. S., and Murray, R. M. (1997). Neurodevelopmentand AdultPsychopa- tology. Cambridge: Cambridge University Press.
46. Kocsis, B., Di Prisco, G. V., and Vertes, R. P. (2001). Theta synchronization in the limbic system: the role of Gudden’s tegmental nuclei. Eur. J. Neurosci. 13, 381-388. doi: 10.1111/j.1460-9568.2001.01392.x
47. Kouki, T., andYamanouchi, K. (2007). Postnatal development of septal projections to the midbrain central gray in female rats: tract-tracing analysis with DiI. Neurosci. Lett. 411, 37-41. doi: 10.1016/j.neulet.2006.09.085
48. Laurent, F. M., Hindelang, C., Klein, M. J., Stoeckel, M. E., and Felix, J. M. (1989). Expression of the oxytocin and vasopressin genes in the rat hypothalamus during development: an in situ hybridization study. Brain Res. Dev. Brain Res. 46, 145-154. doi: 10.1016/0165-3806(89)90152-1
49. Lukas, J. R., Aigner, M., Denk, M., Heinzl, H., Burian, M., and Mayr, R. (1998). Carbocyanine postmortem neuronal tracing: influence of different parameters on tracing distance and combination with immunocytochemistry. J. Histochem. Cytochem. 46, 901-910. doi: 10.1177/002215549804600805
50. Magoul, R., Ciofi, P., and Tramu, G. (1994). Visualization of an efferent pro­jection route of the hypothalamic rat arcuate nucleus through the stria ter- minalis after labeling with carbocyanine dye (DiI) or proopiomelanocortin- immunohistochemistry. Neurosci. Lett. 172, 134-138. doi: 10.1016/0304-3940(94)90680-7
51. Makarenko, I. G. (2007). Prenatal carbocyanine dye tracing of septo- hypothalamic connections. Brain Res. 1130, 38-47. doi: 10.1016/j.brainres.2006.10.080
52. Makarenko, I. G. (2008). “DiI tracing isauseful toolfor studies ofthehypothalamic connections during perinatal development," in Neural Pathways Research, ed L. Pichler (New-York: Nova Science Publishers), 31-71.
53. Makarenko, I. G. (2011). “Innervation of anterior thalamic nuclei by mammil- lothalamic tract during perinatal development: carbocyanine dye tracing study," in Thalamus: Anatomy, Functions and Disorders. Series: Neuroscience Research Progress, ed J. L. Song (New-York: Nova Science Publishers), 33-64.
54. Makarenko, I. G., Ugrumov, M. V., and Calas, A. (2001). Axonal projections from the hypothalamus to the median eminence in rats during ontogenesis: DiI trac­ing study. J. Anat. Embryol. (Berl) 204, 239-252. doi: 10.1007/s004290100181
55. Makarenko, I. G., Ugrumov, M. V., and Calas, A. (2005). Axonal projections from the hypothalamus to the IL of the pituitary in rats during ontogenesis: DiI tracing study. Brain Res. Dev. Brain Res. 155, 117-126. doi: 10.1016/j.devbrainres.2004.12.007
56. Makarenko, I. G., Ugrumov, M. V., Derer, P., and Calas, A. (2000). Pro­jections from the hypothalamus to the posterior lobe in rats during ontogenesis: 1,1’-Dioctadecyl-3,3,3’,3’-Tetramethylindocarbocyanine perchlo­rate tracing study. J. Comp. Neurol. 422, 327-337. doi: 10.1002/1096-9861(20000703)422:3<327::aid-cne1>3.0.co;2-9
57. Makarenko, I. G., Ugrumov, M. V., and Kalas, A. (2002). Involvement of accessory neurosecretory nuclei of hypothalamus in the formation of hypothalamohy- pophyseal system during prenatal and postnatal development in rats. Russ. J. Dev. Biol. 33, 37-42. doi: 10.1023/A:1013873012416
58. Mark, L. P., Daniels, D. L., Naidich, T. P., and Hendrix, L. E. (1995). Limbic connections. AJNR Am. J. Neuroradiol. 16, 1303-1306.
59. Mastick, G. S., and Easter, S.S. (1996). Initial organization of neurons and tracts in the embryonic mouse fore- and midbrain. Dev. Biol. 173, 79-94. doi: 10.1006/dbio.1996.0008
60. Melloni, R. H. Jr., and DeGennaro, L. J. (1994). Temporal onset of synapsin I gene expression coincides with neuronal differentiation during the development of the nervous system. J. Comp. Neurol. 342, 449-462. doi: 10.1002/cne.903420311
61. Molnar, Z., Blakey, D., Bystron, I., and Carney, R. S. E. (2006). “Tract-tracing in developing systems and in postmortem human material using carbocya- nine dyes," in Neuroanatomical Tract-tracing 3 Molecules, Neurons and Systems, eds L. Zaborszky, F. G. Wouterlood and J. L. Lanciego (USA: Springer Sci- ence+Business Media, Inc.), 366-393.
62. Morgane, P. J., Galler, J. R., and Mokler, D. J. (2005). A review of systems and networks ofthe limbic forebrain/limbic midbrain,. Prog. Neurobiol. 75, 143-160. doi: 10.1016/j.pneurobio.2005.01.001
63. Müller, C., and Torrealba, F. (1998). Postnatal development of neuron number and connections in the suprachiasmatic nucleus of the hamster. Brain Res. Dev. Brain Res. 110,203-213. doi: 10.1016/s0165-3806(98)00108-4
64. Okamura, Y., Kawano, H., and Daikoku, S. (1991). Spatial-temporal appearance of developing immunoreactive TRH neurons in the neuroepithelial wall of the diencephalon. Brain Res. Dev. Brain Res. 63, 21-31. doi: 10.1016/0921-8696(91)90845-e
65. Polston, E. K., and Simerly, R. B. (2006). Ontogeny of the projections from the anteroventral periventricular nucleus of the hypothalamus in the female rat. J. Comp. Neurol. 495, 122-132. doi: 10.1002/cne.20874
66. Risold, P. Y., and Swanson, L. W. (1997). Connections of the rat lateral septal complex. Brain Res. Brain Res. Rev. 24, 115-195. doi: 10.1016/s0165-0173(97)00009-x
67. Seki, M., and Zyo, K. (1984). Anterior thalamic afferents from the mammillary body and the limbic cortex in the rat. J. Comp. Neurol. 229, 242-256. doi: 10.1002/cne.902290209
68. Sheehan, T. P., Chambers, R. A., and Russell, D. S. (2004). Regulation of affect by the lateral septum: implications for neuropsychiatry. Brain Res. Brain Res. Rev. 46, 71-117. doi: 10.1016/j.brainresrev.2004.04.009
69. Silverman, R. C., Gibson, M. J., and Silverman, A. J. (1992). Application of a fluorescent dye to study connectivity between third ventricular preoptic area grafts and host hypothalamus. J. Neurosci Res. 31, 156-165. doi: 10.1002/jnr.490310121
70. Simerly, R. B. (2004). “Anatomical substrates of hypothalamic integration," in The Rat Nervous System, ed G. Paxinos (Amsterdam: Science Publishers Academic Press), 335-368.
71. Sofroniew, M. V., Schrell, U., Glasmann, W., Weindl, A., and Wetzstein, R. (1980). Hypothalamic accessory magnocellular vasopressin, oxytocin and neurophysin neurons projecting to the neurohypophysis in the rat. Soc. Neurosci. Abstr. 6, 456.
72. Sparks, D. L., Lue, L.-F., Martin, T. A., and Rogers, J. (2000). Neural tract tracing using Di-I: a review and a new method to make fast Di-I faster in human brain. J. Neurosci. Methods 103, 3-10. doi: 10.1016/s0165-0270(00)00291-0
73. Swanson, L. W. (1986). “Organization of mammalian neuroendocrine system," in Handbook of Physiology: The Nervous System (Vol. IV), ed F. E. Bloom (Baltimore: WaverlyPress), 317-363.
74. Swanson, L. W. (2000). Cerebral hemisphere regulation of motivated behavior. Brain Res. 886, 113-164. doi: 10.1016/s0006-8993(00)02905-x
75. Szabo, N. E., Zhao, T., Çankaya, M., Stoykova, A., Zhou, X., and Alvarez-Bolado, (2011). Interaction between axons and specific populations of surrounding cells is indispensable for collateral formation in the mammillary system. PLoS One 6:e20315. doi: 10.1371/journal.pone.0020315
76. Ugrumov, M. V. (1991). Developing hypothalamus in differentiation of neurose­cretory neurons and in establishment of pathways for neurohormone transport. Int. Rev. Cytol. 129, 207-267. doi: 10.1016/s0074-7696(08)60512-4
77. Ugrumov, M. V. (1992). Development of the median eminence during ontogenesis (morpho-functional aspects). Prog. Brain Res. 91, 349-356. doi: 10.1016/s0079-6123(08)62353-5
78. Ugrumov, M. V., Taxi, J., Tixier-Vidal, A., Thibault, J., and Mitskevich, M. S. (1989). Ontogenesis of tyrosine hydroxylase-immunopositive structures in the rat hypothalamus. An atlas of neuronal cell bodies. Neuroscience 29, 135-156. doi: 10.1016/0306-4522(89)90338-2
79. Vanhatalo, S., Soinila, S., Kaartinen, K., and Back, N. (1995). Colocalization of dopamine and serotonin in the rat pituitary gland in the nuclei innervating it. Brain Res. 669, 275-284. doi: 10.1016/0006-8993(94)01276-n
80. Vercelli, A., Repici, M., Garbossa, D., and Grimald, A. (2000). Recent techniques for tracing pathways in the central nervous system of developing and adult mammals. Brain Res. Bull. 51, 11-28. doi: 10.1016/s0361-9230(99)00229-4
81. Watanabe, K., and Kawana, E. (1980). A horseradish peroxidase study on the mammillothalamic tract in the rat. Acta Anat. (Basel) 108, 394-401. doi: 10.1159/000145322
82. Whitnall, M. H., Key, S., Ben-Barak, Y., Ozato, K., and Gainer, H. (1985). Neuro- physin in the hypothalamo-neurohypophysial system. II. Immunocytochemical studies of the ontogeny of oxytocinergic and vasopressinergic neurons. J. Neu- rosci. 5, 98-109.
83. Zimmerman, E. A., Nilaver, G., Hou-Yu, A., and Silverman, A. J. (1984). Vaso- pressinergic and oxytocinergic pathways in the central nervous system. Fed. Proc. 43, 91-96.