Skip to main content
SpringerLink
Log in

Recent findings on the organization of central nervous system structures involved in the innervation of endocrine glands and other organs; observations obtained by the transneuronal viral double-labeling technique

  • Review
  • Published:
Endocrine Aims and scope Submit manuscript

Abstract

This review summarizes the data obtained with the aid of the recently introduced dual viral tracing technique, which uses isogenic recombinants of pseudorabies virus that express unique reporter gene. This approach made possible to explore simultaneously neural circuits of two organs. The results of these studies indicate: (1) there are neurons innervating exclusively a given organ; (2) left-sided predominance in the supraspinal innervation of the endocrine glands (adrenal, ovary) studied, so far; (3) viral co-infection of neurons, i.e., special neuronal populations coexist in different brain areas that are transsynaptically connected with both paired endocrine and non-endocrine organs, endocrine glands and non-endocrine organs, and organs of bodily systems other than the endocrine one. The number of common neurons seems to be related to the need of coordinating action of different systems. The data on co-infection of neurons suggest that the central nervous system has the capacity to coordinate different organ functions via common brain neurons providing supraspinal innervation of the organs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. A. Bartha, Magyar Állatorvosok Lapja 16, 42–45 (1961)

    Google Scholar 

  2. A. Aujeszky, Veterinarius 25, 387–396 (1902)

    Google Scholar 

  3. P. Card, in Viral Vectors: Gene Therapy and Neuroscience Applications, ed. by M.G. Kaplitt, A.D. Loewy (Academic Press, New York, 1995), pp. 319–347

    Google Scholar 

  4. J.P. Card, L.W. Enquist, in Methods in Molecular Genetics, ed. by K.W. Adolph (Academic Press, New York, 1994), pp. 363–382

    Google Scholar 

  5. G. Ugolini, in Viral Vectors: Gene Therapy and Neuroscience Application, ed. by M.G. Kaplitt, A.D. Loewy (Academic Press, New York, 1995), pp. 293–317

    Google Scholar 

  6. J.P. Card, L.W. Enquist, Curr. Protocol. Neurosci. unit 1.5, 1–28 (1999)

  7. J.S. Kim, L.W. Enquist, J.P. Card, J. Virol. 73, 9521–9531 (1999)

    CAS  PubMed  Google Scholar 

  8. B.W. Banfield, J.D. Kaufman, J.A. Randall, G.E. Pickard, J. Virol. 77, 10106–10112 (2003)

    Article  CAS  PubMed  Google Scholar 

  9. I. Billig, J.M. Foris, L.W. Enquist, J.P. Card, B.J. Yates, J. Neurosci. 20, 7446–7454 (2000)

    CAS  PubMed  Google Scholar 

  10. Zs. Boldogkői, A. Reichart, I.E. Tóth, A. Sik, F. Erdélyi, I. Medveczky, C. Llorens-Cortes, M. Palkovits, Zs. Lenkei, Mol. Brain Res. 109, 105–118 (2002)

    Article  PubMed  Google Scholar 

  11. Zs. Boldogkői, A. Sik, Á. Dénes, A. Reichart, J. Toldi, I. Gerendai, K.J. Kovács, M. Palkovits, Prog. Neurobiol. 72, 417–445 (2004)

    Article  PubMed  Google Scholar 

  12. G. Cano, A.F. Sved, L. Rinaman, B.S. Rabin, J.P. Card, J. Comp. Neurol. 439, 1–18 (2001)

    Article  CAS  PubMed  Google Scholar 

  13. G. Cano, J.P. Card, A.F. Sved, J. Comp. Neurol. 471, 462–481 (2004)

    Article  PubMed  Google Scholar 

  14. A.S.P. Jansen, X.V. Nguyen, V. Karpitskiy, T.C. Mettenleiter, A.D. Loewy, Science 270, 644–646 (1995)

    Article  CAS  PubMed  Google Scholar 

  15. I. Billig, K. Hartge, J.P. Card, B.J. Yates, Brain Res. 912, 24–32 (2001)

    Article  CAS  PubMed  Google Scholar 

  16. R.M. Buijs, J. Wortel, J.J. Heerikhuize, M.G.P. Feenstra, G.J.T. Horst, H.J. Romijn, A. Kalsbeek, Eur. J. Neurosci. 11, 1535–1544 (1999)

    Article  CAS  PubMed  Google Scholar 

  17. W.K. Kesse, T.L. Parker, R.E. Coupland, J. Anat 157, 33–41 (1988)

    CAS  PubMed  Google Scholar 

  18. N. Kleitman, M.A. Holzwarth, Cell Tissue Res. 241, 139–147 (1985)

    Article  CAS  PubMed  Google Scholar 

  19. H.R. Berthoud, T.L. Powley, J. Auton. Nerv. Syst. 42, 153–170 (1993)

    Article  CAS  PubMed  Google Scholar 

  20. R.E. Coupland, T.L. Parker, W.K. Kesse, A.A. Mohamed, J. Anat. 163, 173–181 (1989)

    CAS  PubMed  Google Scholar 

  21. A.A. Mohamed, T.L. Parker, R.E. Coupland, J. Anat. 160, 51–58 (1988)

    CAS  PubMed  Google Scholar 

  22. R.M. Buijs, S.E. La Fleur, J. Wortel, C. Van Heyningen, L. Zuiddam, T.C. Mettenleiter, A. Kalsbeek, K. Nagai, A. Niijima, J. Comp. Neurol. 464, 36–48 (2003)

    Article  PubMed  Google Scholar 

  23. A.M. Strack, W.B. Sawyer, K.B. Platt, A.D. Loewy, Brain Res. 491, 274–296 (1989)

    Article  CAS  PubMed  Google Scholar 

  24. I.E. Tóth, Horm. Metab. Res. 30, 329–333 (1998)

    Article  PubMed  Google Scholar 

  25. M.F. Dallman, W.C. Engeland, J. Shinsako, Am. J. Physiol. 231, 408–414 (1976)

    CAS  PubMed  Google Scholar 

  26. M. Kaneko, T. Hiroshige, J. Shinsako, M.F. Dallman, Am. J. Physiol. 239, 309–316 (1980)

    Google Scholar 

  27. M. Kaneko, K. Kaneko, J. Shinsako, M.F. Dallman, Endocrinology 109, 70–75 (1981)

    Article  CAS  PubMed  Google Scholar 

  28. Y.M. Ulrich-Lai, M.M. Arnhold, W.C. Engeland, Am. J. Physiol. 290, 1128–1135 (2006)

    Google Scholar 

  29. Y.M. Ulrich-Lai, W.C. Engeland, Neuroendocrinology 71, 107–123 (2000)

    Article  CAS  PubMed  Google Scholar 

  30. I.E. Tóth, O. Wiesel, D.E. Tóth, Zs. Boldogkői, B. Halász, I. Gerendai, Microsc. Res. Tech. 71, 503–509 (2008)

    Article  PubMed  Google Scholar 

  31. I. Gerendai, P. Banczerowski, B. Halász, Endocrine 28, 309–318 (2005)

    Article  CAS  PubMed  Google Scholar 

  32. I. Gerendai, I.E. Tóth, Zs. Boldogkői, I. Medveczky, B. Halász, Neuroendocrinology 68, 244–256 (1998)

    Article  CAS  PubMed  Google Scholar 

  33. I.E. Tóth, O. Wiesel, Zs. Boldogkői, K. Bálint, Zs. Tapaszti, I. Gerendai, Microsc. Res. Tech. 70, 710–718 (2007)

    Article  PubMed  Google Scholar 

  34. T.K. Lee, J.H. Lois, J.H. Troupe, T.D. Wilson, B.J. Yates, Am. J. Physiol. Regul. Integr. Comp. Physiol. 292, 1532–1541 (2007)

    Google Scholar 

  35. E.M. Sullivan, A. Gratton, J. Neurosci. 19, 2834–2840 (1999)

    CAS  PubMed  Google Scholar 

  36. A.M. Neville, A.M. Mackay, Clin. Endocrinol. Metab. 1, 361–395 (1972)

    Article  Google Scholar 

  37. J.M. Martins, J. Alves, A. Trinca, B. Grima, S. do Vale, T. Vasconcelos, N. Riso, V. Riscado, J.C. da Costa, Brain Behav. Immun. 16, 383–397 (2002)

    Article  CAS  PubMed  Google Scholar 

  38. I. Gerendai, B. Halász, Front. Neuroendocrinol. 18, 354–381 (1997)

    Article  CAS  PubMed  Google Scholar 

  39. I. Gerendai, B. Halász, News Physiol. Sci. 16, 92–95 (2001)

    CAS  PubMed  Google Scholar 

  40. A.I. Barco, A. Flores, R. Chavira, P. Damian-Matzumura, R. Dominguez, M.E. Cruz, Endocrine 21, 209–215 (2003)

    Article  CAS  PubMed  Google Scholar 

  41. R. Chavez, M.E. Cruz, R. Dominguez, J. Endocrinol. 113, 397–401 (1987)

    Article  CAS  PubMed  Google Scholar 

  42. R. Chavez, R. Dominguez, J. Endocrinol. 140, 197–201 (1994)

    Article  CAS  PubMed  Google Scholar 

  43. A. Flores, J.O. Rodriguez, M.T. Palafox, G. Melendez, A.I. Barco, R. Chavira, M.E. Cruz, R. Dominguez, Reprod. Biol. Edocrinol. 1, 4–11 (2006)

    Google Scholar 

  44. R. Chavez, S. Sanchez, A. Ulloa-Aguirre, R. Dominguez, J. Endocrinol. 123, 441–444 (1989)

    Article  CAS  PubMed  Google Scholar 

  45. I. Gerendai, W. Rotsztejn, B. Marchetti, C. Kordon, U. Scapagnini, Neurosci. Lett. 9, 333–336 (1978)

    Article  CAS  PubMed  Google Scholar 

  46. P.R. Arteaga-Lopez, R. Dominguez, M.A. Cerbon, C.A. Mendoza-Rodriguez, M.E. Cruz, Endocrine 21, 251–260 (2003)

    Article  CAS  PubMed  Google Scholar 

  47. M. Fukuda, K. Yamanouchi, Y. Nakano, H. Furuya, Y. Arai, Neurosci. Lett. 51, 365–370 (1984)

    Article  CAS  PubMed  Google Scholar 

  48. M.E. Cruz, L.P. Jamarillo, R. Dominguez, J. Endocrinol. 123, 437–439 (1989)

    Article  CAS  PubMed  Google Scholar 

  49. J.P. Advis, C.E. Ahmed, S.R. Ojeda, Brain Res. Bull. 22, 605–610 (1989)

    Article  CAS  PubMed  Google Scholar 

  50. J.L. Moran, M.E. Cruz, R. Dominguez, Brain Res. Bull. 33, 663–668 (1994)

    Article  CAS  PubMed  Google Scholar 

  51. I. Gerendai, I.E. Tóth, Zs. Boldogkői, I. Medveczky, B. Halász, J. Auton. Nerv. Syst. 80, 40–45 (2000)

    Article  CAS  PubMed  Google Scholar 

  52. I.E. Tóth, P. Banczerowski, Zs. Boldogkői, J.S. Tóth, A. Szabó, B. Halász, I. Gerendai, Brain Res. Bull. 77, 306–311 (2008)

    Article  Google Scholar 

  53. B.J. Pardini, D.D. Lund, P.G. Schmid, J. Auton. Nerv. Syst. 28, 193–201 (1989)

    Article  CAS  PubMed  Google Scholar 

  54. T.J. Bartness, C.K. Song, G.E. Demas, J. Biol. Rhythms 16, 196–204 (2001)

    CAS  PubMed  Google Scholar 

  55. T. Ueyama, K.E. Krout, X.V. Nguyen, V. Karpitskiy, A. Kollert, T.C. Mettenleiter, A.D. Loewy, Nat. Neurosci. 2, 1051–1053 (1999)

    Article  CAS  PubMed  Google Scholar 

  56. M.A. Levatte, P.J. Mabon, L.C. Weaver, G.A. Dekaban, Neuroscience 82, 1253–1267 (1998)

    Article  CAS  PubMed  Google Scholar 

  57. S.C. Gandevia, K. Killian, D.K. McKenzie, M. Crawford, G.M. Allen, R.B. Gorman, J.P. Hales, J. Physiol. 470, 85–107 (1993)

    CAS  PubMed  Google Scholar 

  58. T.G. Waldrop, F.L. Eldridge, G.A. Iwamoto, J.H. Mitchell, in Handbook of Physiology, Section 12, Exercise: Regulation and Integration of Multiple Systems, ed. by L.B. Rowell, J.T. Stepherd (Oxford University Press, New York, 1996)

    Google Scholar 

  59. I.A. Kerman, L.W. Enquist, S.J. Watson, B.J. Yates, J. Neurosci. 23, 4657–4666 (2003)

    CAS  PubMed  Google Scholar 

  60. S. Kalantaridou, A. Makrigiannakis, E. Zoumakis, G. Chrousos, J. Reprod. Immunol. 62, 61–68 (2004)

    Article  CAS  PubMed  Google Scholar 

  61. M.A. Magiakou, G. Mastorakos, E. Webster, G.P. Chrousos, Ann. N. Y. Acad. Sci. 816, 42–56 (1997)

    Article  CAS  PubMed  Google Scholar 

  62. A.I. Turner, P.H. Hemsworth, B.J. Canny, A.J. Tilbrook, Biol. Reprod. 61, 614–620 (1999)

    Article  CAS  PubMed  Google Scholar 

  63. M.D. Chen, K.T. O’Byrne, S.E. Chiappini, J. Hotchkiss, E. Knobil, Neuroendocrinology 56, 666–673 (1992)

    Article  CAS  PubMed  Google Scholar 

  64. C. Baravalle, N.R. Salvetti, G.A. Mira, J.A. Lorente, H.H. Ortega, Physiol. Res. 56, 67–78 (2007)

    CAS  PubMed  Google Scholar 

  65. F. Kamel, C.L. Kubajak, Endocrinology 121, 561–568 (1987)

    Article  CAS  PubMed  Google Scholar 

  66. M. Saketos, N. Sharma, N.F. Santoro, Biol. Reprod. 49, 1270–1276 (1993)

    Article  CAS  PubMed  Google Scholar 

  67. E.A. Young, M. Altemus, Ann. N. Y. Acad. Sci. 1021, 124–133 (2004)

    Article  CAS  PubMed  Google Scholar 

  68. K.E. Krout, T.C. Mettenleiter, A.D. Loewy, Neuroscience 118, 853–866 (2003)

    Article  CAS  PubMed  Google Scholar 

  69. K.E. Krout, T.C. Mettenleiter, V. Karpitskiy, X.V. Nguyen, A.D. Loewy, Brain Res. 1050, 199–202 (2005)

    Article  CAS  PubMed  Google Scholar 

  70. G.F. Longstreth, D.B. Preskill, L. Youkeles, Dig. Dis. Sci. 35, 1285–1290 (1990)

    Article  CAS  PubMed  Google Scholar 

  71. G.F. Longstreth, Obstet. Gynecol. Surv. 49, 505–507 (1994)

    Article  CAS  PubMed  Google Scholar 

  72. P.J. Whorwell, E.W. Lupton, D. Erduran, K. Wilson, Gut 27, 1014–1017 (1986)

    Article  CAS  PubMed  Google Scholar 

  73. P.J. Whorwell, M. McCallum, F.H. Creed, C.T. Roberts, Gut 27, 37–40 (1987)

    Article  Google Scholar 

  74. M.L. Rouzade-Dominguez, R. Miselis, R.J. Valentino, Eur. J. Neurosci. 18, 3311–3324 (2003)

    Article  PubMed  Google Scholar 

  75. J.M. Kramer, E.D. Plowey, J.A. Beatty, H.R. Little, T.G. Waldrop, Brain Res. Bull. 53, 77–85 (2000)

    Article  CAS  PubMed  Google Scholar 

  76. F.L. Eldridge, D.E. Millhorn, T.G. Waldrop, Science 211, 844–846 (1981)

    Article  CAS  PubMed  Google Scholar 

  77. A.M. Motekaitis, M.P. Kaufman, Respir. Physiol. 106, 263–271 (1996)

    Article  CAS  PubMed  Google Scholar 

  78. J.B. Travers, L. Rinaman, Neuroscience 115, 1139–1151 (2002)

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported in part by grants from the National Research Fund (OTKA T046624 to I.G.), the Ministry of Health (ETT 448/2006 to I.G.), and the Hungarian Academy of Sciences. The authors are grateful to Miss Mariann Akócsi for preparation of the manuscript.

Author information

Authors and Affiliations

  1. Neuromorphological and Neuroendocrine Research Laboratory, Department of Human Morphology and Developmental Biology, Hungarian Academy of Sciences and Semmelweis University, Tűzoltó u. 58, 1094, Budapest, Hungary

    Ida Gerendai, Ida E. Tóth & Béla Halász

  2. Department of Human Morphology and Developmental Biology, Semmelweis University, Tűzoltó u. 58, 1094, Budapest, Hungary

    Ida Gerendai

  3. Department of Biology, Faculty of Medicine, University of Szeged, Somogyi Béla u. 4, 6720, Szeged, Hungary

    Zsolt Boldogkői

Authors
  1. Ida Gerendai
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ida E. Tóth
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zsolt Boldogkői
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Béla Halász
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ida Gerendai.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gerendai, I., Tóth, I.E., Boldogkői, Z. et al. Recent findings on the organization of central nervous system structures involved in the innervation of endocrine glands and other organs; observations obtained by the transneuronal viral double-labeling technique. Endocr 36, 179–188 (2009). https://doi.org/10.1007/s12020-009-9189-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12020-009-9189-8

Keywords

Search

Navigation