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A direct neuronal connection between the subparafascicular and ventrolateral arcuate nuclei in non-lactating female rats. Could this pathway play a role in the suckling-induced prolactin release?

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Abstract

The neuronal pathways, through which prolactin secretion is regulated during lactation, have still not been fully explored. Studies indicate that the suckling stimulus travels through the spinal cord, the brain stem, and then reaches the hypothalamus. The focus of this present experiment is to further explore the neuronal connections between the brain stem and the arcuate nucleus that may be involved in suckling-induced prolactin release. Ante- and retrograde tracing techniques were used. To chemically characterize the explored neurons neuropeptide immunohistochemistry was applied. Previous studies have indicated that the peripeduncular nucleus is a relay of the suckling stimulus in the midbrain, conveying the information to the hypothalamus. In our experiments, we have found an additional cell group in the subparafascicular parvocellular nucleus located just behind the posterior thalamus that projects to the arcuate neurons. The injection of the retrograde tracer into the ventrolateral part of the arcuate nucleus labeled cells in the lateral subdivision of the subparafascicular parvocellular nucleus. Anterograde tracing from the subparafascicular parvocellular nucleus resulted in fiber labeling in the arcuate nucleus in close apposition with dynorphin immunopositive neurons. Double labeling revealed that a subpopulations of the subparafascicular parvocellular neurons projecting to the arcuate nucleus contained tuberoinfundibular peptide of 39 residues or calcitonin gene-related peptide. The presented findings suggest that the ascending fibers from the subparafascicular parvocellular nucleus might be in the pathway involved in the suckling-induced prolactin release.

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Abbreviations

ARC:

Arcuate nucleus

BDA:

Biotinylated dextran amine

CGRP:

Calcitonin gene-related peptide

DAB:

Diaminobenzidine tetrahydrochloride

Dyn:

Dynorphine

FG:

Fluorogold

Gal:

Galanine

KPBS:

Potassium-phosphate buffer saline

NKB:

Neurokinin-B

OT:

Oxytocin

PFA:

Paraformaldehyde

PPN:

Peripeduncular nucleus

PRL:

Prolactin

PV:

Paraventricular nucleus

SPFpc:

Subparafascicular parvocellular nucleus

TH:

Tyrosine hydroxylase

TIDA neurons:

Tuberoinfundibular dopaminergic neurons

TIP39:

Tuberoinfundibular peptide of 39 residues

VMN:

Ventromedial nucleus

References

  1. D.A. Leong, L.S. Frawley, J.D. Neill, Neuroendocrine control of prolactin secretion. Ann Rev Physiol 45, 109–127 (1983)

    Article  CAS  Google Scholar 

  2. K. Fuxe, T. Hökfelt, On the existence of dopaminergic and noradrenergic mechanisms in the control of hormone releasing and inhibitory factor secretion from the median eminence. J. Anat. 111, 475–476 (1972)

    CAS  PubMed  Google Scholar 

  3. D.M. Gibbs, High concentrations of oxytocin in hypophysial portal plasma. Endocrinology 114, 1216–1218 (1984)

    Article  CAS  PubMed  Google Scholar 

  4. W.K. Samson, M.D. Lumpkin, S.M. McCann, Evidence for a physiological role for oxytocin in the control of prolactin secretion. Endocrinology 119, 554–560 (1986)

    Article  CAS  PubMed  Google Scholar 

  5. M. Dubois-Dauphin, W.E. Armstrong, E. Tribollet, J.J. Dreifuss, Somatosensory systems and the milk-ejection reflex in the rat II. The effects of lesions in the ventroposterior thalamic complex, dorsal columns and lateral cervical nucleus-dorsolateral funiculus. Neuroscience 15, 1131–1140 (1985)

    Article  CAS  PubMed  Google Scholar 

  6. S. Hansen, C. Köhler, The importance of the peripeduncular nucleus in the neuroendocrine control of sexual behavior and milk ejection in the rat. Neuroendocrinology 39, 563–572 (1984)

    Article  CAS  PubMed  Google Scholar 

  7. J.S. Tindal, G.S. Knaggs, Determination of the detailed hypothalamic route of the milk-ejection reflex in the guinea-pig. J. Endocrinol. 50, 135–152 (1971)

    Article  CAS  PubMed  Google Scholar 

  8. J.S. Tindal, G.S. Knaggs, Further studies on the afferent path of the milk-ejection reflex in the brain stem of the rabbit. J. Endocrinol. 66, 107–113 (1975)

    Article  CAS  PubMed  Google Scholar 

  9. E.M. Factor, A.D. Mayer, J.S. Rosenblatt, Peripeduncular nucleus lesions in the rat: I. Effects on maternal aggression, lactation, and maternal behavior during pre- and postpartum periods. Behav. Neurosci. 107, 166–185 (1993)

    Article  CAS  PubMed  Google Scholar 

  10. J.S. Tindal, G.S. Knaggs, An ascending pathway for release of prolactin in the brain of the rabbit. J. Endocrinol. 45, 111–120 (1969)

    Article  CAS  PubMed  Google Scholar 

  11. J.S. Tindal, G.S. Knaggs, A. Turvey, The afferent path of the milk-ejection reflex in the brain of the rabbit. J. Endocrinol. 43, 663–671 (1969)

    Article  CAS  PubMed  Google Scholar 

  12. C. Li, P. Chen, M.S. Smith, Identification of neuronal input to the arcuate nucleus (ARH) activated during lactation: implications in the activation of neuropeptide Y neurons. Brain Res. 824, 267–276 (1999)

    Article  CAS  PubMed  Google Scholar 

  13. A. Dobolyi, M. Palkovits, T. Usdin, Expression and distribution of tuberoinfundibular peptide of 39 residues in the rat central nervous system. J. Comp. Neurol. 455, 547–566 (2003)

    Article  CAS  PubMed  Google Scholar 

  14. L.M. Coolen, J.G. Veening, D.W. Peterson, M.T. Shipley, Parvocellular subparafascicular thalamic nucleus in the rat: anatomical and functional compartmentalization. J. Comp. Neurol. 463, 117–131 (2003)

    Article  PubMed  Google Scholar 

  15. G. Paxinos, C. Watson, The rat brain in stereotaxic coordinates (Academic Press, San Diego, 1986)

    Google Scholar 

  16. I. Bodnár, Z. Bánky, B. Tóth, G. Nagy, B. Halász, Brain structures mediating the suckling stimulus-induced release of prolactin. J. Neuroendocrinol. 14, 384–396 (2002)

    Article  PubMed  Google Scholar 

  17. O. Youngren, Y. Chaiseha, K. Al-Zailaie, S. Whiting, S.W. Kang, M. El Halawani, Regulation of prolactin secretion by dopamine at the level of the hypothalamus in the turkey. Neuroendocrinology 75, 185–192 (2002)

    Article  CAS  PubMed  Google Scholar 

  18. C. Li, P. Chen, M.S. Smith, Neural populations in the rat forebrain and brainstem activated by the suckling stimulus as demonstrated by cFos expression. Neuroscience 94, 117–129 (1999)

    Article  CAS  PubMed  Google Scholar 

  19. C.E. Grosvenor, F. Mena, N.S. Whitworth, Sensory stimuli from pups involved in inhibition of milk secretion in rats during late lactation. Horm. Behav. 8, 287–296 (1977)

    Article  CAS  PubMed  Google Scholar 

  20. Y.F. Wang, H. Negoro, K. Honda, Effects of hemitransection of the midbrain on milk-ejection burst of oxytocin neurones in lactating rat. J. Endocrinol. 144, 463–470 (1995)

    Article  CAS  PubMed  Google Scholar 

  21. Y.F. Wang, H. Negoro, K. Honda, Amplitudes and time courses of milk ejection bursts of oxytocin neurons in the midbrain-hemitransected lactating rat. Brain Res. 719, 203–206 (1996)

    Article  CAS  PubMed  Google Scholar 

  22. Y.F. Wang, H. Negoro, K. Honda, Milk ejection bursts of supraoptic oxytocin neurones during bilateral and unilateral suckling in the rat. J. Neuroendocrinol. 8, 427–431 (1996)

    Article  CAS  PubMed  Google Scholar 

  23. S.J. Grundmann, E.A. Pankey, M.M. Cook, A.L. Wood, B.L. Rollins, B.M. King, Combination unilateral amygdaloid and ventromedial hypothalamic lesions: evidence for a feeding pathway. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288, R702–R707 (2005)

    CAS  PubMed  Google Scholar 

  24. J.E. Ledoux, D.A. Ruggiero, R. Forest, R. Stornetta, D.J. Reis, Topographic organization of convergent projections to the thalamus from the inferior colliculus and spinal cord in the rat. J. Comp. Neurol. 264, 123–146 (1987)

    Article  CAS  PubMed  Google Scholar 

  25. M. Fitzsimmons, J. Olschowka, S. Wiegand, G. Hoffman, Interaction of opioid peptide-containing-terminals with dopaminergic perikarya in the rat hypothalamus. Brain Res. 581, 10–18 (1992)

    Article  CAS  PubMed  Google Scholar 

  26. L.M. Coolen, H.J. Peters, J.G. Veening, Fos immunoreactivity in the rat brain following consummatory elements of sexual behavior: a sex comparison. Brain Res. 738, 67–82 (1996)

    Article  PubMed  Google Scholar 

  27. M.S. Smith, Lactation alters neuropeptide-Y and proopiomelanocortin gene expression in the arcuate nucleus of the rat. Endocrinology 133, 1258–1265 (1993)

    Article  CAS  PubMed  Google Scholar 

  28. J.-R. Pape, G. Tramu, Suckling-induced changes in neuropeptide Y and proopiomelanocortin gene expression in the arcuate nucleus of the rat: evaluation of a putative intervention of prolactin. Neuroendocrinology 63, 540–549 (1996)

    Article  CAS  PubMed  Google Scholar 

  29. C. Li, P. Chen, M.S. Smith, The acute suckling stimulus induces expression of neuropeptide Y (NPY) in cells in the dorsomedial hypothalamus and increases NPY expression in the arcuate nucleus. Endocrinology 139, 1645–1652 (1998)

    Article  CAS  PubMed  Google Scholar 

  30. L. Pickavance, S. Dryden, D. Hopkins, C. Bing, H. Frankish, Q. Wang, R.G. Vernon, G. Williams, Relationships between hypothalamic neuropeptide Y and food intake in the lactating rat. Peptides 17, 577–582 (1996)

    Article  CAS  PubMed  Google Scholar 

  31. C. Elie, M.S. Moukhtar, G. Milhaud, M. Cressent, Hypoprolactinemic effect of calcitonin gene-related peptide in the rat. Neuropeptides 16, 109–113 (1990)

    Article  CAS  PubMed  Google Scholar 

  32. L. Debeljuk, M. Lasaga, Tachykinins and the control of prolactin secretion. Peptides 27, 3007–3019 (2006)

    Article  CAS  PubMed  Google Scholar 

  33. E. Isovich, M. del Carmen Diaz, M. Lasaga, D. Pisera, C. Zambruno, M.S. Theas, A. Seilicovich, B.H. Duvilanski, Involvement of hypothalamic substance P in the effect of prolactin on dopamine release. Neuroreport 5, 1752–1754 (1994)

    Article  CAS  PubMed  Google Scholar 

  34. M.C. Burke, P.A. Letts, S.J. Krajewski, N.E. Rance, Coexpression of dynorphin and neurokinin B immunoreactivity in the rat hypothalamus: morphologic evidence of interrelated function within the arcuate nucleus. J. Comp. Neurol. 498, 712–726 (2006)

    Article  CAS  PubMed  Google Scholar 

  35. G.E. Hoffman, M.S. Smith, M.D. Fitzsimmons, Detecting steroidal effects on immediate early gene expression in the hypothalamus. Neuroprotocols 1, 52–66 (1992)

    Article  CAS  Google Scholar 

  36. R.E. Watson Jr, S.J. Wiegand, S.J. Clough, G.E. Hoffman, Use of cryoprotectant to maintain long-term peptide immunoreactivity and tissue morphology. Peptides 7, 155–159 (1986)

    Article  CAS  PubMed  Google Scholar 

  37. T.B. Usdin, S.R. Hoare, T. Wang, E. Mezey, J.A. Kowalak, TIP39: a new neuropeptide and PTH2-receptor agonist from hypothalamus. Nat. Neurosci. 2, 941–943 (1999)

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors would like to acknowledge the technical help of Le Wei Wei.

Author information

Authors and Affiliations

  1. Department of Pediatrics, University of Kentucky, Lexington, KY, USA

    Flora K. Szabo

  2. 570 Big Stoner Rd, Winchester, KY, 40391, USA

    Flora K. Szabo

  3. Department of Anatomy and Neurobiology, University of Maryland, Baltimore, MD, USA

    Natalie Snyder

  4. National Institute of Mental Health, Bethesda, MD, USA

    Ted B. Usdin

  5. Department of Biology, Morgan State University, Baltimore, MD, USA

    Gloria E. Hoffman

Authors
  1. Flora K. Szabo
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  2. Natalie Snyder
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  3. Ted B. Usdin
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  4. Gloria E. Hoffman
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Corresponding author

Correspondence to Gloria E. Hoffman.

Additional information

This work was funded and supported by grant # NIH grant NS 43788 to GEH.

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Szabo, F.K., Snyder, N., Usdin, T.B. et al. A direct neuronal connection between the subparafascicular and ventrolateral arcuate nuclei in non-lactating female rats. Could this pathway play a role in the suckling-induced prolactin release?. Endocr 37, 62–70 (2010). https://doi.org/10.1007/s12020-009-9266-z

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  • DOI: https://doi.org/10.1007/s12020-009-9266-z

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