Thalamic neuropeptide mediating the effects of nursing on lactation and maternal motivation
Open accessAbstract
Nursing has important physiological and psychological consequences on mothers during the postpartum period. Tuberoinfundibular peptide of 39 residues (TIP39) may contribute to its effects on prolactin release and maternal motivation. Since TIP39-containing fibers and the receptor for TIP39, the parathyroid hormone 2 receptor (PTH2 receptor) are abundant in the arcuate nucleus and the medial preoptic area, we antagonized TIP39 action locally to reveal its actions. Mediobasal hypothalamic injection of a virus encoding an antagonist of the PTH2 receptor markedly decreased basal serum prolactin levels and the suckling-induced prolactin release. In contrast, injecting this virus into the preoptic area had no effect on prolactin levels, but did dampen maternal motivation, judged by reduced time in a pup-associated cage during a place preference test. In support of an effect of TIP39 on maternal motivation, we observed that TIP39 containing fibers and terminals had the same distribution within the preoptic area as neurons expressing Fos in response to suckling. Furthermore, TIP39 terminals closely apposed the plasma membrane of 82% of Fos-ir neurons. Retrograde tracer injected into the arcuate nucleus and the medial preoptic area labeled TIP39 neurons in the posterior intralaminar complex of the thalamus (PIL), indicating that these cells but not other groups of TIP39 neurons project to these hypothalamic regions. We also found that TIP39 mRNA levels in the PIL markedly increased around parturition and remained elevated throughout the lactation period, demonstrating the availability of the peptide in postpartum mothers. Furthermore, suckling, but not pup exposure without physical contact, increased Fos expression by PIL TIP39 neurons. These results indicate that suckling activates TIP39 neurons in the PIL that affect prolactin release and maternal motivation via projections to the arcuate nucleus and the preoptic area, respectively.
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In maternal female rats, a subpopulation of PIL neurons expressing TIP39 is activated in response to pup exposure and suckling.
“In maternal female rats, a subpopulation of PIL neurons that expresses tuberoinfundibular peptide 39 (TIP39) were shown to be activated in response to pup exposure and suckling (2-4).”
From Social Interaction Elicits Activity in Glutamatergic Neurons in the Posterior Intralaminar Complex of the Thalamus (2024) · cites this paper as [4]
The PIL is considered a relay center by which sensory information is conveyed to other brain regions for the generation of relevant social behaviors.
“The posterior intralaminar complex of the thalamus (PIL) is considered a relay center by which sensory information is conveyed to other brain regions for the generation of relevant social behaviors (1-6).”
From Social Interaction Elicits Activity in Glutamatergic Neurons in the Posterior Intralaminar Complex of the Thalamus (2024) · cites this paper as [4]
Neuroanatomical studies in lactating rats show that TIP39+ neurons project to the MPOA and the PVH.
“Based on neuroanatomical studies in lactating rats showing that TIP39 + neurons project to the MPOA (4, 30) and the PVH (3)”
From Social Interaction Elicits Activity in Glutamatergic Neurons in the Posterior Intralaminar Complex of the Thalamus (2024) · cites this paper as [4]
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Cites
The rat brain in stereotaxic coordinates
Palkovits, M. (1983) · Neuropeptides · doi:10.1016/0143-4179(83)90049-5 · Cited by 28,959 · see citing works
Self-citationThe Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
Prolactin: structure, function, and regulation of secretion
Freeman, M. E., Kanyicska, B., Lerant, A., & Nagy, G. (2000) · Physiological Reviews · doi:10.1152/physrev.2000.80.4.1523 · Cited by 2,457 · see citing works
Self-citationMAEDA, K., OHKURA, S., & Tsukamura, H. (2000) · Elsevier eBooks · doi:10.1016/b978-012426400-7/50048-0 · Cited by 2,135 · see citing works
Germline Transmission and Tissue-Specific Expression of Transgenes Delivered by Lentiviral Vectors
Lois, C., Hong, E. J., Pease, S., Brown, E. J., & Baltimore, D. (2002) · Science · doi:10.1126/science.1067081 · Cited by 1,974 · see citing works
Knobil and Neill's Physiology of Reproduction
(2015) · Elsevier eBooks · doi:10.1016/c2011-1-07288-0 · Cited by 1,276 · see citing works
Production, concentration and titration of pseudotyped HIV-1-based lentiviral vectors
Kutner, R. H., Zhang, X., & Reiser, J. (2009) · Nature Protocols · doi:10.1038/nprot.2009.22 · Cited by 670 · see citing works
Topographic organization of neurons in the acoustic thalamus that project to the amygdala
LeDoux, J., Farb, C. R., & Ruggiero, D. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-04-01043.1990 · Cited by 546 · see citing works
The organization of neural inputs to the medial preoptic nucleus of the rat
Simerly, R. B., & Swanson, L. W. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902460304 · Cited by 523 · see citing works
The expectant brain: adapting for motherhood
Brunton, P. J., & Russell, J. A. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2280 · Cited by 407 · see citing works
Bosch, O. J., & Neumann, I. D. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.11.002 · Cited by 400 · see citing works
Central prolactin infusions stimulate maternal behavior in steroid-treated, nulliparous female rats.
Bridges, R. S., Numan, M. J., Ronsheim, P. M., MANN, P., & Lupini, C. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.20.8003 · Cited by 349 · see citing works
Hunyady, B., Krempels, K., Harta, G., et al. (1996) · Journal of Histochemistry & Cytochemistry · doi:10.1177/44.12.8985127 · Cited by 275 · see citing works
Insulin induces long-term depression of ventral tegmental area dopamine neurons via endocannabinoids
Labouèbe, G., Liu, S., Dias, C., Zou, H., Wong, J. C. Y., Karunakaran, S., Clee, S. M., Phillips, A. G., Boutrel, B., & Borgland, S. L. (2013) · Nature Neuroscience · doi:10.1038/nn.3321 · Cited by 239 · see citing works
Forebrain expression of c-fos due to active maternal behaviour in lactating rats
Lonstein, J. S., Simmons, D. A., Swann, J. M., & Stern, J. M. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00283-2 · Cited by 237 · see citing works
Central regulation of ejaculation
Coolen, L. M., Allard, J., Truitt, W. A., & McKenna, K. E. (2004) · Physiology & Behavior · doi:10.1016/j.physbeh.2004.08.023 · Cited by 236 · see citing works
Ferris, C. F., Kulkarni, P. P., Sullivan, J. M., Harder, J. A., Messenger, T. L., & Febo, M. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.3156-04.2005 · Cited by 222 · see citing works
TIP39: a new neuropeptide and PTH2-receptor agonist from hypothalamus
Usdin, T. B., Hoare, S. R. J., Wang, T., Mezey, É., & Kowalak, J. A. (1999) · Nature Neuroscience · doi:10.1038/14724 · Cited by 203 · see citing works
Self-citationRussell, J. A., Douglas, A. J., & Ingram, C. D. (2001) · Progress in brain research · doi:10.1016/s0079-6123(01)33002-9 · Cited by 187 · see citing works
Maternity: Neural mechanisms, motivational processes, and physiological adaptations.
Numan, M., & Woodside, B. C. (2010) · Behavioral Neuroscience · doi:10.1037/a0021548 · Cited by 162 · see citing works
Pereira, M., & Morrell, J. I. (2011) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02200.x · Cited by 146 · see citing works
Numan, M., Numan, M. J., Schwarz, J. M., Neuner, C. M., Flood, T. F., & Smith, C. D. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.08.008 · Cited by 139 · see citing works
Pregnancy‐Induced Adaptation in the Neuroendocrine Control of Prolactin Secretion
Grattan, D. R., Steyn, F. J., Kokay, I. C., Anderson, G. M., & Bunn, S. J. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01661.x · Cited by 132 · see citing works
Weickert, C. S., Webster, M. J., Colvin, S. M., Herman, M. M., Hyde, T. M., Weinberger, D. R., & Kleinman, J. E. (2000) · The Journal of Comparative Neurology · doi:10.1002/1096-9861(20000731)423:3 · Cited by 130 · see citing works
Schwarz, J. M., & Bilbo, S. D. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2516-12.2013 · Cited by 115 · see citing works
Prolactin and the hyperphagia of lactation
Woodside, B. C. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.04.015 · Cited by 103 · see citing works
Chapter 19 Neural mediation of nursing and related maternal behaviors
Stern, J. M., & Lonstein, J. S. (2001) · Progress in brain research · doi:10.1016/s0079-6123(01)33020-0 · Cited by 98 · see citing works
Stack, E. C., & Numan, M. (2000) · Behavioral Neuroscience · doi:10.1037//0735-7044.114.3.609 · Cited by 90 · see citing works
Cservenák, M., Bodnár, I., Usdin, T. B., Palkovits, M., Nagy, G. M., & Dobolyi, A. (2010) · Endocrinology · doi:10.1210/en.2010-0767 · Cited by 82 · see citing works
Mattson, B. J., Williams, S. E., Rosenblatt, J. S., & Morrell, J. I. (2003) · Psychopharmacology · doi:10.1007/s00213-002-1351-4 · Cited by 81 · see citing works
GABA receptor agonists in the medial preoptic area and maternal behavior in lactating rats
Gómora‐Arrati, P., CARMONA, C., DOMINGUEZ, G., Beyer, C., & ROSENBLATT, J. (2005) · Physiology & Behavior · doi:10.1016/j.physbeh.2005.08.048 · Cited by 79 · see citing works
Stack, E. C., & Numan, M. (2000) · Behavioral Neuroscience · doi:10.1037/0735-7044.114.3.609 · Cited by 79 · see citing works
Dobolyi, Á., Ueda, H., Uchida, H., Palkovits, M., & Usdin, T. B. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.042416199 · Cited by 78 · see citing works
Self-citationDobolyi, Á., Palkovits, M., & Usdin, T. B. (2009) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2009.10.017 · Cited by 68 · see citing works
Self-citationLactation and Its Hormonal Control
Anderson, S., MacLean, P., McManaman, J., & Neville, M. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-397175-3.00046-6 · Cited by 68 · see citing works
Bagó, A. G., Dimitrov, E., Saunders, R. C., Seress, L., Palkovits, M., Usdin, T. B., & Dobolyi, Á. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.04.054 · Cited by 66 · see citing works
Self-citationSeip, K. M., & Morrell, J. I. (2009) · Behavioral Neuroscience · doi:10.1037/a0017666 · Cited by 63 · see citing works
Dobolyi, Á., Palkovits, M., & Usdin, T. B. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10515 · Cited by 61 · see citing works
Self-citationLi, C., Chen, P., & Smith, M. S. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01217-2 · Cited by 55 · see citing works
Faber, C. A., Dobolyi, Á., Sleeman, M. W., & Usdin, T. B. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21330 · Cited by 46 · see citing works
Self-citationNursing stimulation is more than tactile sensation: It is a multisensory experience
Febo, M., Stolberg, T. L., Numan, M., Bridges, R. S., Kulkarni, P., & Ferris, C. F. (2008) · Hormones and Behavior · doi:10.1016/j.yhbeh.2008.02.024 · Cited by 42 · see citing works
Pathways in the forebrain of the rat concerned with the release of prolactin
TINDAL, J. S., & Knaggs, G. S. (1977) · Brain Research · doi:10.1016/0006-8993(77)90101-9 · Cited by 38 · see citing works
Olazábal, D., Kalinichev, M., Morrell, J., & Rosenblatt, J. (2002) · Hormones and Behavior · doi:10.1006/hbeh.2001.1753 · Cited by 32 · see citing works
Szabo, F. K., Snyder, N., Usdin, T. B., & Hoffman, G. E. (2010) · Endocrine · doi:10.1007/s12020-009-9266-z · Cited by 32 · see citing works
Self-citationMaternal Absence of the Parathyroid Hormone 2 Receptor Affects Postnatal Pup Development
Coutellier, L. D., Logemann, A., Rusnák, M., & Usdin, T. B. (2011) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02149.x · Cited by 30 · see citing works
Self-citationThe Distribution and Neurochemistry of the Parathyroid Hormone 2 Receptor in the Rat Hypothalamus
Dobolyi, Á., Irwin, S., Wang, J., & Usdin, T. B. (2006) · Neurochemical Research · doi:10.1007/s11064-005-9011-9 · Cited by 30 · see citing works
Self-citationNeuropathic and inflammatory pain are modulated by tuberoinfundibular peptide of 39 residues
Dimitrov, E. L., Kuo, J., Kohno, K., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1306342110 · Cited by 23 · see citing works
Development of a rat parathyroid hormone 2 receptor antagonist
Kuo, J., & Usdin, T. B. (2007) · Peptides · doi:10.1016/j.peptides.2006.12.002 · Cited by 21 · see citing works
Self-citationPostnatal development and gender‐dependent expression of TIP39 in the rat brain
Dobolyi, Á., Wang, J., Irwin, S., & Usdin, T. B. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.21063 · Cited by 20 · see citing works
Self-citationAcoustic stress activates tuberoinfundibular peptide of 39 residues neurons in the rat brain
Palkovits, M., Helfferich, F., Dobolyi, Á., & Usdin, T. B. (2009) · Brain Structure and Function · doi:10.1007/s00429-009-0233-5 · Cited by 16 · see citing works
Self-citationParalemniscal TIP39 is induced in rat dams and may participate in maternal functions
Varga, T. R., Mogyoródi, B., Bagó, A. G., Cservenák, M., Domokos, D., Renner, É., Gallatz, K., Usdin, T. B., Palkovits, M., & Dobolyi, Á. (2011) · Brain Structure and Function · doi:10.1007/s00429-011-0357-2 · Cited by 13 · see citing works
Self-citationTuberoinfundibular peptide of 39 residues in the embryonic and early postnatal rat brain
Brenner, D., Bagó, A. G., Gallatz, K., Palkovits, M., Usdin, T. B., & Dobolyi, Á. (2008) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2008.04.001 · Cited by 10 · see citing works
Self-citationBodnár, I., Bánky, Z., Nagy, G. M., & Halász, B. (2005) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2005.01.001 · Cited by 10 · see citing works
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- Authors
- Cservenák, M., Szabó, É. R., Bodnár, I., Lékó, A., Palkovits, M., Nagy, G. M., Usdin, T. B., & Dobolyi, A.
- Affiliations
- Semmelweis University (HU)
- National Institutes of Health (US)
- Venue
- Psychoneuroendocrinology
- Publisher
- Elsevier BV
- Published
- 2013-12
- Volume
- 38
- Issue
- 12
- Pages
- 3070-3084
- ISSN
- 0306-4530 (ISSN-L)
- PMC
- PMC3844093
- OpenAlex
- W2146276207
- Cited by
- 77
- References
- 53
- Citations by year
- 2026: 4 · 2025: 3 · 2024: 9 · 2023: 3 · 2022: 5 · 2021: 8 · 2020: 21 · 2019: 5 · 2018: 6 · 2017: 5 · 2016: 3 · 2015: 2 · 2014: 3
- FWCI
- 4.00
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Psychoneuroendocrinology (publishedVersion)
- PubMed (publishedVersion)
- Repository of the Academy's Library (Library of the Hungarian Academy of Sciences) (acceptedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Bolyai János Fellowship Award of the Hungarian Academy of Sciences
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Keywords
- TIP39, maternal motivation, lactation, prolactin secretion, suckling, arcuate nucleus, medial preoptic area, Fos expression, postpartum period, hypothalamic projections
- MeSH terms
- Animals, Arcuate Nucleus of Hypothalamus, Cholera Toxin, Conditioning, Operant, Female, Image Processing, Computer-Assisted, Lactation, Male, Maternal Behavior, Motivation, Nerve Fibers, Neuropeptides, Preoptic Area, Prolactin, Stereotaxic Techniques, Thalamus, Lentivirus, Polymerase Chain Reaction, Genes, fos, Rats, Wistar, In Situ Hybridization, Rats, Shab Potassium Channels
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