A thalamo-hypothalamic pathway that activates oxytocin neurons in social contexts in female rats

Melinda Cservenak, David Keller, Viktor Kis, Emese A. Fazekas, Hanna Ollos, Andras H. Leko, Eva R. Szabo, Eva Renner, Ted B. Usdin, M. Palkóvits, Arpad Dobolyi

Research output: Contribution to journalArticle

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Abstract

Oxytocin is released from neurons in the paraventricular hypothalamic nucleus (PVN) in mothers upon suckling and during adult social interactions. However, neuronal pathways that activate oxytocin neurons in social contexts are not yet established. Neurons in the posterior intralaminar complex of the thalamus (PIL), which contain tuberoinfundibular peptide 39 (TIP39) and are activated by pup exposure in lactating mothers, provide a candidate projection. Innervation of oxytocin neurons by TIP39 neurons was examined by double labeling in combination with electron microscopy and retrograde tract-tracing. Potential classic neurotransmitters in TIP39 neurons were investigated by in situ hybridization histochemistry. Neurons activated after encounter with a familiar conspecific female in a familiar environment were mapped with the c-Fos technique. PVN and the supraoptic nucleus oxytocin neurons were closely apposed by an average of 2.0 and 0.4 TIP39 terminals, respectively. Asymmetric (presumed excitatory) synapses were found between TIP39 terminals and cell bodies of oxytocin neurons. In lactating rats, PIL TIP39 neurons were retrogradely labeled from the PVN. TIP39 neurons expressed vesicular glutamate transporter 2 but not glutamic acid decarboxylase 67. PIL contained a markedly increased number of c-Fos-positive neurons in response to social encounter with a familiar conspecific female. Furthermore, the PIL received ascending input from the spinal cord and the inferior colliculus. Thus, TIP39 neurons in the PIL may receive sensory input in response to social interactions and project to the PVN to innervate and excite oxytocin neurons, suggesting that the PIL-PVN projection contributes to the activation of oxytocin neurons in social contexts.

Original languageEnglish
Pages (from-to)335-348
Number of pages14
JournalEndocrinology
Volume158
Issue number2
DOIs
Publication statusPublished - Feb 1 2017

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Oxytocin
Neurons
Paraventricular Hypothalamic Nucleus
Interpersonal Relations
Vesicular Glutamate Transport Protein 2
Mothers
Inferior Colliculi
Supraoptic Nucleus
Glutamate Decarboxylase
tuberoinfundibular peptide 39
Thalamus
Synapses
In Situ Hybridization
Neurotransmitter Agents
Spinal Cord
Electron Microscopy

ASJC Scopus subject areas

  • Endocrinology

Cite this

Cservenak, M., Keller, D., Kis, V., Fazekas, E. A., Ollos, H., Leko, A. H., ... Dobolyi, A. (2017). A thalamo-hypothalamic pathway that activates oxytocin neurons in social contexts in female rats. Endocrinology, 158(2), 335-348. https://doi.org/10.1210/en.2016-1645

A thalamo-hypothalamic pathway that activates oxytocin neurons in social contexts in female rats. / Cservenak, Melinda; Keller, David; Kis, Viktor; Fazekas, Emese A.; Ollos, Hanna; Leko, Andras H.; Szabo, Eva R.; Renner, Eva; Usdin, Ted B.; Palkóvits, M.; Dobolyi, Arpad.

In: Endocrinology, Vol. 158, No. 2, 01.02.2017, p. 335-348.

Research output: Contribution to journalArticle

Cservenak, M, Keller, D, Kis, V, Fazekas, EA, Ollos, H, Leko, AH, Szabo, ER, Renner, E, Usdin, TB, Palkóvits, M & Dobolyi, A 2017, 'A thalamo-hypothalamic pathway that activates oxytocin neurons in social contexts in female rats', Endocrinology, vol. 158, no. 2, pp. 335-348. https://doi.org/10.1210/en.2016-1645
Cservenak M, Keller D, Kis V, Fazekas EA, Ollos H, Leko AH et al. A thalamo-hypothalamic pathway that activates oxytocin neurons in social contexts in female rats. Endocrinology. 2017 Feb 1;158(2):335-348. https://doi.org/10.1210/en.2016-1645
Cservenak, Melinda ; Keller, David ; Kis, Viktor ; Fazekas, Emese A. ; Ollos, Hanna ; Leko, Andras H. ; Szabo, Eva R. ; Renner, Eva ; Usdin, Ted B. ; Palkóvits, M. ; Dobolyi, Arpad. / A thalamo-hypothalamic pathway that activates oxytocin neurons in social contexts in female rats. In: Endocrinology. 2017 ; Vol. 158, No. 2. pp. 335-348.
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abstract = "Oxytocin is released from neurons in the paraventricular hypothalamic nucleus (PVN) in mothers upon suckling and during adult social interactions. However, neuronal pathways that activate oxytocin neurons in social contexts are not yet established. Neurons in the posterior intralaminar complex of the thalamus (PIL), which contain tuberoinfundibular peptide 39 (TIP39) and are activated by pup exposure in lactating mothers, provide a candidate projection. Innervation of oxytocin neurons by TIP39 neurons was examined by double labeling in combination with electron microscopy and retrograde tract-tracing. Potential classic neurotransmitters in TIP39 neurons were investigated by in situ hybridization histochemistry. Neurons activated after encounter with a familiar conspecific female in a familiar environment were mapped with the c-Fos technique. PVN and the supraoptic nucleus oxytocin neurons were closely apposed by an average of 2.0 and 0.4 TIP39 terminals, respectively. Asymmetric (presumed excitatory) synapses were found between TIP39 terminals and cell bodies of oxytocin neurons. In lactating rats, PIL TIP39 neurons were retrogradely labeled from the PVN. TIP39 neurons expressed vesicular glutamate transporter 2 but not glutamic acid decarboxylase 67. PIL contained a markedly increased number of c-Fos-positive neurons in response to social encounter with a familiar conspecific female. Furthermore, the PIL received ascending input from the spinal cord and the inferior colliculus. Thus, TIP39 neurons in the PIL may receive sensory input in response to social interactions and project to the PVN to innervate and excite oxytocin neurons, suggesting that the PIL-PVN projection contributes to the activation of oxytocin neurons in social contexts.",
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