A thalamo-hypothalamic pathway that activates oxytocin neurons in social contexts in female rats
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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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Excitatory projections from the PIL to the PVH are involved in social interactions in females and may contribute to oxytocin release via direct inputs to oxytocin cells.
“Previous research has suggested that excitatory projections from the PIL to the PVH are involved in social interactions in females and may contribute to oxytocin release via direct inputs to oxytocin cells (3).”
From Social Interaction Elicits Activity in Glutamatergic Neurons in the Posterior Intralaminar Complex of the Thalamus (2024) · cites this paper as [3]
Tracing studies in rodents have shown that the PIL receives inputs from sensory regions such as the inferior and superior colliculus, auditory cortex, and spinal cord and projects to socially relevant brain regions including the PVH, lateral septum, MPOA, and medial amygdala.
“Tracing studies conducted in rodents have provided anatomical support for this theory, demonstrating that the PIL receives inputs from sensory regions such as the inferior and superior colliculus, auditory cortex, and spinal cord (3, 7-10) and projects to socially relevant brain regions including the paraventricular nucleus of the hypothalamus (PVH), the lateral septum, medial preoptic area (MPOA)”
From Social Interaction Elicits Activity in Glutamatergic Neurons in the Posterior Intralaminar Complex of the Thalamus (2024) · cites this paper as [3]
The PIL has been shown to be activated in rats following the reunion of conspecific females.
“The PIL has also been shown to be activated in rats following the reunion of conspecific females (3)”
From Social Interaction Elicits Activity in Glutamatergic Neurons in the Posterior Intralaminar Complex of the Thalamus (2024) · cites this paper as [3]
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 [3]
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 [3]
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 [3]
These TIP39 neurons co-express calbindin and VGlut2 and form presumed excitatory synapses with oxytocin neurons in the PVH.
“These neurons co-express calbindin and vesicular glutamate transporter 2 (VGlut2), and form presumed excitatory synapses with oxytocin neurons in the PVH (3, 12)”
From Social Interaction Elicits Activity in Glutamatergic Neurons in the Posterior Intralaminar Complex of the Thalamus (2024) · cites this paper as [3]
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Chen, J. C., Wang, X., Li, Z., Yuan, H., Wang, X., Yun, Y., Wu, X., Yang, P., & Qin, L. (2024) · Communications Biology · doi:10.1038/s42003-024-07040-5 · Cited by 5 · see citing works
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Numan, M. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190848675.003.0008 · Cited by 2 · see citing works
Hormonal Control of Maternal Behavior in Nonhuman Mammals
Numan, M. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190848675.003.0003 · Cited by 2 · see citing works
Numan, M. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190848675.003.0002 · Cited by 1 · see citing works
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Numan, M. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190848675.002.0003
Abbreviations Used for Major Brain Regions
Numan, M. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190848675.002.0007
Numan, M. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190848675.002.0004
- Authors
- Cservenák, M., Keller, D., Kis, V., Fazekas, E. A., Öllös, H., Lékó, A. H., Szabó, É. R., Renner, É., Usdin, T. B., Palkovits, M., & Dobolyi, Á.
- Affiliations
- Eötvös Loránd University (HU)
- MTA-ELTE NAP B Laboratory of Molecular and Systems Neurobiology, Department of Physiology and Neurobiology, Hungarian Academy of Sciences and Eötvös Loránd University, Budapest 1117, Hungary;
- Laboratory of Neuromorphology and
- Semmelweis University (HU)
- National Institutes of Health (US)
- ORCID
- Venue
- Endocrinology
- Publisher
- The Endocrine Society
- Published
- 2016-11-14
- Volume
- 158
- Issue
- 2
- Pages
- 335-348
- ISSN
- 0013-7227 (ISSN-L)
- 1945-7170
- PMC
- PMC5413079
- OpenAlex
- W2552286825
- Cited by
- 64
- References
- 61
- Citations by year
- 2026: 2 · 2025: 4 · 2024: 9 · 2023: 4 · 2022: 7 · 2021: 9 · 2020: 22 · 2019: 2 · 2018: 3 · 2017: 2
- FWCI
- 3.63
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Endocrinology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Hungarian Scientific Research Fund
- Magyar Tudományos Akadémia
- Emberi Eroforrások Minisztériuma
- National Institutes of Health
- National Institute of Mental Health (ZIAMH002685)
- 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
- oxytocin neurons, paraventricular nucleus, social interaction, lactation, female rats, synaptic innervation, c-fos, supraoptic nucleus, vesicular glutamate transporter 2, inferior colliculus, maternal behavior
- MeSH terms
- Animals, Animals, Newborn, Female, Hypothalamus, Maternal Behavior, Neurons, Oxytocin, Thalamus, Proto-Oncogene Proteins c-fos, Rats, Wistar
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