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Maternally involved galanin neurons in the preoptic area of the rat

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Abstract

Recent selective stimulation and ablation of galanin neurons in the preoptic area of the hypothalamus established their critical role in control of maternal behaviors. Here, we identified a group of galanin neurons in the anterior commissural nucleus (ACN), and a distinct group in the medial preoptic area (MPA). Galanin neurons in ACN but not the MPA co-expressed oxytocin. We used immunodetection of phosphorylated STAT5 (pSTAT5), involved in prolactin receptor signal transduction, to evaluate the effects of suckling-induced prolactin release and found that 76 % of galanin cells in ACN, but only 12 % in MPA were prolactin responsive. Nerve terminals containing tuberoinfundibular peptide 39 (TIP39), a neuropeptide that mediates effects of suckling on maternal motivation, were abundant around galanin neurons in both preoptic regions. In the ACN and MPA, 89 and 82 % of galanin neurons received close somatic appositions, with an average of 2.9 and 2.6 per cell, respectively. We observed perisomatic innervation of galanin neurons using correlated light and electron microscopy. The connection was excitatory based on the glutamate content of TIP39 terminals demonstrated by post-embedding immunogold electron microscopy. Injection of the anterograde tracer biotinylated dextran amine into the TIP39-expressing posterior intralaminar complex of the thalamus (PIL) demonstrated that preoptic TIP39 fibers originate in the PIL, which is activated by suckling. Thus, galanin neurons in the preoptic area of mother rats are innervated by an excitatory neuronal pathway that conveys suckling-related information. In turn, they can be topographically and neurochemically divided into two distinct cell groups, of which only one is affected by prolactin.

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Acknowledgments

Grant support was provided by HAS Postdoctoral Research Fellowship Program for MCs, OTKA K100319, OTKA K116538 and KTIA_NAP_B_13-2-2014-0004 Program for AD, and NIMH IRP for TBU. The technical assistance of Nikolett Hanák and Szilvia Deák is also acknowledged. The authors also thank Cintia K Finszter for technical contribution to pSTAT5 immunohistochemistry.

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    Authors and Affiliations

    1. MTA-ELTE NAP B Laboratory of Molecular and Systems Neurobiology, Department of Physiology and Neurobiology, Hungarian Academy of Sciences and Eötvös Loránd University, Budapest, Hungary

      Melinda Cservenák, Viktor Kis, Dávid Keller, Diána Dimén, Szilvia Oláh, Éva R. Szabó & Arpád Dobolyi

    2. Laboratory of Neuromorphology, Department of Anatomy, Histology and Embryology, Semmelweis University, 1094, Budapest, Hungary

      Melinda Cservenák, Dávid Keller, Éva R. Szabó, János Barna & Arpád Dobolyi

    3. Department of Anatomy, Cell and Developmental Biology, Institute of Biology, Eötvös Loránd University, Budapest, Hungary

      Viktor Kis, Diána Dimén & Lilla Menyhárt

    4. Human Brain Tissue Bank, Semmelweis University, Budapest, Hungary

      Éva Renner

    5. MTA-SE NAP Human Brain Tissue Bank Microdissection Laboratory, Semmelweis University, Budapest, Hungary

      Éva Renner

    6. Section on Fundamental Neuroscience, National Institute of Mental Health, Bethesda, USA

      Ted B. Usdin

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    Correspondence to Arpád Dobolyi.

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    M. Cservenák and V. Kis contributed to the work equally.

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    429_2016_1246_MOESM1_ESM.tif

    Supplementary fig. 1. Oxytocin neurons in sagittal plane. A: Schematic drawing of the rat brain 0.4 mm lateral from the bregma (Paxinos and Watson 1997). The framed area corresponds to B. The positions of the anterior commissural nucleus (ACN) and the paraventricular nucleus (PVN) are shown. B: An oxytocin immunolabeled sagittal section demonstrated the presence of oxytocin-ir neurons in both the ACN and the PVN. The distance between the two nuclei can also be appreciated. Additional abbreviations: cc – corpus callosum, Cx – cerebral cortex, f – fornix, OB – olfactory bulb, och – optic chiasm, TH – thalamus. Scale bar = 500 μm (TIFF 6080 kb)

    429_2016_1246_MOESM2_ESM.tif

    Supplementary fig. 2. Glutamate and GABA immunoreactivities in boutons establishing symmetric and asymmetric synapses in the preoptic area. A: A representative electron micrograph of a section double labeled for GABA and glutamate with gold particles of 10 and 18 nm, respectively. The boutons establishing synapses on the same dendrite are marked by dashed lines. The bouton on the left (b1) establishes a symmetric synapse pointed to by an empty arrow and contains a very high density of 10 nm gold particles indicative of the presence of GABA. In contrast, the number of 18 nm gold particles is very low in this terminal. In turn, the terminal on the right (b2) establishes an asymmetric synapse on the dendrite and contains a high density of 18 nm gold particles indicative of the presence of glutamate, while the number of 10 nm gold particles is very low. B: The scatterplot shows the GABA gold particle density as a function of glutamate gold particle density in all the terminals examined. Symmetric (green) and asymmetric (orange) synapses form clearly separate clusters. C: The glutamate/GABA gold particle density ratio is shown in a box plot for terminals establishing asymmetric and symmetric synapses. To construct the box plot, the same data set was used as for the scatter plot diagram. The glutamate/GABA ratio is highly significantly different between the two groups of terminals (***: p < 0.001) (TIFF 8979 kb)

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    Cservenák, M., Kis, V., Keller, D. et al. Maternally involved galanin neurons in the preoptic area of the rat. Brain Struct Funct 222, 781–798 (2017). https://doi.org/10.1007/s00429-016-1246-5

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