Coordinated regulation of feeding and social preferences by oxytocin in the rat and human

• Applicant: Professor Valery Grinevich, Ph.D.
• Subject Area: Cognitive, Systems and Behavioural Neurobiology
• Term: from 2020 to 2023
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 447311929

• Final Report Year: 2024

Final Report Abstract

This project resulted in a successful cooperation between the three partner labs. Despite the tremendously difficult situation in Israel during the last year, Prof. Dr. Shlomo Wagner and Prof. Dr. Kobi Rosenblum were able to obtain very novel and challenging results. The most important findings indicate that oxytocin acting at the insula (as well as in the prefrontal cortex) is critical to balance motivation towards social communication in the condition of choice between food and a conspecific. This process is likely mediated via the local population of oxytocinsensitive interneurons, namely axo-axonic or Chandelier cells, which “biasedly” modulate activity of principle neurons projecting to subcortical areas. However, this potential mechanism requires further investigation. Therefore, Wagner and Grinevich teams are currently running an experiment to answer the question whether projecting neurons, which are “biasedly” controlled by local interneurons, may reduce levels of anxiety and increase social motivation via their specific projections to the amygdala and nucleus accumbens, respectively.

Publications

• Astrocytes mediate the effect of oxytocin in the central amygdala on neuronal activity and affective states in rodents. Nature Neuroscience, 24(4), 529-541.
  Wahis, Jérôme; Baudon, Angel; Althammer, Ferdinand; Kerspern, Damien; Goyon, Stéphanie; Hagiwara, Daisuke; Lefevre, Arthur; Barteczko, Lara; Boury-Jamot, Benjamin; Bellanger, Benjamin; Abatis, Marios; Da Silva, Gouveia Miriam; Benusiglio, Diego; Eliava, Marina; Rozov, Andrei; Weinsanto, Ivan; Knobloch-Bollmann, Hanna Sophie; Kirchner, Matthew K.; Roy, Ranjan K. ... & Charlet, Alexandre
  
• A thalamo-preoptic pathway promotes social grooming in rodents. Current Biology, 32(21), 4593-4606.e8.
  Keller, Dávid; Láng, Tamás; Cservenák, Melinda; Puska, Gina; Barna, János; Csillag, Veronika; Farkas, Imre; Zelena, Dóra; Dóra, Fanni; Küppers, Stephanie; Barteczko, Lara; Usdin, Ted B.; Palkovits, Miklós; Hasan, Mazahir T.; Grinevich, Valery & Dobolyi, Arpád
  
• Altered PVN‐to‐CA2 hippocampal oxytocin pathway and reduced number of oxytocin‐receptor expressing astrocytes in heart failure rats. Journal of Neuroendocrinology, 34(7).
  Althammer, Ferdinand; Roy, Ranjan K.; Lefevre, Arthur; Najjar, Rami S.; Schoenig, Kai; Bartsch, Dusan; Eliava, Marina; Feresin, Rafaela G.; Hammock, Elizabeth A. D.; Murphy, Anne Z.; Charlet, Alexandre; Grinevich, Valery & Stern, Javier E.
  
• Calcium imaging and BAPTA loading of amygdala astrocytes in mouse brain slices. STAR Protocols, 3(1), 101159.
  Baudon, Angel; Clauss-Creusot, Etienne; Darbon, Pascal; Patwell, Ryan; Grinevich, Valery & Charlet, Alexandre
  
• Compartmental Neuropeptide Release Measured Using a New Oxytocin Sensor.
  Qian, Tongrui; Wang, Huan; Wang, Peng; Geng, Lan; Mei, Long; Osakada, Takuya; Tang, Yan; Kania, Alan; Grinevich, Valery; Stoop, Ron; Lin, Dayu; Luo, Minmin & Li, Yulong
  
• Identification and three-dimensional reconstruction of oxytocin receptor expressing astrocytes in the rat and mouse brain. STAR Protocols, 3(1), 101160.
  Althammer, Ferdinand; Krause, Eric G.; de Kloet, Anette D.; Smith, Justin; Grinevich, Valery; Charlet, Alexandre & Stern, Javier E.
  
• Oxytocin normalizes altered circuit connectivity for social rescue of the Cntnap2 knockout mouse. Neuron, 110(5), 795-808.e6.
  Choe, Katrina Y.; Bethlehem, Richard A.I.; Safrin, Martin; Dong, Hongmei; Salman, Elena; Li, Ying; Grinevich, Valery; Golshani, Peyman; DeNardo, Laura A.; Peñagarikano, Olga; Harris, Neil G. & Geschwind, Daniel H.
  
• Peer‐induced cocaine seeking in rats: Comparison to nonsocial stimuli and role of paraventricular hypothalamic oxytocin neurons. Addiction Biology, 27(5).
  Hammerslag, Lindsey R.; Humburg, Bree A.; Malone, Samantha G.; Beckmann, Joshua S.; Saatman, Kathryn E.; Grinevich, Valery & Bardo, Michael T.
  
• Transcription factor Creb3l1 maintains proteostasis in neuroendocrine cells. Molecular Metabolism, 63, 101542.
  Greenwood, Mingkwan; Gillard, Benjamin T.; Farrukh, Rizwan; Paterson, Alex; Althammer, Ferdinand; Grinevich, Valery; Murphy, David & Greenwood, Michael P.
  
• Viral vectors for opto-electrode recording and photometry-based imaging of oxytocin neurons in anesthetized and socially interacting rats. STAR Protocols, 3(1), 101032.
  Tang, Yan; Benusiglio, Diego; Lefevre, Arthur; Küppers, Stephanie; Lapies, Olga; Kerspern, Damien; Charlet, Alexandre & Grinevich, Valery
  
• An analgesic pathway from parvocellular oxytocin neurons to the periaqueductal gray in rats. Nature Communications, 14(1).
  Iwasaki, Mai; Lefevre, Arthur; Althammer, Ferdinand; Clauss, Creusot Etienne; Łąpieś, Olga; Petitjean, Hugues; Hilfiger, Louis; Kerspern, Damien; Melchior, Meggane; Küppers, Stephanie; Krabichler, Quirin; Patwell, Ryan; Kania, Alan; Gruber, Tim; Kirchner, Matthew K.; Wimmer, Moritz; Fröhlich, Henning; Dötsch, Laura; Schimmer, Jonas ... & Charlet, Alexandre
  
• High-calorie diets uncouple hypothalamic oxytocin neurons from a gut-to-brain satiation pathway via κ-opioid signaling. Cell Reports, 42(10), 113305.
  Gruber, Tim; Lechner, Franziska; Murat, Cahuê; Contreras, Raian E.; Sanchez-Quant, Eva; Miok, Viktorian; Makris, Konstantinos; Le Thuc, Ophélia; González-García, Ismael; García-Clave, Elena; Althammer, Ferdinand; Krabichler, Quirin; DeCamp, Lisa M.; Jones, Russell G.; Lutter, Dominik; Williams, Rhiannan H.; Pfluger, Paul T.; Müller, Timo D.; Woods, Stephen C. ... & García-Cáceres, Cristina
  
• Oxytocin activity in the paraventricular and supramammillary nuclei of the hypothalamus is essential for social recognition memory in rats. Molecular Psychiatry, 29(2), 412-424.
  Thirtamara, Rajamani Keerthi; Barbier, Marie; Lefevre, Arthur; Niblo, Kristi; Cordero, Nicholas; Netser, Shai; Grinevich, Valery; Wagner, Shlomo & Harony-Nicolas, Hala
  
• Oxytocin promotes prefrontal population activity via the PVN-PFC pathway to regulate pain. Neuron, 111(11), 1795-1811.e7.
  Liu, Yaling; Li, Anna; Bair-Marshall, Chloe; Xu, Helen; Jee, Hyun Jung; Zhu, Elaine; Sun, Mengqi; Zhang, Qiaosheng; Lefevre, Arthur; Chen, Zhe Sage; Grinevich, Valery; Froemke, Robert C. & Wang, Jing
  
• Simultaneous recording of ultrasonic vocalizations and sniffing from socially interacting individual rats using a miniature microphone. Cell Reports Methods, 3(11), 100638.
  John, Shanah Rachel; Tiwari, Rishika; Goussha, Yizhaq; Amar, Rotem; Bizer, Alex; Netser, Shai & Wagner, Shlomo
  
• A Better PIL to Swallow: A Thalamic Node in the Social Brain Network. Biological Psychiatry, 95(2), 97-99.
  Wagner, Shlomo & Maroun, Mouna
  
• Synchronized LFP rhythmicity in the social brain reflects the context of social encounters. Communications Biology, 7(1).
  Mohapatra, Alok Nath; Peles, David; Netser, Shai & Wagner, Shlomo