Oxytocin-driven territorial mapping in the mammalian hippocampal formation

Orienting in space recruits brain mechanisms well conserved across mammalian species. Within the entorhinal-hippocampal network, a core system of spatially-selective cells supports spatial geometry computations. Yet, when navigating familiar surroundings, neural computations of space usually escape our attention. Instead, we parse space into socially meaningful territories. Territorial boundaries are social in nature since they capture the location of utilities available to individuals tied to group hierarchy and affiliation. How does our brain integrate geometry and territory? We propose that this process is regulated by the oxytocin (OT) system, acting on the entorhinal-hippocampal regions. OT, a hypothalamic neuropeptide known for its pro-social effects in mammals, modulates neural activity in the hippocampal formation, but its potential role in territorial representations has not yet been studied. Here, experts in complementary fields – social behaviors, spatial navigation, neurophysiology, anatomy, and cell signaling – will study brain similarities and differences of socio-territorial strategies in five mammalian species: bats, mice, rats, marmosets, and macaques. Our central goal is to investigate how neurons coding for space (e.g. place cells, boundary cells, grid cells) respond to perceived socio-spatial parameters of ownership, utility, and social hierarchies. We expect spatial cells to be sensitive to territorial manipulations (ownership, proximity, intrusion), regulated by OT in a context-dependent manner. OT inhibition may enhance territorial defense when territories are challenged (e.g., conspecific approaches or transgresses borders) and may sharpen territorial boundary representations. Conversely, OT stimulation could blur the boundaries of territorial perception. Our cross-species perspective will be the first to provide information on possible species-specific vs. shared neural mechanisms for territorial maps and OT-induced hippocampal plasticity.