On the origin of our sense of space: the emergence of networks for spatial cognition before active navigation
Matteo Guardamagna
Moser Groupe, Kavli Institute for Systems Neuroscience
Trondheim, Norway

Abstract
Is our sense of space something we learn, or something that we are born with? My research studies the ontogeny of the brain’s spatial navigation networks in the medial entorhinal cortex (MEC). The MEC is a central hub of the mammalian navigation system, containing spatially and directionally tuned neurons, including grid cells and head-direction cells, which encode an animal’s position and orientation. These cells form internal maps with periodic topologies: head-direction cells traverse ring-like manifolds, while grid cells are organized on toroidal manifolds. However, very little is known about the rules that characterize the emergence of these neural networks: are these low-dimensional manifolds derived from experience, or are they genetically preconfigured? Using Neuropixels 2.0, we recorded up to ~1,000 simultaneous MEC units in sleeping rat pups from postnatal day 8 (P8). We discovered that toroidal manifolds emerge as early as P10, preceding eye and ear opening, quadrupedal gait and active exploration. These toroidal manifolds were modular from the beginning, with multiple tori simultaneously identified along the dorsoventral axis of the MEC. Their abrupt emergence coincided with increased inhibitory drive, enabling the entorhinal cortex to disengage from external sensory inputs. Similarly, we detected clusters with HD ring-like topology as early as P9 in the parasubiculum (PaS), a major input region to the MEC. The movement dynamics of tori and rings were coordinated as soon as they were recorded simultaneously (P10). From P15, as pups began exploring open-field arenas, grid fields gradually emerged in cells belonging to toroidal ensembles, reflecting a slow, experience-dependent mapping of the torus onto physical space. This suggests that networks for spatial coding have strong experience-independent components, with self-organizing principles forming low-dimensional manifolds later mapped onto the world with experience.

Invited by Rosa Cossart
Monday 19 October at 11.00 am – Inmed conference room