Toroidal topology of grid-cell activity precedes spatial navigation during development

Abstract

The medial entorhinal cortex (MEC) is a central component of the mammalian navigation system1-5, in which spatially and directionally tuned neurons, including grid cells and head-direction cells, encode an animals position and orientation6-8. These cells form internal maps with periodic topologies: head-direction cells traverse ring-like manifolds9,10, while grid cells are organized on toroidal manifolds11. The persistence of these topologies across behavioral states and environments11,12 raises the possibility that they arise intrinsically from network architecture rather than through sensory experience4,5,13-17. Consistent with this view, observations in juvenile rats have shown that rudimentary spatial tuning appears in place cells, head direction cells and grid cells almost as soon as pups begin to explore their surroundings at 2-3 weeks of age18-20. However, it remains unclear whether spatial experience is required for the initial emergence of positional tuning and for the organization of tuned cells into periodic maps. Here we show, using large-scale ensemble recordings in rat pups, that toroidal manifolds emerge in MEC subnetworks as early as postnatal day 10 (P10), preceding eye and ear opening, upright posture, quadrupedal gait, and active exploration21,22. These toroidal networks were modular from the beginning, with increasing differentiation of their dynamics appearing on P11-12. The onset of toroidal topology coincided with a transition in MEC network activity characterized by desynchronization and increased inhibitory connectivity, a developmental shift observed broadly across cortical regions at this age23,24. In contrast, ring-like manifolds were already detectable by P9, with traces of directional tuning appearing in individual cells at P8 -- consistent with an earlier maturation of subcortical circuitry25. As pups subsequently began to explore the environment around P15-16, these internally generated maps progressively aligned with external landmarks, culminating in stable, periodic firing fields by three weeks of age. Taken together, these findings identify ring-like and toroidal manifolds as instinctive computational motifs of the developing brain. Their early emergence, preceding major sensory input and navigation, supports the view that spatial representations are preconfigured and later anchored to the external world through experience-dependent plasticity.