Coherence among Head Direction Cells before Eye Opening in Rat Pups

Mammalian navigation is thought to depend on an internal map of space consisting of functionally specialized cells in the hippocampus and the surrounding parahippocampal cortices [1–7]. Basic properties of this map are present when rat pups explore the world outside of their nest for the first time, around postnatal day 16–18 (P16–P18) [8–10]. One of the first functions to be expressed in navigating animals is the directional tuning of the head direction cells [8, 9]. To determine whether head direction tuning is expressed at even earlier ages, before the start of exploration, and to establish whether vision is necessary for the development of directional tuning, we recorded neural activity in pre- and parasubiculum, or medial entorhinal cortex, from P11 onward, 3–4 days before the eyelids unseal. Head direction cells were present from the first day of recording. Firing rates were lower than in adults, and preferred firing directions were less stable, drifting within trials and changing completely between trials. Yet the cells drifted coherently, i.e., relative firing directions were maintained from one trial to the next. Directional tuning stabilized shortly after eye opening. The data point to a hardwired attractor network for representation of head direction in which directional tuning develops before vision and visual input serves primarily to anchor firing direction to the external world. •Head direction cells are present 3–4 days before eye opening or earlier•Before eye opening, directional tuning is unstable•Head direction cells drift coherently before eye opening•Directional tuning stabilizes as soon as the eyes open Bjerknes et al. show that head direction cells are present in young rat pups several days before eye opening and initiation of active exploration. There is considerable drift in the cells’ directional preferences, but the relative differences in firing direction are maintained, consistent with a predominantly innate attractor network for directional representation.