The Development of the Head Direction System before Eye Opening in the Rat

Head direction (HD) cells are neurons found in the hippocampal formation and connected areas that fire as a function of an animal’s directional orientation relative to its environment [1, 2]. They integrate self-motion and environmental sensory information to update directional heading [3]. Visual landmarks, in particular, exert strong control over the preferred direction of HD cell firing [4]. The HD signal has previously been shown to appear adult-like as early as postnatal day 16 (P16) in the rat pup, just after eye opening and coinciding with the first spontaneous exploration of its environment [5, 6]. In order to determine whether the HD circuit can begin its organization prior to the onset of patterned vision, we recorded from the anterodorsal thalamic nucleus (ADN) and its postsynaptic target in the hippocampal formation, the dorsal pre-subiculum (PrSd), before and after eye opening in pre-weanling rats. We find that HD cells can be recorded at the earliest age sampled (P12), several days before eye opening. However, this early HD signal displays low directional information content and lacks stability both within and across trials. Following eye opening, the HD system matures rapidly, as more cells exhibit directional firing, and the quality and reliability of the directional signal improves dramatically. Cue-rotation experiments show that a prominent visual landmark is able to control HD responses within 24 hr of eye opening. Together, the results suggest that the directional network can be organized independently of visual spatial information while demonstrating the importance of patterned vision for accurate and reliable orientation in space.