Coherence among head direction cells before eye opening in rat pups

Abstract

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. 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). One of the first functions to be expressed in navigating animals is the directional tuning of the head direction cells. 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.

Figure 1

Head Direction Cells Are Present before Eye Opening (A) Nissl-stained sagittal brain sections with representative recording locations in presubiculum (PrS) and parasubiculum (PaS). See also Figure S1 for recording locations in the remaining animals. (B) Polar plots showing distribution of firing rate for eight head direction cells recorded before eye opening. Rat number (five digits), postnatal day, and peak firing rate are indicated. All head directions were covered during all recording trials. The low peak rates are representative for the parahippocampal area in this age group [8–10].

Figure 2

The Effect of Eye Opening on Head Direction Tuning (A) Four representative head direction cells recorded before eye opening at P14 and four different head direction cells recorded after eye opening at P15 in the same rats. Polar plots for the distribution of firing rate are shown for each cell. Rat number (five digits) and peak firing rate are indicated. All head directions were covered during all recording trials. (B) Frequency distributions showing mean vector length of firing rate in observed data (top) and shuffled versions of the same data (bottom) before and after eye opening. The red stippled line and the red text indicate the 95^th percentile for mean vector length in the shuffled data. (C) Percentage of head direction cells passing the 95^th percentile criterion for mean vector length of firing rate. The red stippled line indicates the upper limit for a 95% confidence interval around the proportion of cells, P₀, expected to pass the 95^th percentile criterion by chance (5%). (D) Mean vector length of firing rate for cells recorded before and after eye opening (mean ± SEM for all head direction cells). The red stippled line indicates the 95^th percentile for mean vector length from the shuffled data. (E) Within-trial directional correlation before and after eye opening (mean ± SEM). (F) Between-trial directional correlation before and after eye opening (mean ± SEM). See also Figure S2.

Figure 3

Head Direction Cells Are Unstable before Eye Opening but Maintain Coherence (A) Polar plots showing distribution of firing rate for ten pairs of head direction cells from a single experiment before eye opening. One member of the pair is shown in red, the other in blue. Cell number (1–5) and peak firing rate are indicated for each cell. All head directions were covered during all recording trials. Note that cells are unstable between trials yet rotate in a coherent manner. (B) Change in mean firing direction across trials for individual cells. The analysis includes all cells that were recorded simultaneously with one or several other head direction cells on two consecutive trials before eye opening. (C) Change in relative firing direction (angular difference) across trials for all pairs of head direction cells recorded on two consecutive trials. Low values imply that relative firing directions are maintained.