Topographical organization of head direction signals in medial entorhinal cortex

Spatial navigation is thought to depend on functionally specialized neurons in the parahippocampus, such as head direction and grid cells. Previous work has shown a topographically organized expansion of spatial scale in grid cells along the dorsal-ventral axis of MEC (Hafting et al., 2005; Sargolini et al., 2006). Because this expansion parallels gradients in a myriad of properties of intrinsic membrane potential dynamics and synaptic integration (Giocomo et al., 2007; Garden et al., 2008), we asked if functional gradients are a broader feature of medial entorhinal topography by examining another specialized MEC cell population - head direction neurons. To examine the organization in MEC head direction neurons, we implanted rats with micro-drives running parallel to layer III or V of MEC and recorded neural activity during exploration of large open environments. Using this approach, we found a dorsal-ventral organization in the tuning breadth of MEC head direction cells that resulted from a dorsal-ventral decrease in the proportion of sharply tuned head direction cells. This organization in tuning applied to multiple populations of MEC head direction cells and existed in at least two different rodent species. Unfolded flat maps revealed that sharply tuned head direction cells were present in a dorsal band that ran along the entire medial-lateral axis investigated, suggesting that the topographical organization in head direction cells occurs predominately along the dorsal-ventral axis. Comparison with grid cell data collected from the same group of rats indicates that the dorsal to ventral head direction organization may follow a more continuous topography than the highly discrete and modular dorsal-ventral increase in grid scale (Stensola et al., 2012). Combined, our data points to a general change in scale along the dorsal-ventral axis of the MEC, expressed in multiple functional cell types and across different rodent species, suggesting that graded representations may be a fundamental coding scheme utilized by MEC circuits.