Spatial Navigation is Guided by an Internally Organized Sense of Direction

Post by Shireen Parimoo

What's the science?

Spatial navigation is a complex process that requires both an egocentric and an allocentric awareness of the environment. An egocentric perspective refers to our knowledge of the environment in relation to our body position, whereas an allocentric perspective is our awareness of the relations between different parts of the environment (e.g. the relation between two buildings). As such, having a sense of direction is important for successful navigation. Head direction cells are a subpopulation of neurons in the medial entorhinal cortex (MEC) that are active when an animal’s head is facing a particular direction. However, it is unclear whether their direction-specific activity is consistently modulated by allocentric aspects of the environment (e.g. the location of two buildings) or if it is internally referenced (e.g. based on our previous position in space) during navigation. This week in Neuron, Park and colleagues investigated how head direction cells represent directions while rats navigated a rotating and stationary arena.

How did they do it?

Thirteen rats were implanted with recording electrodes and habituated to a large circular arena that was either stationary or rotated every 30 minutes. There were spatial cues in the arena (local, olfactory (smell) cues) and in the room that the arena was housed in (distal, visual cues). This was followed by a place avoidance training phase during which rats received a shock if they entered a “shock zone” in the arena. This shock zone remained stable when the arena was stationary and could be identified in relation to distal room cues (e.g. the part of the arena facing the clock on the wall). When the arena rotated, the shock zone dissociated into two shock zones and created two spatial frames – a “stationary” shock zone (room frame) and a “rotating” shock zone (arena frame). In the room frame, the stationary shock zone was the same area that resulted in a shock when the arena was stable (i.e. the part of the rotating arena that faced the clock in the room). In relation to the arena floor, the shock zone would rotate along with the arena. If the rat remained still in one part of the arena, it would only receive a shock when the rotation caused it to face the clock. The rotating shock zone remained fixed to the arena surface but changed in relation to distal cues, so during rotation there was both a rotating and a stationary shock zone.

Neural activity was recorded from MEC neurons during the stationary (two sessions) and rotating phases (one session) of the place avoidance task. The authors identified 115 head direction cells and examined their activity during the place avoidance paradigm to determine spike activity, directional tuning (a cell’s preferred direction), directional strength (the strength of directional tuning), and directional stability (the consistency of the cell’s preferred direction) across the stationary and rotating sessions. They also estimated whether the cells represented internally referenced head direction by examining the firing rate distribution of head direction cells in relation to the activity of one directionally tuned cell rather than the rat’s actual head direction, and they measured the strength of this internally referenced directional tuning in the rotating condition.

What did they find?

The rats successfully avoided the shock zone in both the stationary and the rotating sessions, indicating that their spatial navigation ability was not affected by the rotating arena. However, the directional tuning of their head-direction cells decreased in the rotating condition, and there were more decoding errors when the authors attempted to decode direction from cell activity in the rotating condition versus in the stationary conditions. The directional stability of the head-direction cells also decreased (i.e. became more unstable) across the two stationary sessions, and across the stationary and rotating sessions, than it did within the first stationary session. Specifically, the preferred direction of head-direction cells changed the most in the rotating arena frame condition.

In the rotating condition, directional tuning of cell ensembles was organized based on the spatial frame of the distal shock zone. This means that when rats were close to the room frame shock zone, cell activity and the preferred direction was based on the arena frame shock zone, and the opposite pattern was observed when the rats were close to the arena frame shock zone. These findings suggest that head-direction cells represent directions based on an internally-organized framework, rather than environmental landmarks. At short intervals, the strength of this internally referenced directional tuning did not differ in the room and arena spatial frames. However, after 10 seconds, directional strength decreased in the arena frame, indicating that head-direction cells represent room frame directions more consistently for longer periods of time. Finally, decoding of directions from cell ensemble activity was better in the room frame when the directions were aligned with specific room frame landmarks that did not rotate, suggesting that although these head-direction cells are largely internally referenced, they can also register to directions set by environmental cues.

What's the impact?

This study is the first to show that the head-direction cells in the rodent MEC that represent the internally referenced direction sense also register to environmental landmarks variably and transiently during navigation, instead of operating like a GPS with a stably registered compass. These findings highlight that navigating external spaces is fundamentally egocentric, but the internal direction sense also routinely registers to the allocentric landmarks of the environment for successful navigation. This has important implications for understanding the spatial representations of the environment, which seem to arise from internally-organized, dynamical neural activity that is projected onto the environment, rather than the brain passively reflecting stimuli in the environment.

Park et al. How the internally organized direction sense is used to navigate. Neuron (2018). Access the original scientific publication here.