Directional learning, but no spatial mapping by rats performing a navigational task in an inverted orientation

Abstract

Previous studies have identified neurons throughout the rat limbic system that fire as a function of the animal's head direction (HD). This HD signal is particularly robust when rats locomote in the horizontal and vertical planes, but is severely attenuated when locomoting upside-down (Calton & Taube, 2005). Given the hypothesis that the HD signal represents an animal's sense of its directional heading, we evaluated whether rats could accurately navigate in an inverted (upside-down) orientation. The task required the animals to find an escape hole while locomoting inverted on a circular platform suspended from the ceiling. In experiment 1, Long-Evans rats were trained to navigate to the escape hole by locomoting from either one or four start points. Interestingly, no animals from the 4-start point group reached criterion, even after 30 days of training. Animals in the 1-start point group reached criterion after about 6 training sessions. In Experiment 2, probe tests revealed that animals navigating from either 1-or 2-start points utilized distal visual landmarks for accurate orientation. However, subsequent probe tests revealed that their performance was markedly attenuated when required to navigate to the escape hole from a novel starting point. This absence of flexibility while navigating upside-down was confirmed in experiment 3 where we show that the rats do not learn to reach a place, but instead learn separate trajectories to the target hole(s). Based on these results we argue that inverted navigation primarily involves a simple directional strategy based on visual landmarks.

The Head-Direction Signal Is Critical for Navigation Requiring a Cognitive Map but Not for Learning a Spatial Habit

“…When the inverted animals were released from a familiar test location they needed to use landmarks within the room to establish a directional bearing to the correct escape hole. They also had to discriminate their visual views between the two start locations in order to head in the correct direction (see [4] for details). During the Center condition trials, the inverted rats were placed in an unfamiliar location (the maze center) and had to use their representation of landmarks in the environment to compute their directional orientation and an accurate route to the escape hole.…”

“…Recent research has shown that the HD signal is disrupted when the animal is positioned in an inverted plane either under 1-g or 0-g conditions [5, 6]. In addition, a recent study demonstrated that inverted rats were unable to learn to navigate to an escape hole unless they were released from one of two familiar locations [4]. When released from novel locations, they were unable to reach the escape hole, despite the presence of familiar visual landmarks within the environment and the fact that the escape hole was < 1 m from the release point.…”

“…The information from HD cells is used with place and grid cells to form a spatial representation (cognitive map) of the environment [2,3]. Previous studies have shown that when rats are inverted (upside-down), they have difficulty learning a task that requires them to find an escape hole from one of four entry points, but can learn it when released from one or two start points [4]. Previous reports also indicate that the HD signal is disrupted when a rat is oriented upside-down [5,6].…”

Hippocampal contribution to vector model hypothesis during cue-dependent navigation

“…A navigating animal is thought to have two sources of information with which it can locate itself within an environment: egocentric and allocentric (Pearce et al 1998;Aggleton et al 2000;Begega et al 2001;Valerio et al 2010). In egocentrically based navigation, animals can use view-dependent information, whereby any available external information (e.g., cues or landmarks) is represented in relation to the animal itself (Brown 1992;Maurer and Derivaz 2000).…”

The neural correlates of navigation beyond the hippocampus

“…In one study (Valerio et al, 2010), rats performed a spatial task while inverted. In this task, a circular board was hung from the ceiling with four identical escape holes spaced equally apart.…”