Current Biology
Volume 23, Issue 16, 19 August 2013, Pages 1536-1540
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The Head-Direction Signal Is Critical for Navigation Requiring a Cognitive Map but Not for Learning a Spatial Habit

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Highlights

  • We recorded HD cells from rats while inverted moving from familiar or novel locations

  • Direction-specific firing was disrupted after release from both conditions

  • Rats navigated accurately from the familiar, but not from the novel release points

  • Navigation using a flexible representation of space requires a functional HD signal

Summary

Head-direction (HD) cells fire as a function of an animal’s directional heading in the horizontal plane during two-dimensional navigational tasks [1]. 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 that they 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]. Here we monitored HD cell activity in the two-entry-point version of the inverted task and when the rats were released from a novel start point. We found that despite the absence of direction-specific firing in HD cells when inverted, rats could successfully navigate to the escape hole when released from one of two familiar locations by using a habit-associated directional strategy. In the continued absence of normal HD cell activity, inverted rats failed to find the escape hole when started from a novel release point. The results suggest that the HD signal is critical for accurate navigation in situations that require a flexible allocentric cognitive mapping strategy, but not for situations that utilize habit-like associative spatial learning.

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