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

Abstract

Summary Head-direction (HD) cells fire as a function of an animal’s directional heading in the horizontal plane during 2-D 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 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 an allocentric cognitive mapping strategy, but not for situations that utilize habit-like associative spatial learning.

Lesions of the hippocampus or dorsolateral striatum disrupt distinct aspects of spatial navigation strategies based on proximal and distal information in a cued variant of the Morris water task

“…When the cue is absent, however, it appears that directional responding, to some extent, remains intact after HPC lesions. This could be due to spared HPC tissue from incomplete lesions, or that head direction (HD) cells that code for directional orientation have been found in several structures outside the HPC [27]. It is possible that this HD circuit might guide behavior in HPC rats, indeed such a result has been reported recently in mice [16].…”

The Nucleus Prepositus Hypoglossi Contributes to Head Direction Cell Stability in Rats

“…These cells were clearly not classically defined HD cells and were instead labeled "drifting cells." However, some of these cells had an overall Rayleigh R greater than the traditional HD cell cutoff (Muir et al, 2009;Yoder and Taube, 2009;Gibson et al, 2013;R Ͼ 0.40). An illustration of the similarities and differences between these cells and normal HD cells is shown in Figure 3.…”

“…The internal cues used by the HD system include both vestibular and proprioceptive information, each of which depends on unique sets of brain structures (Goodridge et al, 1998). Lesions of the vestibular system disrupt direction-specific firing throughout the HD network (Stackman and Taube, 1997;Muir et al, 2009).…”

Rat thalamic neurons encode complex combinations of heading and movement directions and the trajectory route during translocation with sensory conflict

“…Recent studies have reported that information from HD cells is processed in place and grid cells to form a spatial representation (cognitive map) of the environment (O'Keefe and Nadel, 1978; Moser and Moser, 2008), and it is critical for accurate navigation in situations that require a flexible allocentric cognitive mapping strategy (Gibson et al, 2013). It has been reported that up to 10 different brain structures contain neurons selective for HD, including the anterodorsal (AD) and laterodorsal (LD) thalamic nuclei (Taube, 2007).…”