Place recognition and heading retrieval are mediated by dissociable cognitive systems in mice

Abstract

A lost navigator must identify its current location and recover its facing direction to restore its bearings. We tested the idea that these two tasks-place recognition and heading retrieval-might be mediated by distinct cognitive systems in mice. Previous work has shown that numerous species, including young children and rodents, use the geometric shape of local space to regain their sense of direction after disorientation, often ignoring nongeometric cues even when they are informative. Notably, these experiments have almost always been performed in single-chamber environments in which there is no ambiguity about place identity. We examined the navigational behavior of mice in a two-chamber paradigm in which animals had to both recognize the chamber in which they were located (place recognition) and recover their facing direction within that chamber (heading retrieval). In two experiments, we found that mice used nongeometric features for place recognition, but simultaneously failed to use these same features for heading retrieval, instead relying exclusively on spatial geometry. These results suggest the existence of separate systems for place recognition and heading retrieval in mice that are differentially sensitive to geometric and nongeometric cues. We speculate that a similar cognitive architecture may underlie human navigational behavior.navigation | scene perception | spatial representation | geometry processing | neural specialization A navigator who becomes lost must solve two tasks to regain her bearings. First, she must identify her current location, a process we term place recognition. Second, she must identify her current facing direction, a process we term heading retrieval. These two tasks are logically dissociable from each other: A "you are here" map identifies location without revealing heading, whereas a compass reveals heading without identifying location. Neurophysiological work on rodents suggests that the outputs of these two processes are represented by distinct neural populations: Location is coded in the hippocampus, in both general terms (different environments elicit different hippocampal maps) and specific terms (place cells fire at specific coordinates within an environment), whereas heading is encoded by head direction (HD) cells in several structures including the postsubiculum, thalamus, and retrosplenial cortex (1-3). However, little is known about the systems that determine these quantities from perceptual inputs. In particular, it is not known whether place recognition and heading retrieval are mediated by the same or different processing streams.Here, we use a novel behavioral paradigm to test the hypothesis that the mechanisms that mediate place recognition at the coarse level (i.e., identification of the current environment) in mice are dissociable from the mechanisms that mediate heading retrieval. We use a variant of a spatial reorientation task that has been used extensively to study navigation behavior in a variety of species, including rodents and human children (4-7...

Do not get lost in translation: The role of egocentric heading in spatial orientation

“…This evidence suggest that, coherently with its interconnectivity with the hippocampus, the RCS may selectively engaged in translating the stored allocentric reference frame to an egocentric one thanks to a re-establishment of an "ego-oriented bearing" [18], resulting from the continuous synchronization between the inter-object direction in the environment in respect to egocentric current heading. A recent study carried out by Julian and colleagues gave support to our findings [33]. They examined the navigational behavior of mice in two tasks, in which animals had to recognize the chamber in which they were located (i.e., place recognition) and to retrieve their facing direction within that chamber (i.e., heading retrieval).…”

Environmental Geometry Aligns the Hippocampal Map during Spatial Reorientation

“…A visual cue that had been previously shown to be discriminable to both oriented and disoriented mice was present along one wall [6]. To disorient the mouse prior to the start of each trial, the mouse was removed from the chamber and placed in a small, lidded cylinder, which was subjected to four full clockwise and counterclockwise rotations.…”

“…Notably, nongeometric cues that could potentially distinguish the geometrically equivalent corners, such as a marking along one wall, are often ignored. This pattern of results—observed across numerous species including birds [5], rodents [4,6], and humans [7]—indicates that reorientation behavior is strongly informed by the spatial geometry of the environment.…”

Schematic representations of local environmental space guide goal-directed navigation

“…For example, recent work in our lab demonstrated a behavioral dissociation between local coordinate and global identity representations when rodent navigators were required to reorient themselves to their surroundings before locating a goal (Julian, Keinath, Muzzio, & Epstein, 2015). Previous studies had established that after disorientation, rodents (Cheng, 1986), humans (Hermer & Spelke, 1994; Learmonth, Newcombe, & Huttenlocher, 2001; Lee & Spelke, 2011), and many other species (Lee, Ferrari, Vallortigara, & Sovrano, 2015; Vallortigara, 2009) exhibit “geometric errors” in their search patterns.…”

“…Notably, this search pattern is often unaffected by non-geometric cues such as colors or patterns on a wall that could potentially disambiguate these two geometrically equivalent corners. We demonstrated that mice will, however, use these non-geometric cues to determine which chamber they are in—even while simultaneously ignoring them as a guide to locations within the chamber (Julian et al, 2015). That is, the mice used visual features to establish their coarse location within the wider world (e.g.…”