The cognitive map in humans: spatial navigation and beyond

Abstract

The 'cognitive map' hypothesis proposes that brain builds a unified representation of the spatial environment to support memory and guide future action. Forty years of electrophysiological research in rodents suggest that cognitive maps are neurally instantiated by place, grid, border and head direction cells in the hippocampal formation and related structures. Here we review recent work that suggests a similar functional organization in the human brain and yields insights into how cognitive maps are used during spatial navigation. Specifically, these studies indicate that (i) the human hippocampus and entorhinal cortex support map-like spatial codes, (ii) posterior brain regions such as parahippocampal and retrosplenial cortices provide critical inputs that allow cognitive maps to be anchored to fixed environmental landmarks, and (iii) hippocampal and entorhinal spatial codes are used in conjunction with frontal lobe mechanisms to plan routes during navigation. We also discuss how these three basic elements of cognitive map based navigation-spatial coding, landmark anchoring and route planning-might be applied to nonspatial domains to provide the building blocks for many core elements of human thought.

Figures

Figure 1. Neuroimaging studies reveal a network of brain regions involved in spatial navigation

Neurosynth was used to perform an automated meta-analysis of 64 studies of human navigation (www.neurosynth.org), revealing common activation across these studies in the hippocampus (Hipp), as well as parahippocampal, retrosplenial, and entorhinal cortices, among other regions (Map thresholded at p<0.01, FDR-corrected). This navigational network overlaps with three regions (OPA, RSC, OPA) that response strongly during viewing of scenes and buildings, which were defined in a large group of participants (n=42) using standard methods. Only the right hemisphere inflated cortical surface is shown, though similar regions are also found in the left hemisphere.

Figure 2. Map- and grid-like coding of navigable space in humans

A) Evidence from fMRI adaptation. When viewing images of landmarks from a familiar college campus, fMRI activity in the left hippocampus scales with the real-world distance between the landmark shown on each trial and the landmark shown on the immediately preceding trial (adapted from ref. 25). B) Evidence from multi-voxel pattern analysis (MVPA). Voxelwise activity patterns in the hippocampus reflect distances between events intermittently logged by a camera worn by participants in the 30 days prior to the scan (aerial map of navigated territory shown on the left, as well as example pictures; adapted from ref. 28). C) Evidence from an encoding model. Participants performed a virtual reality navigation task. Grid cells in an individual rat all have the same orientation (φ; top row), and thus it was predicted that movements aligned with the grid orientation should result in more fMRI activity than movements misaligned with the grid. The expected pattern of results was observed in human entorhinal cortex (EC, bottom row; adapted from ref. 29)

Figure 3. Anchoring the cognitive map to the world

A) In oriented rats, from trial-to-trial, the orientation of the hippocampal map is set by featural cues on the walls of the chamber, rotating in concert with rotation of those cues. B) Following disorientation, the hippocampal map is anchored primarily by the geometric shape of the chamber rather than featural cues. For this example place cell, from trial-to-trial, two place fields were observed relative to chamber geometry, one being 180° rotation of the other, mirroring the chamber’s geometric symmetry (adapted from ref. 64). C) fMRI evidence that human retrosplenial/medial parietal region represents heading direction (adapted from ref. 87). During scanning, participants were shown pictures associated with different facing directions learned in a virtual-reality arena (left). fMRI adaptation was found in medial parietal cortex (BA 31) when the same facing direction was elicited on successive trials (right). D) fMRI evidence that the retrosplenial complex (RSC) represents heading in a local reference frame (adapted from ref. 85). During training before scanning, participants learned the locations of objects (denoted by circles) inside virtual reality museums. During scanning, participants performed a task that required them to imagine facing each object encountered during training. Multivoxel activity patterns in RSC were similar for facing directions across the two museums defined in a local, but not global, reference frame. E) In rodents, retrosplenial cortex (RSP) contains both “bidirectional” (BD) cells that represent heading in a local reference frame and head direction (HD) cells that represent heading in a global reference frame (adapted from ref. 95).

Figure 4. Hippocampus codes metrics of the environment along a journey

A) Map showing an example street journey in London’s Soho that was used in Howard et al. (2014) and Javadi et al. (2017), . At various points in the journey, entorhinal cortex codes the Euclidean distance to the goal, while the right posterior hippocampus codes path distance, an interaction between goal direction and path distance, as well as a more complex aspects of environment, such as how many other streets a given street is connected with (degree centrality). Right anterior hippocampus (not shown) activity increases when entering streets with high global connections (closeness centrality). B) Left: Path distance and goal direction coding has also been found in the hippocampus of bats while they freely fly towards a target location. Activity increases as the goal is closer and more directly ahead (adapted from ref. 10).

Figure 5. Frontal areas involved in planning during navigation

A number of prefrontal areas have been identified that support navigation in humans. Inferior lateral prefrontal activity has been shown to correlate with the number of possible paths available at a choice point (A), while lateral PFC and superior frontal gyrus activations have been found when participants encounter a detour and need to find an alternative way (B&C). Hierarchical planning involves dorsal-medial frontal areas, independent of distance to the goal. In the example shown in D, the two routes the goals are equal in length, but one involves multiple turns and street segments, and intersections where decisions need to be made thus requiring a hierarchical route plan.