Misun Kim

Hexadirectional modulation (HexMod) of macroscopic neural activity by movement direction is widely used to measure grid cell activity in human neuroimaging, but its neuronal origin is unclear. Two mechanisms have been proposed: conjunctive grid×direction cells whose preferred directions align with the grid axes, and firing rate adaptation, which reduces firing when grid fields are visited in quick succession during movement along grid axes. Analysing almost 4,000 grid cells from foraging rats, we found that conjunctive cells’ directional tuning was broad and unaligned with grid axes, whereas firing was reduced shortly after grid field visits, consistent with firing rate adaptation. Simulations of realistic grid cell populations demonstrate HexMod with the typical trajectories of human experiments, and show how it depends on grid scale, adaptation time constant, movement speed, and controlling for variation with location. We show firing rate adaptation provides a plausible mechanism for HexMod and a framework for relating human neuroimaging to neuronal activity.

Humans build mental models of the world and utilize them for various cognitive tasks. The exact form of cognitive maps is not fully understood, especially for novel and complex environments beyond the flat Euclidean environment. To address this gap, we investigated path integration—a critical process underlying cognitive mapping—and spatial-memory capacity on the spherical (non-Euclidean) and planar (Euclidean) environments in young healthy adults ( N = 20) using immersive virtual reality. We observed a strong Euclidean bias during the path-integration task on the spherical surface, even among participants who possessed knowledge of non-Euclidean geometry. Notably, despite this bias, participants demonstrated reasonable navigation ability on the sphere. This observation and simulation suggest that humans navigate nonflat surfaces by constructing locally confined Euclidean maps and flexibly combining them. This insight sheds light on potential neural mechanisms and behavioral strategies for solving complex cognitive tasks.

Humans build mental models of the world and utilize them for various cognitive tasks. The exact form of cognitive maps is not fully understood, especially for novel and complex environments beyond the flat Euclidean environment. To address this gap, we investigated path integration - a critical process underlying cognitive mapping - and spatial memory capacity on the spherical (non-Euclidean) and planar (Euclidean) environments in young healthy adults (n=20) using immersive virtual reality. We observed a strong Euclidean bias during the path integration task on the spherical surface, even among participants who possessed knowledge of non-Euclidean geometry. Notably, despite this bias, participants demonstrated reasonable navigation ability on the sphere. This observation and simulation suggest that humans navigate non-flat surfaces by constructing locally confined Euclidean maps and flexibly combining them. This insight sheds light on potential neural mechanisms and behavioral strategies for solving complex cognitive tasks.

Terrains in a 3D world can be undulating. Yet, most prior research has exclusively investigated spatial representations on a flat surface, leaving a 2D cognitive map as the dominant model in the field. Here, we investigated whether humans represent a curved surface by building a dimension-reduced flattened 2D map or a full 3D map. Participants learned the location of objects positioned on a flat and curved surface in a virtual environment by driving on the concave side of the surface (Experiment 1), driving and looking vertically (Experiment 2), or flying (Experiment 3). Subsequently, they were asked to retrieve either the path distance or the 3D Euclidean distance between the objects. Path distance estimation was good overall, but we found a significant underestimation bias for the path distance on the curve, suggesting an influence of potential 3D shortcuts, even though participants were only driving on the surface. Euclidean distance estimation was better when participants were exposed more to the global 3D structure of the environment by looking and flying. These results suggest that the representation of the 2D manifold, embedded in a 3D world, is neither purely 2D nor 3D. Rather, it is flexible and dependent on the behavioral experience and demand.

With the proliferation of GPS technology, studying how humans and other animals find their way using the Sun, stars, and landmarks may feel ancient and irrelevant. However, two recent books convincingly argue that such endeavors are well worth our time. In Supernavigators, David Barrie tells astounding tales of how various animals navigate the world and the equally intriguing stories of the scientists who study them. Exchanging animal migration for human navigation, in Wayfinding, M. R. O9Connor offers stories from the Arctic, Australia, and the South Pacific, where people still practice traditional methods of navigation in the seemingly featureless landscapes of snow, sand, and water.

Head direction cells are critical for navigation because they convey information about which direction an animal is facing within an environment. To date, most studies on head direction encoding have been conducted on a horizontal two‐dimensional (2D) plane, and little is known about how three‐dimensional (3D) direction information is encoded in the brain despite humans and other animals living in a 3D world. Here, we investigated head direction encoding in the human brain while participants moved within a virtual 3D “spaceship” environment. Movement was not constrained to planes and instead participants could move along all three axes in volumetric space as if in zero gravity. Using functional magnetic resonance imaging (fMRI) multivoxel pattern similarity analysis, we found evidence that the thalamus, particularly the anterior portion, and the subiculum encoded the horizontal component of 3D head direction (azimuth). In contrast, the retrosplenial cortex was significantly more sensitive to the vertical direction (pitch) than to the azimuth. Our results also indicated that vertical direction information in the retrosplenial cortex was significantly correlated with behavioral performance during a direction judgment task. Our findings represent the first evidence showing that the “classic” head direction system that has been identified on a horizontal 2D plane also seems to encode vertical and horizontal heading in 3D space in the human brain.

It is widely agreed that patients with bilateral hippocampal damage are impaired at binding pairs of words together. Consequently, the verbal paired associates (VPA) task has become emblematic of hippocampal function. This VPA deficit is not well understood and is particularly difficult for hippocampal theories with a visuospatial bias to explain (e.g., cognitive map and scene construction theories). Resolving the tension among hippocampal theories concerning the VPA could be important for leveraging a fuller understanding of hippocampal function. Notably, VPA tasks typically use high imagery concrete words and so conflate imagery and binding. To determine why VPA engages the hippocampus, we devised an fMRI encoding task involving closely matched pairs of scene words, pairs of object words, and pairs of very low imagery abstract words. We found that the anterior hippocampus was engaged during processing of both scene and object word pairs in comparison to abstract word pairs, despite binding occurring in all conditions. This was also the case when just subsequently remembered stimuli were considered. Moreover, for object word pairs, fMRI activity patterns in anterior hippocampus were more similar to those for scene imagery than object imagery. This was especially evident in participants who were high imagery users and not in mid and low imagery users. Overall, our results show that hippocampal engagement during VPA, even when object word pairs are involved, seems to be evoked by scene imagery rather than binding. This may help to resolve the issue that visuospatial hippocampal theories have in accounting for verbal memory.

Humans commonly operate within 3D environments such as multifloor buildings and yet there is a surprising dearth of studies that have examined how these spaces are represented in the brain. Here, we had participants learn the locations of paintings within a virtual multilevel gallery building and then used behavioral tests and fMRI repetition suppression analyses to investigate how this 3D multicompartment space was represented, and whether there was a bias in encoding vertical and horizontal information. We found faster response times for within-room egocentric spatial judgments and behavioral priming effects of visiting the same room, providing evidence for a compartmentalized representation of space. At the neural level, we observed a hierarchical encoding of 3D spatial information, with left anterior hippocampus representing local information within a room, while retrosplenial cortex, parahippocampal cortex, and posterior hippocampus represented room information within the wider building. Of note, both our behavioral and neural findings showed that vertical and horizontal location information was similarly encoded, suggesting an isotropic representation of 3D space even in the context of a multicompartment environment. These findings provide much-needed information about how the human brain supports spatial memory and navigation in buildings with numerous levels and rooms.