Effect of reward on electrophysiological signatures of grid cell population activity in human spatial navigation

Abstract

The regular equilateral triangular periodic firing pattern of grid cells in the entorhinal cortex is considered a regular metric for the spatial world, and the grid-like representation correlates with hexadirectional modulation of theta (4-8 Hz) power in the entorhinal cortex relative to the moving direction. However, researchers have not clearly determined whether grid cells provide only simple spatial measures in human behavior-related navigation strategies or include other factors such as goal rewards to encode information in multiple patterns. By analysing the hexadirectional modulation of EEG signals in the theta band in the entorhinal cortex of patients with epilepsy performing spatial target navigation tasks, we found that this modulation presents a grid pattern that carries target-related reward information. This grid-like representation is influenced by explicit goals and is related to the local characteristics of the environment. This study provides evidence that human grid cell population activity is influenced by reward information at the level of neural oscillations.

Figure 1

Paradigm and behavioral division with the effect of goals. (A) The four task stages of each trial in the memory task performed by the participants (adapted from Chen et al. (Current Biology, 2018)). (B) An aerial view of the circular arena. The drop error is defined as the relative distance between the subjective response location and the reallocation. (C) Two types of groups are defined by drop error in behavior. The top row is GoodPerf, and the bottom row is BadPerf. The middle column is the trajectory of the participants, achieving extensive coverage in both groups. The right-most column shows the movement direction of the participants, which is evenly distributed at all angles between the two groups (Rayleigh’s tests for non-uniformity, p > 0.05). (D) Comparison of experimental data between GoodPerf and BadPerf. A significant difference was not observed between the two groups (t test, p > 0.5). (E) Comparison of performance in the trials corresponding to GoodPerf and BadPerf goal objects. The difference in drop error between the two groups was significant (t test, p < 0.001). (F) An example of the time sequence of GoodPref and BadPref trials during the whole experiment period (taking subject #1 as an example), and the trial sequence number index of each type group is calculated based on the average sequence number of all trials in this category. (G) Temporal distribution of the two groups in the experiment. We define the trial serial number index to represent the temporal distribution, represented by the average serial number of all trials in each group in the experiment. Statistics showed that Goodpref and Badpref were evenly distributed in the experiment, without significant difference (paired t test, p < 0.05).

Figure 2

Hexadirectional modulation of entorhinal theta power by movement direction under the influence of goals. (A) Depiction of all the electrode contacts in the entorhinal cortex (red dots). (B) According to alignment or misalignment with the preference angle φ (left figure), we predicted the sixfold rotational symmetric sinusoidal modulation of the theta power signal by the moving direction according to the schematic diagram (right, adapted from Maidenbaum et al. (PNAS, 2018)). (C) GoodPerf and BadPerf groups correspond to each rotational symmetric modulation, among which only the sixfold modulation of the BadPerf was significant (t test, p = 0.003). (D) The BadPerf had significantly higher hexadirectional modulation than the GoodPerf (t test, p < 0.01).

Figure 3

Theta power comparison in the case of movements aligned and misaligned with the grid axe of periodic symmetry. (A) Theta power of sixfold symmetry in GoodPref. (B) Theta power is higher during movements aligned with the grid axes as compared to misaligned movements. of sixfold symmetry in BadPref. (C–F) Theta power under other rotation symmetries (4/5/7/8-fold) in BadPref did not show the alternating trend of the high and low differences between aligned and misaligned.

Figure 4

Spatial characteristics of the two groups of hexadirectional modulation. (A) All types of periodic rotation symmetries of the GoodPerf group are not significant in the space boundary region and the central region (t test, p > 0.05). (B) The BadPerf group shows no obvious directional modulation in the boundary region, but displays significant six-directional modulation in the central region (t test, p = 0.005).

Figure 5

Analysis of symmetric rotational modulation using different partitioning radii. (A) For sixfold modulation, the BadPerf group shows a significant difference when the dividing radius of the boundary region and central region is 800–900 virtual units (t test, p < 0.001), while GoodPerf shows no significance for all the partition radius (t test, p > 0.05). (B) For the GoodPerf group, the modulation of other rotation symmetries (4/5/7/8-fold) is not significant (t test, p > 0.05) in the central area (left panel) and the boundary area (right panel). (C) For the Boodobj group, the directional modulation of the 4/5/7/8-fold rotational symmetry is also not significant (t test, p > 0.05) in the central area (left panel) and the boundary area (right panel).