Direct recordings of grid-like neuronal activity in human spatial navigation

Abstract

Grid cells in the entorhinal cortex appear to represent spatial location via a triangular coordinate system. Such cells, which have been identified in rats, bats and monkeys, are believed to support a wide range of spatial behaviors. Recording neuronal activity from neurosurgical patients performing a virtual-navigation task, we identified cells exhibiting grid-like spiking patterns in the human brain, suggesting that humans and simpler animals rely on homologous spatial-coding schemes.

Figure 1. Virtual navigation task

A. Patient’s view of the experiment. B. Mean duration of successive deliveries in the task, averaged across consecutive pairs of deliveries. Error bars denote 95% confidence intervals. C. Mean excess path length.

Figure 2. Examples of grid-like spatial firing

A. The activity of a cell from Patient 6’s left entorhinal cortex (EC). The left panel shows an overhead view of the environment, with color representing the firing rate (in Hz) at each virtual location (See also Fig. S6). The middle panel depicts the 2-D autocorrelation of the cell’s activity. Peaks in the autocorrelation function determine the spacing and angle of the fitted grid, which is then used to plot the estimated grid peaks as white ×s across the entire environment. Right panel shows the cell’s spike waveform. This cell had a gridness score of 0.51. B. The firing of a different cell from Patient 10’s right EC (gridness score 0.63). C & D. The firing of a cell from Patient 10’s right EC in two consecutive sessions (gridness scores 0.6 and 0.74, respectively). E. The activity of a different cell from Patient 10’s right EC (gridness score 0.63). F. The activity of a cell from Patient 11’s right cingulate cortex (CC) (gridness score 0.67). G. The activity of a cell from Patient 7’s right CC (gridness score 0.51). H. The activity of a cell from Patient 7’s right CC (gridness score 0.8). I. The activity of a cell from Patient 10’s right hippocampus (gridness score 0.46). J. The activity of a cell from Patient 10’s right parahippocampal gyrus (gridness score 0.72).

Figure 3. Population measurements of cells exhibiting significant grid-like spatial firing

A. The distribution of gridness scores from each region. Black bars indicate the gridness scores of cells that exhibited significant grid-like activity (p<0.05), gray bars indicate other cells. Region labels: EC, entorhinal cortex; H, hippocampus; PHG, parahippocampal gyrus; A, amygdala; CC, cingulate cortex; Cx, frontal cortex. B. The proportion of significant grid-like cells across regions. Dotted line indicates the Type 1 error rate (5%). Asterisks denote regions where the observed number of cells exceeds the Type 1 error rate at p<0.01 (binomial test). C. The significance of cells exhibiting 4-, 6-, 8-, and 10-fold symmetric activity (binomial test).