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

Journal name:
Nature Neuroscience
Volume:
16,
Pages:
1188–1190
Year published:
DOI:
doi:10.1038/nn.3466
Received
Accepted
Published online

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.

At a glance

Figures

  1. Virtual navigation task.
    Figure 1: Virtual navigation task.

    (a) Participant's view of the experiment. (b) Mean duration of successive deliveries in the task, averaged across consecutive pairs of deliveries. (c) Mean excess path length. VRU is a measure of virtual distance. Error shading denotes 95% confidence intervals.

  2. Examples of grid-like spatial firing.
    Figure 2: Examples of grid-like spatial firing.

    (a) The activity of a cell from participant 6's left entorhinal cortex. Left, overhead view of the environment, with color representing the firing rate (in Hz) at each virtual location. Middle, two-dimensional autocorrelation of the cell's activity. Peaks in the autocorrelation function determined the spacing and angle of the fitted grid, which was then used to plot the estimated grid peaks (white ×) across the entire environment. Right, cell spike waveform; red denotes mean. This cell had a gridness score of 0.51. (b) The firing of a cell from participant 10's right entorhinal cortex (gridness score = 0.63). (c,d) The firing of a different cell from participant 10's right entorhinal cortex in two consecutive sessions (gridness scores = 0.60 and 0.74). (e) The activity of a different cell from participant 10's right entorhinal cortex (gridness score = 0.63). (f) The activity of a cell from participant 11's right cingulate cortex (gridness score = 0.67). (g) The activity of a cell from participant 7's right cingulate cortex (gridness score = 0.51). (h) The activity of a different cell from participant 7's right cingulate cortex (gridness score = 0.8). (i) The activity of a cell from participant 10's right hippocampus (gridness score = 0.46). (j) The activity of a cell from participant 10's right parahippocampal gyrus (gridness score = 0.72).

  3. Population measurements of cells exhibiting significant grid-like spatial firing.
    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) and gray bars indicate other cells. A, amygdala; CC, cingulate cortex; Cx, frontal cortex; EC, entorhinal cortex; H, hippocampus; PHG, parahippocampal gyrus. (b) The proportion of significant grid-like cells across regions. Dashed line indicates the type 1 error rate (5%). Asterisks denote regions in which the observed number of cells exceeded the type 1 error rate at P < 0.01 (binomial test). (c) The significance of cells exhibiting four-, six-, eight- and tenfold symmetric activity (binomial test).

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Author information

  1. These authors contributed equally to this work.

    • Itzhak Fried &
    • Michael J Kahana

Affiliations

  1. School of Biomedical Engineering, Science and Health Systems, Drexel University, Philadelphia, Pennsylvania, USA.

    • Joshua Jacobs &
    • Jonathan F Miller
  2. Department of Psychology, Swansea University, Swansea, UK.

    • Christoph T Weidemann
  3. Princeton Neuroscience Institute, Princeton University, Princeton, New Jersey, USA.

    • Alec Solway
  4. Department of Psychology, University of Pennsylvania, Philadelphia, Pennsylvania, USA.

    • John F Burke,
    • Xue-Xin Wei &
    • Michael J Kahana
  5. Department of Neurosurgery, David Geffen School of Medicine and Semel Institute for Neuroscience and Human Behavior, University of California, Los Angeles, California, USA.

    • Nanthia Suthana &
    • Itzhak Fried
  6. Department of Neurology, Thomas Jefferson University, Philadelphia, Pennsylvania, USA.

    • Michael R Sperling
  7. Department of Neurosurgery, Thomas Jefferson University, Philadelphia, Pennsylvania, USA.

    • Ashwini D Sharan
  8. Functional Neurosurgery Unit, Tel-Aviv Medical Center and Sackler Faculty of Medicine, Tel-Aviv University, Tel-Aviv, Israel.

    • Itzhak Fried

Contributions

The experiment was designed by J.J., C.T.W., M.J.K., A.S. and I.F. Data were collected by J.J., C.T.W., J.F.M., J.F.B., I.F., M.R.S., A.D.S. and N.S. Data analyses were performed by J.J., X.-X.W., C.T.W., A.S. and M.J.K. J.J. and M.J.K. wrote the manuscript.

Competing financial interests

The authors declare no competing financial interests.

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