Temporal frequency of subthreshold oscillations scales with entorhinal grid cell field spacing

Abstract

Grid cells in layer II of rat entorhinal cortex fire to spatial locations in a repeating hexagonal grid, with smaller spacing between grid fields for neurons in more dorsal anatomical locations. Data from in vitro whole-cell patch recordings showed differences in frequency of subthreshold membrane potential oscillations in entorhinal neurons that correspond to different positions along the dorsal-to-ventral axis, supporting a model of physiological mechanisms for grid cell responses.

Fig. 1

Higher frequency of subthreshold oscillations in dorsal versus ventral entorhinal cortex. A. Top: Dorsal view of brain after slicing. Bottom: Sagittal view showing anatomical location of horizontal slices A to H. B. Mean frequency of subthreshold oscillations for neurons from dorsal slices (3.8 – 4.9 mm Bregma) and ventral slices (4.9 – 7.1 mm Bregma) at −50 mV and −45 mV. C. Subthreshold oscillation frequency plotted versus anatomical distance from dorsal surface. D. Examples of subthreshold oscillations at −50 mV in dorsal regions (left) and ventral regions (right). E. Corresponding autocorrelations used to measure frequency in D.

Fig. 2

Differences in resonance properties of neurons in dorsal versus ventral entorhinal cortex. A. Examples of resonance responses of neurons in dorsal (blue traces) and ventral entorhinal cortex (red traces) in response to impedance amplitude profile (ZAP) stimulus (black). B. Histogram of mean peak resonance frequency for neurons in dorsal versus ventral entorhinal cortex. C. Resonance frequency plotted versus anatomical distance from the dorsal surface.

Fig. 3

Relationship of subthreshold membrane potential oscillations to sag potential. For single neurons in dorsal (A) and ventral entorhinal cortex (B), traces on left show membrane potential responses to multiple current injection levels. Single traces (right) show sag potentials at higher resolution. C. First time constant of sag potential (ms) plotted versus anatomical location. D. Time constant of sag potential plotted versus subthreshold oscillation frequency.

Fig. 4

Subthreshold oscillations may underlie differences in grid field spacing. A. Reciprocal of oscillation frequency plotted versus anatomical depth for anatomical range matching a previous publication (7) as shown in B. C–D. Simulation of grid cell model (3, 8). Top: Gray indicates trajectory of simulated rat. Red indicates firing locations. Bottom: Firing rate map (red=maximum, blue=no spikes). Grid field spacing is small for mean dorsal oscillation frequency of 6.42 Hz (C) and larger for mean ventral frequency of 4.23 Hz (D).