Superficial-layer versus deep-layer lateral entorhinal cortex: Coding of allocentric space, egocentric space, speed, boundaries, and corners

Abstract

Entorhinal cortex is the major gateway between the neocortex and the hippocampus and thus plays an essential role in subserving episodic memory and spatial navigation. It can be divided into the medial entorhinal cortex (MEC) and the lateral entorhinal cortex (LEC), which are commonly theorized to be critical for spatial (context) and non-spatial (content) inputs, respectively. Consistent with this theory, LEC neurons are found to carry little information about allocentric self-location, even in cue-rich environments, but they exhibit egocentric spatial information about external items in the environment. The superficial and deep layers of LEC are believed to mediate the input to and output from the hippocampus, respectively. As earlier studies mainly examined the spatial firing properties of superficial-layer LEC neurons, here we characterized the deep-layer LEC neurons and made direct comparisons with their superficial counterparts in single unit recordings from behaving rats. Because deep-layer LEC cells received inputs from hippocampal regions, which have strong selectivity for self-location, we hypothesized that deep-layer LEC neurons would be more informative about allocentric position than superficial-layer LEC neurons. We found that deep-layer LEC cells showed only slightly more allocentric spatial information and higher spatial consistency than superficial-layer LEC cells. Egocentric coding properties were comparable between these two subregions. In addition, LEC neurons demonstrated preferential firing at lower speeds, as well as at the boundary or corners of the environment. These results suggest that allocentric spatial outputs from the hippocampus are transformed in deep-layer LEC into the egocentric coding dimensions of LEC, rather than maintaining the allocentric spatial tuning of the CA1 place fields.

Keywords: entorhinal cortex; hippocampus; medial temporal lobe; parahippocampal.

Figure 1.

Example cresyl violet stained coronal sections showing typical recording sites in the LEC. The arrowheads indicate example tetrode tracks. The LEC area was divided into three regions: the superficial layers (layer II and III), lamina dissecans (layer IV), and deep layers (layer V and VI). The dashed and solid lines in the figure denote the superficial- and deep-layers of LEC, respectively. The numbers indicate the rat identification.

Figure 2.

Comparison of spatial information scores of superficial- and deep-layer LEC neurons. (a) Fifteen example rate maps of cells in the superficial layers of LEC. The number on top for each cell indicates the peak firing rate. White and black shades in the rate maps indicate 0 Hz (no firing) and maximal firing rates, respectively. (b) Fifteen example rate maps of cells in the deep layers of LEC, as shown in (a). (c) Cumulative distribution of spatial information scores of superficial- (black) and deep-layer (gray) LEC neurons. Deep-layer LEC neurons had significantly larger spatial information scores than superficial-layer neurons, although the difference was small. (d) Cumulative distribution of the Pearson’s correlation coefficients between the rate maps of the first and second halves of the session. Deep-layer LEC neurons had significantly larger correlations than superficial-layer neurons.

Figure 3.

Theta modulation of neural firing in deep- and superficial-layers of LEC. (a) Representative spike train autocorrelations of superficial-layer LEC neurons. Most cells did not show evidence of theta-modulated peaks. (b) Example spike train autocorrelations of deep-layer LEC neurons. Numbers on top indicate the spike train spectrum-based theta modulation index. Most cells did not show evidence of theta-modulated peaks. (c) Scatter plot of the spatial information and spike train spectrum-based theta modulation index for all LEC neurons. (d) Cumulative distribution of the theta modulation index for both superficial- and deep-layer LEC neurons. (e) and (f), same as (c) and (d) but for LFP-based, theta phase modulation index.

Figure 4.

Comparison of egocentric properties of superficial- and deep-layer LEC neurons. Some LEC neurons had spatial firing patterns associated with the boundaries or corners of the apparatus. (a) Two example superficial-layer LEC neurons (rows) with egocentric bearing tuning properties with respect to the nearest boundary. Left image, spatial firing rate map, number on top denotes peak firing rate; right curve, egocentric bearing tuning curve, number on top denotes mean vector length. (b) Same as (a) for two example deep LEC neurons. (c) Distributions of ΔBIC_boundary for superficial- and deep-layer LEC neurons.

Figure 5.

Comparison of speed tuning properties of superficial- and deep-layer LEC neurons. Some LEC neurons demonstrated tuning for running speed. (a) Speed tuning curves of 20 example speed selective LEC neurons. (b) Distribution of the empirical speed index for all sampled LEC cells and for the subset of speed selective cells. (c) Same as (b) for the GLM speed index. (d) Scatter plot of the empirical speed index and the GLM speed index for speed selective LEC neurons. (e) Cumulative distribution of the empirical speed index for both superficial- and deep-layer LEC neurons.

Figure 6.

Boundary- and corner-related firing properties in LEC neurons. (a) Examples of boundary-related cells in LEC. For each cell, 3 rate maps are presented: left to right, spatial firing rate map for the whole session, first half session, and second half session. (b) Examples of corner-related cells in LEC. Format is the same as (a). (c) Schematics showing the procedure for calculating the corner score from the spatial firing rate maps. Four corner scores were defined as the relative differences between center and corner portions of each quadrant of the spatial rate map.

Figure 7.

Comparison of corner-related activity between superficial- and deep-layer LEC neurons. (a) Left, average of the normalized spatial rate maps for cells that had spatial information scores greater than 0.2 bit/spike. Right images, three instances of ensemble average fields after randomly relocating the blobs in the individual maps that had a minimum of 5 pixels that exceeded 0.2 bit/spike (numbers on top, ensemble corner score). (b) The ensemble corner score (vertical line) is significantly different from a null distribution created by randomly relocating the spatial blobs in the rate maps. Left to right, real and shuffled ensemble corner score from spatial rate maps with information score greater than 0.05, 0.10, 0.15, 0.2 bit/spike, respectively. (c) Same as (b) except that the statistics were obtained with standard spike shuffling procedures in which the spike trains were circularly shuffled by a random amount relative to the position train. (d) The ensemble corner score of superficial- and deep-layer LEC neurons shows no significant differences. Left to right, real and shuffled ensemble corner score differences (superficial − deep) from spatial rate maps with information score greater than 0.05, 0.10, 0.15, 0.2 bits/spike, respectively.