Landmark-modulated directional coding in postrhinal cortex

Abstract

Visual landmarks can anchor an animal's internal sense of orientation to the external world. The rodent postrhinal cortex (POR) may facilitate this processing. Here, we demonstrate that, in contrast to classic head direction (HD) cells, which have a single preferred orientation, POR HD cells develop a second preferred orientation when an established landmark cue is duplicated along another environmental wall. We therefore refer to these cells as landmark-modulated-HD (LM-HD) cells. LM-HD cells discriminate between landmarks in familiar and novel locations, discriminate between visually disparate landmarks, and continue to respond to the previous location of a familiar landmark following its removal. Rats initially exposed to different stable landmark configurations show LM-HD tuning that may reflect the integration of visual landmark information into an allocentric HD signal. These results provide insight into how visual landmarks are integrated into a framework that supports the neural encoding of landmark-based orientation.

Fig. 1.. AB session.

(A) Left: Nissl-stained sagittal section from one rat showing anatomical borders and cannula track through POR. Right: Atlas diagram showing anatomical borders between brain regions visible in the sagittal section to the left. PaS, parasubiculum; HPC, hippocampus. (B) Experimental design for the AB experiment. Top-down view of the recording arena showing the locations of visual cues across A1, AB, and A2 sessions, as well as the reference frame for measuring allocentric HD. (C) Histogram of A1 HD PFDs for all 87 POR LM-HD cells recorded in the AB experiment. Note the clustering around 270° (looking toward the cue) and 90° (looking away from the cue). (D) Tuning curves for three example POR LM-HD cells recorded across A1, AB, and A2 sessions that showed peak-locked tuning relative to the visual cues. (E) Same as (C) but for two LM-HD cells that showed trough-locked tuning. (F) Normalized tuning curves for all POR LM-HD cells recorded in the AB experiment. The first 40 cells show trough-locked firing, whereas the remaining 47 are peak-locked; this separation is indicated by a red arrow. (G) Comparison of BI between the initial A1 session and both AB and A2 sessions, showing an increase in bidirectionality during the AB session. Asterisk (*) denotes statistical significance. (H) Scatter plot depicting the degree of firing rate modulation attributed to cue A or cue B for all POR LM-HD cells recorded during the AB session. Black line shows x = y. Note that modulation was generally stronger for cue A than cue B. (I) Tuning curves for a representative ATN HD cell recorded across A1, AB, and A2 sessions. (J) Same as (F) but for ATN HD cells. (K) Same as (G) but for ATN HD cells.

Fig. 2.. AB_west session.

(A) Experimental design for the AB_west experiment. A top-down view of the recording arena demonstrating the locations of visual cues across A1, AB_west, and A2 sessions, as well as the reference frame for measuring allocentric HD. (B) Tuning curves for an example peak-locked POR LM-HD cell (left) and a trough-locked POR LM-HD cell (right) recorded across A1-AB_west-A2 sessions that showed broadening of their tuning curves in the direction of the new cue location. (C) Normalized tuning curves for all POR LM-HD cells recorded across the three sessions of the AB_west experiment. (D) Scatter plot showing the degree of firing rate modulation that each cell displayed relative to each cue. Note that modulation relative to cue A was generally stronger than to cue B_west. Black line shows x = y. (E) Cross-correlation of tuning curves between A1 and A2 sessions (blue) and between A and B_west sessions (black). Note that the A1 × AB_west correlations are shifted counterclockwise and show a small bump at 270° corresponding to the location of cue B_west. The location of this bump is indicated by the vertical line labeled B_west. Error bars show SEMs.

Fig. 3.. No cue session.

(A) Top-down view of the A1–No cue–A2 experiment showing locations of visual cues. (B) Tuning curves for an example peak-locked POR LM-HD cell (left) and an example trough-locked cell (right) that reduced their tuning strength when cue A was removed. (C) Normalized tuning curves for all POR LM-HD cells recorded in the No cue experiment. (D) Comparison of BI between A1 and both No cue and A2 sessions. Note that cells did not become bidirectional during the No cue or A2 sessions. (E) Comparison of tuning strength as measured by the MI (see Methods) between the initial A1 session and both No cue and A2 sessions, showing a decrease in modulation during the No cue session. (F) Tuning curves for a POR LM-HD cell that stayed strongly tuned across all sessions. (G) Tuning curves for an example POR LM-HD cell that showed almost complete tuning degradation during the No cue session. (H) Tuning curves for an example ATN HD cell that maintained its firing properties across all sessions. (I) Change in MI between the A1 condition and both No cue and A2 conditions for ATN HD cells. (J) Experimental design for the A1–AB–No cue–A2 experiment. (K) Normalized tuning curves for all POR LM-HD cells recorded in the A1–AB–No cue–A2 experiment. (L) Tuning curves for two example peak-locked LM-HD cells. Note that both cells show bidirectionality during the AB session but not during the No cue session where they show unidirectional firing of reduced magnitude. (M) Comparison of tuning strength (MI) between the initial A1 session and both No cue and A2 sessions, showing a decrease in tuning strength for the No cue session. (N) Comparison of BI between different sessions. Only the AB session displayed increased bidirectionality. Asterisk (*) denotes statistical significance.

Fig. 4.. B session.

(A) Experimental design for the B experiment. Top-down view of the recording arena showing the locations of visual cues across A1, B, and A2 sessions, as well as the reference frame for measuring allocentric HD. (B) Tuning curves for two example POR LM-HD cell that showed trough-locked (left) or peak-locked (right) tuning relative to both cue B and the previous location of cue A. (C) Normalized tuning curves for all POR LM-HD cells recorded in the B experiment. (D) Comparison of BI between the initial A1 session and both B and A2 sessions, showing an increase in bidirectionality during the B session. Asterisk (*) denotes statistical significance. (E) Scatter plot comparing the degree of firing rate modulation attributed to cues A and B during the B session for all recorded POR HD cells. Black line shows x = y. (F) Normalized tuning curves for LM-HD cells recorded during the B experiment that have been split according to whether their firing during the B session mostly favors cue A (MI_A − MI_B > 0.2), upper row or cue B (MI_A − MI_B < −0.2), lower row. (G) Tuning curves for an example POR LM-HD cell that remained tuned to cue A across all sessions. (H) Tuning curves for an example POR LM-HD cell that switched to mainly encoding cue B during the B session. (I) Cross-correlation between A1 and B session tuning curves, split according to the groupings in (F). Note that cells preferring cue A show a peak near 0°, while cells preferring cue B show a peak near 180° (J) Tuning curves for an example ATN HD cell that maintained its firing properties across all sessions. (K) Change in bidirectionality from session A1 to sessions B and A2 for ATN HD cells.

Fig. 5.. AC session.

(A) Experimental design for the AC experiment. Top-down view of the recording arena showing the locations of visual cues across A1, AC, and A2 sessions, as well as the reference frame for measuring allocentric HD. (B) Tuning curves for an example POR LM-HD cell recorded across A1, AC, and A2 sessions that did not respond to the addition of cue C. (C) Normalized tuning curves for all POR LM-HD cells recorded in the AC experiment. (D) Comparison of BI between the initial A1 session and both AC and A2 sessions, showing no change in bidirectionality in either session. (E) Scatter plot comparing the degree of firing rate modulation attributed to cues A and C during the AC session for all recorded POR LM-HD cells. Black line shows x = y. Note that cells largely showed stronger tuning to cue A than cue C. (F) Tuning curves for two co-recorded POR LM-HD cells, one of which did not respond to the addition of cue C (left) while the other became bidirectional (right); note the increase in firing rate around 30°.

Fig. 6.. Effects of habituation to different cue configurations.

(A) Experimental design for the AB black experiment. Top-down view showing the locations of visual cues across A1 black, AB black, and A2 black sessions. (B) Tuning curves for two example POR LM-HD cells from the AB black experiment that showed bidirectional tuning in the AB black session. (C) Normalized tuning curves for all POR LM-HD cells recorded in the AB black experiment. (D) Comparison of BI between A1 black and both AB black and A2 black sessions. Asterisk (*) denotes statistical significance. Note that bidirectionality was increased in the AB black session relative to both A1 black and A2 black sessions, although it was slightly elevated in the A2 black session. (E) Distribution of HD PFDs for all LM-HD cells recorded in the A1 black session. (F) Experimental design for the AB1-A-AB2 experiment. (G) Tuning curves for two example POR LM-HD cells recorded across the sessions of the AB1-A-AB2 experiment that showed largely unidirectional tuning in all sessions. (H) Normalized tuning curves for all POR LM-HD cells recorded in the AB1-A-AB2 experiment. (I) Comparison of BI between AB1 and both A and AB2 sessions. (J) Distribution of HD PFDs for all LM-HD cells recorded in the AB1 session. (K) Experimental design for the No cue 1–AB–No cue 2 experiment. (L) Tuning curves for two example POR LM-HD cells recorded across the sessions of the No cue 1–AB–No cue 2 experiment that showed unidirectional tuning in all sessions. (M) Normalized tuning curves for all POR LM-HD cells recorded in the No cue 1–AB–No cue 2 experiment. (N) Comparison of BI between No cue 1 and both AB and No cue 2 sessions. (O) Distribution of HD PFDs for all LM-HD cells recorded in the No cue 1 session.