Hippocampal place cell instability after lesions of the head direction cell network

Abstract

The occurrence of cells that encode spatial location (place cells) or head direction (HD cells) in the rat limbic system suggests that these cell types are important for spatial navigation. We sought to determine whether place fields of hippocampal CA1 place cells would be altered in animals receiving lesions of brain areas containing HD cells. Rats received bilateral lesions of anterodorsal thalamic nuclei (ADN), postsubiculum (PoS), or sham lesions, before place cell recording. Although place cells from lesioned animals did not differ from controls on many place-field characteristics, such as place-field size and infield firing rate, the signal was significantly degraded with respect to measures of outfield firing rate, spatial coherence, and information content. Surprisingly, place cells from lesioned animals were more likely modulated by the directional heading of the animal. Rotation of the landmark cue showed that place fields from PoS-lesioned animals were not controlled by the cue and shifted unpredictably between sessions. Although fields from ADN-lesioned animals tended to have less landmark control than fields from control animals, this impairment was mild compared with cells recorded from PoS-lesioned animals. Removal of the prominent visual cue also led to instability of place-field representations in PoS-lesioned, but not ADN-lesioned, animals. Together, these findings suggest that an intact HD system is not necessary for the maintenance of place fields, but lesions of brain areas that convey the HD signal can degrade this signal, and lesions of the PoS might lead to perceptual or mnemonic deficits, leading to place-field instability between sessions.

Figure 1.

Diagram of cue card position and order of sessions during the standard session (A), cue-rotation experiment (B), and cue-removal experiment (C).

Figure 2.

Diagram showing the location and extent of the smallest (black) and largest (gray) lesion observed in animals with ADN lesions (A) or PoS lesions (B). Values located beside each plate represent the distance in millimeters relative to bregma in the rostrocaudal dimension. Plates were reproduced from Paxinos and Watson (1998).

Figure 3.

Representative place/rate plots of standard sessions obtained from three control cells (top row), three cells from ADN-lesioned animals (middle row), and three cells from PoS-lesioned animals (bottom row). The highest firing rate pixels are shown in purple, with firing rates in descending order shown in blue, green, red, and orange. Yellow pixels represent firing rates of zero, and white pixels represent unsampled locations. Cells in the first column were chosen because they were representative of their respective groups in spatial coherence (smoothness of firing rate contours), and cells in the second column were chosen because they were, likewise, representative of their respective groups in the average outfield firing rate.

Figure 4.

Analysis of the directional modulation of place cell activity. A, Histogram showing the distribution of directional information content scores across the three conditions. B, Place/rate plots of two place cells from PoS-lesioned animals showing directional modulation of location-specific activity. For each panel, central plots show location-specific activity across all head directions in the session. The eight plots located around each central plot represent the location-specific activity of the cell when the head of the animal was pointing in the direction represented by the position of the plot (i.e., plots located above the central plot indicate the firing activity of the cell when the animal was facing in the northerly direction). C, A typical cell from a control animal.

Figure 5.

Place/rate plots showing the response of representative place cells from each condition during the three sessions of the cue-rotation experiment. The bottom two plots, Pre-Rotation A and Pre-Rotation B, show the first- and second-half activity of the pre-rotation session shown from the PoS lesion group.

Figure 6.

A, Scatter diagrams showing the amount of angular shift between sessions during cue-rotation experiments. Each plot shows the angular shift of location-specific activity observed between pairs of sessions. The left column shows the amount of angular shift observed in the rotation session relative to the pre-rotation session. The middle column shows the amount of angular shift observed in the counter-rotation session relative to the rotation session. The right column shows the amount of angular shift observed in the counter-rotation session relative to the pre-rotation session. The thick line outside each plot indicates the position of the cue card for the second session in each pair. B, Scatter diagrams showing the amount of angular shift between the first and second halves of pre-rotation sessions (top row) and between the second half of pre-rotation and the first half of rotation sessions (bottom row). In A and B, the angular position of the filled circles represents the angular shift of individual cells between the two sessions. The dotted arrow denotes the expected mean vector angle if the angular shift is perfectly predicted by the cue card, and the solid arrow denotes the observed mean vector angle. The length of the solid arrow denotes the mean vector length, with a length of 1.0 (no variability in shift scores) represented by a vector spanning the radius of the circle.

Figure 7.

A, Representative place/rate plots of cells recorded in the cue-removal experiment. B, Scatter diagrams showing the amount of angular shift observed between consecutive sessions of the cue-removal experiment. In each plot, the dotted arrow denotes the expected mean vector angle if there is no shift between conditions, and the solid arrow denotes the observed mean vector angle. The length of the solid arrow denotes the mean vector length, with a length of 1.0 (no variability in shift scores) represented by a vector spanning the radius of the circle. Group data reflect results similar to those seen for the representative plots shown in A.