Head direction cell representations maintain internal coherence during conflicting proximal and distal cue rotations: comparison with hippocampal place cells

Abstract

Place cells of the hippocampal formation encode a spatial representation of the environment, and the orientation of this representation is apparently governed by the head direction cell system. The representation of a well explored environment by CA1 place cells can be split when there is conflicting information from salient proximal and distal cues, because some place fields rotate to follow the distal cues, whereas others rotate to follow the proximal cues (Knierim, 2002a). In contrast, the CA3 representation is more coherent than CA1, because the place fields in CA3 tend to rotate in the same direction (Lee et al., 2004). The present study tests whether the head direction cell network produces a split representation or remains coherent under these conditions by simultaneously recording both CA1 place cells and head direction cells from the thalamus. In agreement with previous studies, split representations of the environment were observed in ensembles of CA1 place cells in approximately 75% of the mismatch sessions, in which some fields followed the counterclockwise rotation of proximal cues and other fields followed the clockwise rotation of distal cues. However, of 225 recording sessions, there was not a single instance of the head direction cell ensembles revealing a split representation of head direction. Instead, in most of the mismatch sessions, the head direction cell tuning curves rotated as an ensemble clockwise (94%) and in a few sessions rotated counterclockwise (6%). The findings support the notion that the head direction cells may be part of an attractor network bound more strongly to distal landmarks than proximal landmarks, even under conditions in which the CA1 place representation loses its coherence.

Figure 1.

Schematic representation of the circular track location and the cue configuration. A, Photograph showing the circular track with salient visual and tactile information (proximal cues) in the center of the room, surrounded by the black curtain with distal landmarks. B, The circular track had four different textures as proximal cues (each covering a quadrant of the track) and was placed in the center of the behavioral room, surrounded by a black curtain. The set of distal cues comprised six objects either hanging on the curtain or standing on the floor. Throughout the training, the relationship between proximal and distal cues was that of the standard configuration. During recording sessions, three standard sessions (STD) were interleaved with two mismatch sessions (MIS), in which the cues were rotated in opposite directions (proximal cues CCW; distal cues CW), for a total mismatch of 45°, 90°, 135°, or 180°. Shown in the figure are examples of 180° and 90° mismatch sessions.

Figure 2.

Cresyl violet-stained coronal sections showing representative electrode tracks and recording sites (arrows). A, Hippocampal CA1 region. B, ADN of the thalamus. The majority of head direction cells were recorded from ADN. C-E, In some rats, head direction units were recorded from the border region between the AVN and VAN of the thalamus (C), the AVN of the thalamus (D), the LDN of the thalamus (E), and the border region between the AVN and RT (F). Scale bars, 1 mm.

Figure 3.

Representative examples of simultaneously recorded CA1 place field rate maps and head direction cell tuning curves across standard and mismatch sessions. In mismatch sessions, some place fields followed the CCW proximal cue rotation (11903-1.1 and 11903-6.7), and some followed the CW distal cue rotation (11903-5.1 and 11903-6.6) within a given ensemble recording. (Numbers below each place field rate map represent maximum firing rates in Hertz.) However, unlike place cells, all of the head direction cells rotated coherently in the mismatch session. The head direction tuning curves of cells 11903-13.1 and 11903-13.2 shifted their preferred firing direction CW by an amount equal to the rotation of the distal cues. (Head direction tuning curves are plotted in polar coordinates. The axes are scaled as follows: 11903-13.1, 80 Hz; 11903-13.2, 30 Hz.) Numbers preceding each row indicate rat number (first three digits) and day of recording, followed by tetrode and cell number. For the color code, red indicates >90% of the peak firing rate for that cell, blue indicates no firing, and intervening colors of the spectrum indicate successive decrements of 10% of the peak firing rate.

Figure 4.

Rotational coherence of head direction cells. Shown are the five head direction cell tuning curves recorded simultaneously in a single recording session across standard (STD) and mismatch (MIS) conditions from the ADN. All five head direction tuning curves shifted their preferred firing direction CW by an amount equal to the rotation of distal cues. (The axes for each cell are scaled as follows: 11908-12.1, 112 Hz; 11908-12.2, 41 Hz; 11908-13.1, 110 Hz; 11908-13.2, 80 Hz; 11908-13.3, 156 Hz.) Numbers preceding each row indicate rat number (first three digits) and day of recording, followed by tetrode and cell number.

Figure 5.

Summary of CA1 place field and head direction cell tuning curve rotations. Each dot on the polar plot (open dots, 10 data points; filled dots, 1 data point) represents the amount of rotation of a CA1 place field and a head direction cell tuning curve between two standard sessions (A, C) and between standard (STD) versus different mismatch (MIS) sessions (45°, 90°, 135°, and 180°) (B, D). The arrows represent the mean angle of rotation of the population, and the length of the arrow represents the angular dispersion around the mean. The dashed lines indicate the rotation amounts of the proximal (CCW) and distal (CW) cue sets. Because cells were recorded over multiple sessions and days, each dot does not correspond to a unique cell. P, Proximal cue; D, distal cue.

Figure 6.

Split representation in mismatch sessions. A total of 90 mismatch sessions were recorded out of 225 recording sessions. In 75% of the mismatch sessions, the hippocampal CA1 ensembles revealed split representations in which some place fields rotated CW and some rotated CCW in the same dataset. In contrast, the head direction (HD) cells always rotated either CW (94%) or CCW (6%) as an ensemble in mismatch sessions, never showing a split representation of head direction.

Figure 7.

Split control of CA1 place cell ensembles. The occurrence of partial remapping in place cells might contribute to the observed split representation by place cells if randomly remapped fields happen to fall within the range of nondominant cue rotation. To rule out this possibility, the data were statistically analyzed on 88 cells that formed a group that was not controlled by the dominant set of cues. If these cells were controlled by the nondominant set of cues, then their place fields should cluster within the 45° range centered on the rotation of that cue set. Alternatively, if they remap to arbitrary angles, then the location of their place fields should be distributed randomly. One-half of the place fields rotated within the 45° range of nondominant cue control, and the other half rotated outside this range, which is different from the expected chance distribution (χ² = 28.35; p < 0.0001).

Figure 8.

Hypothetical pathways by which proximal and distal cue information may reach the hippocampus. Distal landmarks may provide orientation information via head direction cell control over medial entorhinal input into the hippocampus. Proximal cues are hypothesized to exert control via an object/item pathway through the lateral entorhinal cortex.