Article Figures & Data
Figures
- Fig. 1.
Diagram of behavioral apparatus in standard (A) and 90° mismatch (B) configurations. The circular track was composed of four different textured surfaces, each covering one-quarter of the ring: a gray rubber mat with a pebbled surface, brown medium-grit sand paper, beige carpet pad material, and gray duct tape with white tape stripes. The ring was centered inside a 9-foot-diameter black circular curtain. Hanging on the curtain or standing on the floor at the perimeter of the curtain were six objects (see Materials and Methods). Lighting was provided by a single 25 W bulb on the ceiling centered over the ring. In between recording sessions, the track was rotated CCW and the cues on the floor and curtains were rotated CW, as inB.
- Fig. 2.
Representative examples of place cells from a single recording session. The black dots indicate the location of the rat when each spike was fired. Because the rat ran the track in a unidirectional manner, each part of the track was visited in approximately equal proportions. Spikes that occur outside the outlines of the circular track result from instances in which the rat extended its head off the track; these spikes were excluded from the quantitative analyses, because the sampling locations were not consistently reproducible between sessions. In Session 2 (180° mismatch), Cells 1–3 rotated their place fields ∼90° CW to follow the distal cues. Cells 4–6 rotated their place fields ∼90° CCW to follow the local cues. Cell 7 split its place field in two, with one subfield rotating CW and the other CCW.Cell 8 developed a field, whereas Cells 9and 10 lost their fields. Most cells behaved similarly in session 4 (135° mismatch), except that Cell 7 rotated CW rather than spitting its field and Cell 9 rotated CW instead of losing its field.
- Fig. 3.
Summary of place field rotations. Eachdot on the diagram represents the amount of rotation of a single place field between the standard and mismatch sessions.A, Degree of rotation for each place field between two standard sessions (left) and between the standard and mismatch sessions (45, 90,135, and 180°). The distribution of rotation angles for the 45° mismatch sessions was centered around 0°, although a comparison with the standard sessions (left) shows that the variance was greater for the 45° mismatch session. For the 90, 135, and 180° mismatch sessions, the distributions were bimodal, with subsets of cells rotating with the distal cue set and with the local cue set. B, Degree of rotation for each place field broken down by subject. All mismatch session types (45, 90, 135, and 180°) are combined. Thearrow represents the mean angle for that rat, and thelength of the arrow signifies the angular dispersion around the mean (Zar, 1999). Some rats were controlled more strongly by the local cue set (e.g., Rats 20 and21), whereas other rats were controlled more strongly by the distal cue set (e.g., Rats 31 and44).
- Fig. 4.
Split place fields. A, Examples of five cells that split their place fields in the mismatch session.B, Examples of six cells that displayed dynamic changes in their place fields over the time course of a mismatch session.S indicates the location of the place field in the previous standard session, L indicates the location corresponding to precise control by local cues, and Dindicates the location corresponding to precise control by distal cues. Note that because the circular track is plotted along the abscissa, there is a wraparound effect for cells c andd. Cell a initially fired at theD location for the first two laps and then fired at both the D and L locations for the next few laps, and eventually fired almost exclusively at the Llocation for the remainder of the session. Cell b (same cell as cell a in a later session) fired initially at the D location and then developed a split field at both the D and L locations. Cellc initially was silent and then after two laps began to fire in between the S and Llocations. Midway through the session, it developed a split field, firing at the D location as well. (In the subsequent standard and mismatch sessions, this cell lost its strong spatial tuning.) Cell d was fairly quiet for the first eight laps and then began to fire at both the L andD locations. (In the second mismatch session of the day, the place field of cell d was controlled only by the distal cues, but the strength of the field changed over time; it started out weak, became strong for 5–6 laps, and then became weaker again.) Cell e had a strong field at theL location on the first lap only and then became relatively quiet. Cell f was quiet for the first 10 laps and then developed a completely new field near the end of the session. (A shift in the recording electrode after the subsequent standard session made it impossible to determine what cells e andf did on the second mismatch session of the day.)
- Fig. 5.
Place fields that overlap in standard or mismatch sessions. A, Of these three simultaneously recorded cells that had overlapping place fields in the standard session,Cells 1 and 2 rotated CW to follow the distal cues and Cell 3 rotated CCW to follow the local cues. B, Two simultaneously recorded cells that had overlapping place fields in the standard session. Cell 1rotated CCW, and Cell 2 rotated CW in the mismatch session (with a slight subfield rotating CCW). Cell 2retained the subfield in the subsequent standard session. Thus, the subfield initially followed the local cues in the mismatch session but then followed the distal cues when they were rotated back to the standard configuration. C, Two simultaneously recorded cells that had place fields originally ∼180° apart. During the mismatch session, the place fields followed different sets of cues and now overlapped. D, A cross-correlogram demonstrates that the two cells in C fired many spikes within 10 msec of each other. The strong rhythmicity in the correlogram is caused by the strong modulation of the cells by the theta rhythm.
- Fig. 6.
The experience-dependent, backward-shift effect ofMehta et al. (1997). A, The center of mass of each place field was calculated on each lap that the rat ran, and this lap-specific center of mass was subtracted from the center of mass of the place field calculated from the average of all laps in the session. In the standard session (black dots), the center of mass of place fields shifted in a direction opposite to the trajectory of the rat. In the first mismatch session (open squares), this backward shift was greater than in the standard session. B, The magnitude of the effect decreased in subsequent sessions (Standard 2 and Mismatch 2), although the shift was still greater for theMismatch 2 session compared with Standard 2. The effect was absent by the last standard session (Standard 3).
- Fig. 7.
Extrinsic versus intrinsic inputs onto place cells. Distal is shorthand for distal-dominated inputs;local is shorthand for local-dominated inputs.A, A model in which only extrinsic inputs from external cues drive place cells can explain the main effects, but it fails to account for the subtle nonlinear effects of place cells. In this model, remapping might result from cells that are controlled by exact configurations of local and distal cells and become silent or active when presented with new configurations in the mismatch session (AND-gated cells). Split place fields might result from cells that are controlled by either the local or the distal cues (OR-gated cells). B, In a network in which the input from external cues is weak compared with the intrinsic circuitry, the responses of place cells will be dominated by the attractor dynamics of the intrinsic circuitry. Although in this example the local cues dominate over the distal cues, in another session or in another rat, the cells might follow the distal cue set, but they will do so as an integrated ensemble. The differential sensitivity to local versus distal cues does not imply that the black cell is sensitive only to local cues and the white cellsensitive only to distal cues. More likely, each cell gets input from both sets, but because of stochastic differences in input strengths, the black cell has somewhat greater input from local cues, and the white cell has somewhat greater input from distal cues. The differential sensitivity also does not imply that the inputs onto these cells are directly from pure sensory representations of these cues. It is probable that the direct inputs onto place cells are from an intermediary set of cells that are themselves controlled by the cues in complex ways (e.g., head direction cells and entorhinal cortex cells). C, In a network in which the inputs from external cues are much stronger than the intrinsic circuitry, the external cues can dominate over the attractor dynamics, leading to the range of dynamic effects seen when the cues are rearranged. As a result, the white and stippled cells are allowed to fire together because they are being driven by their respective cue sets more strongly than they are being controlled by the intrinsic attractor dynamics. Similarly, the white cellbecomes decoupled from the black cell because the input from the external cues is stronger than the excitatory connections between the two cells. One way in which split place fields might emerge is if certain individual cells are controlled equally by one set of external cues and by other place cells that are controlled by the other set of cues. Cells that gain or lose fields or rotate to arbitrary orientations might result from subsequent alterations in the attractor basins of the network.
Tables
45° 90° 135° 180° Maintain field 90 (65%) 82 (52%) 81 (52%) 79 (59%) Lose field 31 (22%) 51 (32%) 42 (27%) 36 (27%) Gain field 17 (12%) 24 (15%) 34 (22%) 18 (14%)
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