Remembering the past and planning for the future in rats

Abstract

A growing body of research suggests that rats represent and remember specific earlier events from the past. An important criterion for validating a rodent model of episodic memory is to establish that the content of the representation is about a specific event in the past rather than vague information about remoteness. Recent evidence suggests that rats may also represent events that are anticipated to occur in the future. An important capacity afforded by a representation of the future is the ability to plan for the occurrence of a future event. However, relatively little is known about the content of represented future events and the cognitive mechanisms that may support planning. This article reviews evidence that rats remember specific earlier events from the past, represent events that are anticipated to occur in the future, and develops criteria for validating a rodent model of future planning. These criteria include representing a specific time in the future, the ability to temporarily disengage from a plan and reactivate the plan at an appropriate time in the future, and flexibility to deploy a plan in novel conditions.

Figure 1

Schematic representation of experimental design of Zhou and Crystal’s (2009) study. a. Design of Experiment 1. First helpings (study phase; encoding) and second helpings (test phase; memory assessment) of food was presented either in the morning or afternoon, which was randomly selected for each session and counterbalanced across rats. Study and test phases show an example of the accessible arms, which were randomly selected for each rat in each session. Chocolate or chow flavored pellets were available at the distal end of four arms in the study phase (randomly selected). After a 2-min retention interval, the test phase provided chow-flavored pellets at locations that were previously blocked by closed doors. The figure shows chocolate replenished in the test phase conducted in the morning (7 a.m.) but not in the afternoon (1 p.m.), which occurred for a randomly selected half of the rats; these contingencies were reversed for the other rats (not shown). For each rat, one session was conducted per day. b. Phase-shift design of Experiment 2. Light onset occurred at midnight, which was 6 hr earlier than in Experiment 1, and the session occurred in the morning. The horizontal lines emphasize the similarity of the 7-hr gap between light onset and sessions in probe (solid) and training (dashed) conditions in Experiment 1. This design puts the predictions for time-of-day and how-long-ago cues in conflict; performance typical of the morning baseline is expected based on time of day whereas afternoon performance is expected based on how long ago. c. Transfer-test design of Experiment 3. Study phases occurred at the same time of day as in Experiment 1. Test phases occurred at novel times of day (7 hr later than usual). Therefore, early and late sessions had study times (but not test times) that corresponded to those in Experiment 1. The first two sessions in Experiment 3 were one replenishment and one non-replenishment condition, counterbalanced for order of presentation. An early or late session was randomly selected on subsequent days. More revisits to the chocolate location are expected in replenishment compared to non-replenishment conditions if the rats remembered the time of day at which the study episode occurred; revisit rates are expected to be equal in early and late sessions if the rats used the current time of day when the test phase occurred. Study and test phases were as in Experiment 1, except that they were separated by 7-hr delays (shown by horizontal brackets). d. Conflict-test design of Experiment 4. The study phase occurred at 1 p.m. and was followed by a test phase at 2 p.m. These times correspond to the time of day at which a late-session study phase and early-session test phase occurred in Experiment 3, which put predictions for time of day at study and time of day at test in conflict. If rats remembered the time of day at which the study episode occurred, they would be expected to behave as in its late-session, second-helpings baseline; alternatively, if the rats used the current time of day at test, they would be expected to behave as in its early-session, second-helpings baseline. Reproduced with permission from Zhou, W., & Crystal, J. D. (2009). Evidence for remembering when events occurred in a rodent model of episodic memory. Proceedings of the National Academy of Sciences of the United States of America, 106, 9525–9529. © 2009 National Academy of Sciences, U.S.A.

Figure 2

a. Rats preferentially revisited the chocolate location when it was about to replenish in Experiment 1. The probability of a revisit to the chocolate location in the first four choices of a test phase is plotted for replenishment and non-replenishment conditions. b. Rats used time of day, rather than information about remoteness, to adjust revisit rates in Experiment 2. The figure shows the difference between observed and baseline revisit rates. For the bar labeled interval, the baseline is the probability of revisiting chocolate in the afternoon. The significant elevation above baseline shown in the figure documents that the rats did not use remoteness or an interval mechanism. For the bar labeled time of day, the baseline is the probability of revisiting chocolate in the morning. The absence of a significant elevation above baseline is consistent with the use of time of day. The horizontal line corresponds to the baseline rate of revisiting the chocolate location in Experiment 1. Positive difference scores correspond to evidence against the hypothesis shown on the horizontal axis. c. and d. Rats preferentially revisited the replenishing chocolate location when the study, but not the test, time of day was familiar in Experiment 3. The probability of a revisit to the chocolate location in the first four choices of a test phase is shown for first replenishment and first non-replenishment sessions (c; initial) and for subsequent sessions (d; terminal). e. Rats remembered the time of day at which the study episode occurred in Experiment 4. Rats treated the novel study-test sequence as a late-session test phase, documenting memory of the time of day at study rather than discriminating time of day at test. The figure shows the difference between observed and baseline revisit rates. For the bar labeled test time, the baseline was the probability of revisiting chocolate in the test phase of the early session in Experiment 3. The significant elevation above baseline documents that the rats did not use the time of day at test to adjust revisit rates. For the bar labeled study time, the baseline was the probability of revisiting chocolate in the test phase of the late session in Experiment 3. The absence of a significant elevation above baseline is consistent with memory of the time of day at study. The horizontal line corresponds to the baseline revisit rate to the chocolate location from Experiment 3 (terminal). Positive difference scores correspond to evidence against the hypothesis indicated on the horizontal axis. a–e. Error bars indicate SEM. a, c, and d. The probability expected by chance is 0.41. Repl = replenishment condition. Non-repl = non-replenishment condition. a. * P < 0.001 difference between conditions. b. * P < 0.04 different from baseline. c and d. * P < 0.04 and ** P < 0.0001 difference between conditions. e. * P < 0.001 different from baseline. Reproduced with permission from Zhou, W., & Crystal, J. D. (2009). Evidence for remembering when events occurred in a rodent model of episodic memory. Proceedings of the National Academy of Sciences of the United States of America, 106, 9525–9529. ©2009 National Academy of Sciences, U.S.A.

Figure 3

Schematic representation of experimental design of training from Zhou, Hohmann and Crystal’s (2012) study. a. Five-arm task. Each rat was presented with study and test phases, separated by a brief retention interval (1 trial/day). An example of the accessible arms in the study phase and corresponding test phase is shown. Accessible arms were randomly selected for each rat on each session. Grey shading in the figure identifies arms used in the five-arm radial maze task. Doors to T-maze arms (shown in white) were closed. b. T-maze task. Sample and choice phases were separated by a brief retention interval. In the sample phase, each rat was either given food (6 pellets) or no food (0 pellets). In the choice phase, each rat was rewarded with 6 pellets after turning left or right. Food and no-food samples led to reward in opposite sides of the T maze (counterbalanced across rats). Six trials were conducted per day with a random order of food and no-food samples. Doors to the five-arm radial maze were closed. a–b. All arms of the actual maze were white. Reproduced with permission from Zhou, W., Hohmann, A. G., & Crystal, J. D. (2012). Rats answer an unexpected question after incidental encoding. Current Biology, 22, 1149–1153. © 2012 Elsevier Ltd.

Figure 4

Schematic representation of experimental design of probes from Zhou, Hohmann and Crystal’s (2012) study. a. Food and b no-food probes started with a study phase in the five-arm-radial-maze using arms situated 135°, 180° and 225° opposite to the sample arm. In the food probe, rats encountered one pellet at each of the three arms. In the no-food probe, rats visited these three arms but did not receive food pellets. Next, two choice arms from the T-maze were opened. c. The rotation probe was identical to T-maze training (Figure 3B), except the sample was presented in the arm 180° opposite to that used in T-maze training. a–c. All arms of the actual maze were white. Reproduced with permission from Zhou, W., Hohmann, A. G., & Crystal, J. D. (2012). Rats answer an unexpected question after incidental encoding. Current Biology, 22, 1149–1153. © 2012 Elsevier Ltd.

Figure 5

a. Rats answered unexpected questions after incidentally encoding the presence or absence of food. Baseline data come from the first daily T-maze trial in the terminal five days before probe testing. Food and no-food probes were each conducted once per rat. b. Temporary inactivation of CA3 of the hippocampus before encoding impaired accuracy in answering an unexpected question relative to baseline but did not interfere with answering the expected question (rotation probe). Accuracy was selectively reduced by lidocaine in the unexpected probe relative to baseline and other probes. Baseline data come from the first daily T-maze trial in sessions before and after surgery. Each rat was tested once in each probe condition with the order counterbalanced according to a Latin Square design. Error bars represent 1 SEM. * p < 0.01 difference between the unexpected + lidocaine probe and baseline. Reproduced with permission from Zhou, W., Hohmann, A. G., & Crystal, J. D. (2012). Rats answer an unexpected question after incidental encoding. Current Biology, 22, 1149–1153. © 2012 Elsevier Ltd.

Figure 6

Performance in an ongoing task was selectively impaired near the time of an anticipated future event. The probability of judging an interval as long (a) increased as a function of the interval duration, as expected. Performance, as measured by the slope of the probability function (b) declined immediately before the end of the daily session in the meal group (a) but not in the no-meal group (not shown). Importantly, the interaction between early vs. late time points and duration was significant for the meal group (a, p < 0.001) but not for the no-meal group (p = 0.1), and these group differences were significant as documented by the three-way interaction (p < 0.009). Similarly, the slope of the psychophysical function was smaller (i.e., poor performance) at the late relative to early time points (p = 0.009) in the meal group but not in the no-meal group (p = 0.8), and these group differences were significant as documented by the interaction (p = 0.03). The meal group anticipated the arrival of the meal, as documented by the increase in food-trough responses before the meal whereas the increase in food-trough responses was absent in the no-meal group (c). These data document a selective impairment in performance in an ongoing task near the time of an anticipated future event (but not at other times). (a–c) Error bars indicate SEM. Reproduced from Wilson, A. G. & Crystal, J. D. (2012). Prospective memory in the rat. Animal Cognition. 15, 349–358. © 2011 Springer-Verlag.