Prospective cognition in rats

Abstract

Efforts to develop animal models of memory are critical for understanding the neural substrate of memory. Memory is essential for daily life and enables information to be stored and retrieved after seconds to years. The ability to remember episodes from the past is thought to be related to the ability to plan for the future. Here we focus on a particular aspect of prospective cognition, namely the ability to remember to take action when a future scenario occurs. This review focuses on a recently developed method to evaluate prospective memory in the rat. Available evidence suggests that rats remember to take action in the future, but little is known about the temporal specificity of such memories or about the flexibility and limitations of prospective memories. Recent studies that suggest that rats remember a specific past episode are reviewed to underscore potential approaches that may be used to explore the range and limits of prospective cognition. The review highlights some directions to explore, including the temporal specificity of prospective cognition, the range of flexibility or creativity within prospective cognition, and the constraints imposed by multiple motivational systems.

Fig. 1

Anticipation of a meal reduced sensitivity to time in an ongoing interval-duration classification task near the meal time. Sensitivity to time in the ongoing task declined near the meal time in the meal group but not in the no-meal group. The probability of judging an interval as long (a) increased as a function of the interval duration. Sensitivity to time, 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 and late variable is significant in the meal group (a, p < 0.001) but not in the no-meal group (p = 0.1), and these differences are significant as shown by the three-way interaction (p < 0.009). Similarly, the slope of the psychophysical function was smaller 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 differences are significant as shown by the interaction (p = 0.03). The meal group anticipated the arrival of the meal, as shown 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). (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.

Fig. 2

Roberts and Feeney’s (2009) proposed conceptualization of mental time travel. Memories of the past and planned events for the future are shown at varying temporal distances into the past or future. Temporal remoteness determines disparateness of detail. The size of the cones and balloons represent the clarity of the memories or plans. Because remoteness plays a critical role according to this proposal, Roberts and Feeney further propose that tests for mental time travel in animals must show that animals remember when a specific event occurred in the past and that they are planning for a specific time in the future. Reproduced from Roberts, W. A., & Feeney, M. C. (2009). The comparative study of mental time travel. Trends in Cognitive Sciences, 13, 271-277. © 2009 Elsevier.

Fig. 3

Experimental design of Zhou and Crystal’s (2009) study. a. Design of Experiment 1. The morning or afternoon was randomly selected for presentation of first helpings (study phase; encoding) and second helpings (test phase; memory assessment) of food. An example of the accessible arms and flavors in study and test phases is shown. Chocolate or chow flavored pellets were available at four arms in the study phase (randomly selected). After a 2-min retention interval, chow-flavored pellets were available at previously inaccessible locations in the test phase. Chocolate replenished in the test phase conducted in the morning (7 a.m.) but not in the afternoon (1 p.m.) for half of the rats; these contingencies were reversed for the remaining rats (not shown). For each rat, one session (i.e., study and test phases) was conducted per day. b. Phase-shift design of Experiment 2. Light onset occurred at 12 a.m. (i.e., 6 hr earlier than in Experiment 1) and the study and test phases occurred at the time of a typical morning session. Note that 7 hr elapsed between light onset and the study-test sequence (solid horizontal line), which is comparable to the time between the typical light onset and a typical afternoon session (dashed horizontal line) in Experiment 1. The design of the experiment puts predictions for time-of-day and how-long-ago cues in conflict. Thus, a rat would be expected to behave as in its morning baseline (based on time of day) or as in its afternoon baseline (based on how long ago). c. Transfer-test design of Experiment 3. The time of day at which the study phase occurred was the same as in Experiment 1. The introduction of 7-hr retention intervals in Experiment 3 produced test phases that occurred at novel times of day. 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 consisted of one replenishment and one non-replenishment condition. An early or late session was randomly selected on subsequent days. Differential revisits to the chocolate location is expected if the rats were adjusting revisit rates based on 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 time of day at which 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 and test phases occurred at 1 p.m. and 2 p.m., respectively. These times correspond to the typical time of day at which a late-session study phase and early-session test phase occurred in Experiment 3. The design of the experiment put predictions for time of day at study and time of day at test in conflict. A rat would be expected to behave as in its early-session, second-helpings baseline (based on test time of day) or as in its late-session, second-helpings baseline (based on study time of day). 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.

Fig. 4

a. Rats preferentially revisit the chocolate location when it is 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 shown for replenishment and non-replenishment conditions. b. Rats used time of day, rather than an interval, to adjust revisit rates in Experiment 2. The figure plots the difference between observed and baseline revisit rates. For the bar labeled interval, the baseline was the probability of revisiting chocolate in the afternoon; thus, the significant elevation above baseline shown in the figure suggests that the rats did not use an interval mechanism. For the bar labeled time of day, the baseline was the probability of revisiting chocolate in the morning; thus, the absence of a significant elevation above baseline is consistent with the use of time of day. The horizontal line corresponds to the baseline revisit rate to the chocolate location from Experiment 1. Positive difference scores correspond to evidence against the hypothesis indicated on the horizontal axis. c. and d. Rats preferentially revisited the chocolate location when it was about to replenish 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 conditions (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, suggesting memory of the time of day at study rather than discriminating time of day at test. The figure plots 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; thus, the significant elevation above baseline suggests 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; thus, 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.

Fig. 5

a. Schematic representation of Zhou and Crystal’s (2011) study. The morning or afternoon was randomly selected for presentation of study and test phases. An example of the accessible arms and flavors is shown in encoding and the corresponding memory assessment phases that would occur after a 2-min retention interval. The presence or absence of food in the hub, immediately prior to memory assessment, served as a cue that could be used to predict the replenishment or non-replenishment of chocolate. In the replenishment conditions, chocolate replenished at the location that recently delivered chocolate, which was predicted by the presence or absence of food (e.g., presence of chocolate in the central hub immediately prior to second helpings memory assessment in the morning but absence of chocolate in the hub in the afternoon); these contingencies were reversed in the non-replenishment conditions. These conditions were counterbalanced across rats (not shown). For each rat, one session (i.e., study phase, hub-baiting retrieval cue, and test phase) was conducted per day. Rats preferentially revisit the chocolate location when it is about to replenish when the retention interval was approximately b. 2 min and c. 1hr. The probability of a revisit to the chocolate location in the first four choices of a test phase is shown for replenishment and non-replenishment conditions. Error bars represent 1 SEM. b. *** p < 0.001 difference between replenishment and non-replenishment conditions. c. Each condition was tested once, in random order. ** p = 0.009 difference between replenishment and non-replenishment conditions. Reproduced from Zhou, W., & Crystal, J. D.(2011). Validation of a rodent model of episodic memory. Animal Cognition, 14, 325-340. © 2011 Springer-Verlag.