Navigating the interface between learning and cognition

Abstract

The interface of learning and cognition applied to the study of animal behavior represents a target for significant progress if conceptual barriers can be reduced. Is animal behavior exclusively a product of learning or cognition, or are both implicated? Are special (i.e., new) methods required to study cognition or will the enterprise be accomplished by using well-established methods from learning? What types of hypotheses need to be tested to dissociate cognition from learning, and may these hypotheses be profitably tested? This article addresses the above questions by focusing on conceptual, methodological, and hypothesis-testing perspectives for navigating the interface between learning and cognition. Examples from contemporary research are used to develop some suggestions for best practices. The development of a rodent model of episodic memory is used as a case study to feature the validation of an animal model of cognition.

Figure 1

Results of a simulation of reinforcement density as a function of variation in threshold for the uncertainty response. The simulation used the generalization and constant-threshold concepts from Smith et al. (2008). Reinforcement and delays were based on Beran et al. (2006). Although no food was delivered upon selecting the uncertainty response, the simulation shows that the value of the threshold for selecting the uncertainty response influences the amount of food obtained per unit time in the primary discrimination. Thus, the uncertainty response was indirectly reinforced despite efforts to eliminate reinforcement. Reproduced with permission from Crystal, J. D., & Foote, A. L. (2009). Metacognition in animals. Comparative Cognition & Behavior Reviews, 4, 1–16. © J. D. Crystal & A. L. Foote.

Figure 2

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 a study and test phases is shown. Chocolate or chow flavored pellets were available at four arms in the study phase (randomly selected); closed doors prevented access to the other arms. After a 2-min retention interval, chow-flavored pellets were available at previously inaccessible locations in the test phase. Chocolate replenished at the location that had chocolate in the study phase in the replenishment condition (shown for the morning session). Chocolate did not replenish at the other time of day in the non-replenishment condition (shown in the afternoon session). 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. The same study-phase baiting pattern was used in the figure, but these arms were randomly selected in each session for each rat. 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 (i.e., starting at 7 a.m.). 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 (i.e., 7 a.m. in early or 1 p.m. in late sessions). The introduction of 7-hr retention intervals in Experiment 3 produced test phases that occurred at novel times of day (2 p.m. in early and 8 p.m. in late sessions). 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(23), 9525–9529. © 2009 National Academy of Sciences, U.S.A.

Figure 3

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; replenish and non-replenish sessions were presented in random order. b. Rats used time of day, rather than an interval, to adjust revisit rates in Experiment 2. Rats treated the study-test sequence as a morning session, suggesting the use of a time-of-day rather than an interval-timing mechanism. 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(23), 9525–9529. ©2009 National Academy of Sciences, U.S.A.

Figure 4

Schematic representation of Zhou and Crystal’s (2011) study. The morning or afternoon was randomly selected for presentation of study and test phases. The figure shows an example of the accessible arms and flavors in encoding and the corresponding memory assessment phases that would occur after a 2-min retention interval. The presence or absence of chocolate pellets in the central hub immediately prior to memory assessment was needed to predict the replenishment of chocolate in the test phase. 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. The same study-phase baiting pattern was used to illustrate morning and afternoon sessions in the figure to facilitate inspection of presence and absence of chow and chocolate, but these arms were randomly selected in each session for each rat. Reproduced from Zhou, W., & Crystal, J. D.(2011). Validation of a rodent model of episodic memory. Animal Cognition, 14(3), 325–340. © 2011 Springer-Verlag.

Figure 5

Rats preferentially revisit the chocolate location when it is about to replenish when the retention interval was approximately a. 2 min and b. 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; replenishment and non-replenishment conditions were presented in random order. 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. Error bars represent 1 SEM. a. *** p < 0.001 difference between replenishment and non-replenishment conditions. b. 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(3), 325–340. © 2011 Springer-Verlag.

Figure 6

a. In the chocolate probe, rats revisited the corresponding chocolate location in Maze 2 at a higher rate when chocolate was unexpectedly replenished compared with the non-replenishment mixed baseline in Maze 1 (labeled Replenish and Non-replenish) and designated baseline in Maze 2 (labeled Designated; a measure of randomly selected arm entries). The probability of revisiting corresponding chocolate location in Maze 2 is labeled Chocolate Probe. ⁺⁺ p = 0.005 difference between chocolate probe and non-replenishment mixed baseline; ^xxx p = 0.001 difference between chocolate probe and designated baseline. b. In the sucrose probe, rats revisited the corresponding sucrose location in Maze 2 when sucrose was unexpectedly replenished compared with the non-replenishment mixed baseline in Maze 1 and designated baseline in Maze 2. ⁺ p = 0.03 (one-tailed) difference between sucrose probe and non-replenishment mixed baseline; ^xx p = 0.01 difference between sucrose probe and designated baseline. (a–b) Error bars represent 1 SEM. Reproduced from Zhou, W., & Crystal, J. D. (2011). Validation of a rodent model of episodic memory. Animal Cognition, 14(3), 325–340. © 2011 Springer-Verlag.