The availability of food, mates, predators, and other biologically significant stimuli generally varies across both space and time. If these stimuli vary predictably, then it would be advantageous for animals to learn this spatiotemporal variability, so that they might maximally exploit these resources. The ability to learn spatiotemporal variability has become known as time–place learning (TPL). In The Organization of Learning, Gallistel (1990) put forth a theory stating that whenever a biologically significant event occurs, a memory code is formed that includes the nature of the event, as well as the time and place in which it occurred. When the animal is later faced with a biological need, it can consult these time–place–event memory codes, determine when and where that need has been met in the past, and use that information to guide its current behavior. In Gallistel's theory, animals' ability to tell time is of fundamental importance. This chapter examines this ability in rats and pigeons and considers three timing systems: ordinal timing, phase timing, and interval timing.

Gallistel (1990) theorized that when animals encounter a biologically significant event, they automatically form a tripartite code consisting of the time, place, and nature of the event. Recent research examining such time-place learning (TPL) has shown that rats are reluctant to perform TPL tasks and appear to do so only under high-response-cost situations (Thorpe, Bates, & Wilkie, 2003; Widman, Gordon, & Timberlake, 2000). In the present study, we trained rats on a low-response-cost daily TPL task, in which the amount of food varied with the spatiotemporal contingencies. It was found that rats readily learned this task. We hypothesize that, rather than automatically encoding a tripartite code when faced with a biologically important event, rats instead automatically encode bipartite codes consisting of time-event and event-place information.

In time–place learning (TPL) paradigms animals are thought to form tripartite memory codes consisting of the spatiotemporal characteristics of biologically significant events. In Phase I, rats were trained on a modified TPL task in which either the spatial or temporal component was constant, while the other component varied randomly. If the memory codes are tripartite then when one aspect of the code is random the rats should have difficulty learning the constant aspect of the code. However, rats that were trained with a fixed spatial sequence of food availability and a random duration did in fact learn the task. Rats that were trained with a fixed duration and a random sequence did not learn the task. In Phase II all rats were placed on a TPL task in which food availability was contingent upon both spatial and temporal information. According to the tripartite theory, prior knowledge of either aspect of the code should have little effect on the acquisition of the task. The rats that received fixed spatial training learned the task relatively more quickly. The use of bipartite, rather than tripartite codes, is better able to explain the results of the current study.

Rats were trained on an interval time-place learning (TPL) task in which the location of food availability depended on the time since the start of the session. Each of four levers (numbered 1, 2, 3, 4) provided food on an intermittent schedule for two nonconsecutive 3-min periods. The order in which the levers provided food was 1, 2, 4, 3, 2, 3, 1, 4. This order was consistent across sessions. Previous research conducted in our lab has shown that when only four “places” are used, rather than the eight in the present study, rats use a timing strategy to track the location of food. Pizzo and Crystal (2004) recently trained rats on an interval TPL in which each of eight arms of a radial arm maze provided food. They found evidence suggesting that rats used both spatial and temporal information. In the present study, in which a revisiting strategy was used (i.e., each lever provided food on more than one occasion), the rats tracked both the spatial and the temporal availability of food for the first half of the session. Interestingly, in the second half of the sessions, the rats appeared to be timing the availability of food even though they did not know where it would occur. That is, the rats knew the temporal, but not the spatial, contingencies for the second half of the session. It appears that the requirement of revisiting a previously reinforced lever resulted in rats' no longer being able to solve the spatial aspect of the task.

Two experiments with rats were conducted to study interval time-place learning when the spatiotemporal contingencies of food availability were more similar to those likely to be encountered in natural environments, than those employed in prior research. In Experiment 1, food was always available on three levers on a variable ratio (VR) 35 schedule. A VR8 schedule was in effect on Lever 1 for 5 min, then on Lever 2 for 5 min, and so forth. While rats learned to restrict the majority of their responding to the lever that provided the highest density of reinforcement, they seemed to rely on a win-stay/lose-shift strategy rather than a timing strategy. In Experiment 2, the four levers provided food on variable ratios of 15, 8, 15, and 30, each for 3 min. As expected the rats learned these contingencies. A novel finding was that the rats had a spike in response rate immediately following a change from a higher to lower reinforcement density. It is concluded that rats exposed to spatiotemporal contingencies behave so as to maximize the rate of obtained reinforcement.

Previous research has shown that pigeons can remember which of four spatially distinct responses was last reinforced, for at least 72 h. The present study sought to replicate this finding using rats. Rats were tested in an operant chamber containing four spatially distinct levers. In each session one lever was randomly selected to provide reinforcement for 15 min. This reinforced period was preceded by a non-reinforced period that was 30 s long, on average. During the non-reinforced period the amount the rat pressed on the previously reinforced lever was compared to responding on the other three levers, and was taken as a measure of memory. Sessions were separated either by 17 min, 24 or 72 h. Unlike pigeons, rats responded at chance levels following each of these retention intervals. This finding adds to previous research suggesting differences in cognitive processes in rats and pigeons.

Because the presence or absence of memories in the brain cannot be directly observed, scientists must rely on indirect measures and use inferential reasoning to make statements about the status of memories. In humans, memories are often accessed through spoken or written language. In animals, memory is accessed through overt behaviours such as running down an arm in a maze, pressing a lever, or visiting a food cache site. Because memory is measured by these indirect methods, errors in the veracity of statements about memory can occur. In this brief paper, we identify three areas that may serve as pitfalls in reasoning about memory in animals: (1) the presence of ‘silent associations’, (2) intrusions of species-typical behaviours on memory tasks, and (3) improper mapping between human and animals memory tasks. There are undoubtedly other areas in which scientists should act cautiously when reasoning about the status of memory.

The ability of animals to associate an event with predictable time and place information confers a major biological advantage. The current research uses a variety of procedures and paradigms (e.g. place preference, radial arm maze, Morris water maze, T-maze, go no-go) to show that rats, unlike pigeons [e.g. Anim Learn Behav 22 (1994) 143] do not readily make an event-time-place association. They do make associations between event-time and event-place information, however. These findings are in disagreement with Gallistel's (The Organization of Learning, MIT Press, Cambridge, MA ) theory that claims that animals automatically store a memory code that has these three pieces of information. The present research is in line with the work of others who also find that rats do not readily make daily time-place associations [Behav Processes 23 (1997) 232; Behav Processes 52 (2000) 11; Behav Processes 49 (2000) 21; Anim Learn Behav 28 (2000) 298]. An interesting finding that did emerge from the present research was that at least some rats can use a circadian timer to solve a time-of-day discrimination if the task is a go no-go discrimination.

In time-place learning tasks food availability depends upon both spatial and temporal variables. For example, food might be first available at location one, then location two, then location three, and finally location four. To date, the duration of food availability at each of the locations have been identical (e.g. for 4 min). The major purpose of the present experiment was to determine if rats can successfully learn a time-place task in which four locations provided food for different durations. Lever 1 intermittently produced food for 6 min, then Lever 2 produced food for 4 min. Lever 3 and 4 provided food for 2 and 8 min, respectively. Rats were able to learn this unequal interval time-place task. However, their behavior on this unequal interval time-place task was not in agreement with Scalar Expectancy Theory/Weber's Law.

How rats process spatiotemporal information in the face of distraction was assessed. Rats were trained on a time-place learning task in which the location of food availability depended on the amount of time elapsed since the beginning of the training session. In each training session each of four levers provided food pellets for 5 min on an intermittent schedule. In probe sessions interspersed with the final training sessions, the rats were presented with a second highly preferred food source-a piece of cheese-at various times into the session. Rats choose the correct lever after the cheese distraction, but it appeared that their internal clock had stopped during the cheese consumption period. Thus rats' internal clock, like that of pigeons, displays the properties of 'stop', 'reset', and 'restart'. Rat-pigeon differences in timing processes may be restricted to circadian or time of day timing. Present results also suggest that rats process spatial and temporal information separately.

This experiment examined the effect of medial prefrontal lesions on time–place learning in the rat. During the first phase, prior to lesioning, rats received training on an interval time–place task. Food was available on each of four levers for 3 consecutive min of a 12-min session. The levers provided food in the same sequence on all trials. Rats restricted the majority of their presses on each lever to the time in each session when it provided food and were able to anticipate when a lever was going to provide food. During the second phase some rats received lesions that were restricted to the medial prefrontal cortex. Following these very restricted lesions, rats continued pressing a lever after it stopped providing food (i.e. perseverated, as if their internal clock was running slow). The third phase involved changing the order in which the levers provided food. Lesions had no discernable effect on the rats' ability to learn the correct sequence of food availability. However, this change made the rats' timing perseveration even more noticeable. Our results suggest the medial prefrontal cortex is not necessary for acquisition of time–place sequencing information. However, lesions do appear to produce perseveration on components of the sequence.

Rats were trained on an interval time-place task. Food was intermittently available on each of four levers for 4 min in a 16-min session. After baseline training the rats received 'open hopper' sessions in which food was available on all levers for all of the 16-min sessions. Despite the absence of any contingencies for doing so, the rats continued to press the levers in the 'correct' sequence, for roughly the 'correct' amount of time. This confirms that the rat behavior was controlled, in part, by a representation of an elapsed interval of time. The rats responding was more variable in 'open hopper' sessions and error increased (in an exponential fashion) as the session proceeded. This finding suggests that the rats may have used shifts in the location of food availability to minimize the accumulation of error throughout baseline sessions.

The present experiments investigated the effects of pregnancy on performance in the Morris water maze and on hippocampal volume. In the first study, pregnant rats (in between the first and second trimester) outperformed nonpregnant rats on the Morris water maze on 1 day of testing. In the second study, rats were tested in a working memory variation of the maze in which the spatial location of the platform varied. Pregnant females traveled shorter distances than nonpregnant females during the first two trimesters, but performed worse than nonpregnant females during the third trimester. Latency measures showed a similar profile. Group differences in performance were not related to changes in swim speed. However, changes in performance in pregnant females may be related to estrogen, progesterone, and/or corticosterone levels during pregnancy, with low levels of estradiol and high levels of progesterone being associated with better performance. There were no significant differences between pregnant and nonpregnant animals on any of the brain measures, although pregnant animals tended to have a smaller hippocampus than nonpregnant animals. These results indicate that pregnancy can affect performance, possibly related to the hormonal changes that accompany pregnancy.

In the literature on animals' spatial cognition several investigators have started to use photographs and digitized computer images as stimulus materials. In the current paper a representative overview of this research is described. Research on the following topics is reviewed: 1) habitat preference in migrating birds, 2) conceptual categorization of naturalistic spatial locations, 3) pigeons' use of landmarks in pictures of naturalistic spatial locations, 4) pigeons' attention to certain features in naturalistic spatial locations, and 5) pigeons' attention to the natural horizon. The paper concludes by describing the broad generalizations that emerge from this research.

Rats received morning, midday, and afternoon sessions each day in a chamber located in a room containing distal spatial cues. A lever was mounted on each of the four walls. The rats could work for food on a different lever during each of the three sessions. The rats were able to learn the location of food availability during morning, midday, and afternoon sessions. Results obtained after skipped morning, midday, and afternoon sessions support our contention that rats solve this time–place task using ordinal timing, or knowledge of the daily spatiotemporal sequence of food availability. However, during probe sessions when the predicted location of food availability based on ordinal information conflicted with the predictions based on other types of information, behavioural compromise was evident. It appears that rats use multiple types of information, one of which is ordinal timing, to track the location of food availability in the daily time–place task.

On daily time–place learning tasks animals can work for food at different spatial locations during sessions at different times of the day. In previous experiments rats tracked this pattern of food availability with ordinal timing—they learned to respond at the locations in the correct order each day. In contrast, pigeons used circadian timing. In this experiment rats received a mixture of morning session only days, afternoon session only days, and morning and afternoon session days. Under these conditions ordinal timing had low predictive ability, but circadian timing was potentially perfectly predictive of the location of food availability. We thought this procedural change might encourage rats to use circadian timing. However, we found little evidence that rats can use time of day information to track this daily spatiotemporal pattern of food availability. These results are suggestive of differences in the use of circadian clock consultation by rats and pigeons.

It is commonly assumed that errors in animal memory paradigms such as delayed matching to sample, radial mazes, and food-cache recovery are due to failures in memory for information necessary to perform the task successfully. A body of research, reviewed here, suggests that this is not always the case: animals sometimes make errors despite apparently being able to remember the appropriate information. In this paper a case study of this phenomenon is described, along with a demonstration of a simple procedural modification that successfully reduced these non-memory errors, thereby producing a better measure of memory.

Rats were tested on the interval time-place task. During test sessions, 4 levers provided food in succession. Each lever provided food pellets on a variable ratio schedule for an equal period of time, which ranged from 4 to 8 min across 3 groups of rats. Experienced rats restricted the majority of their responses on each lever to the reinforced period of sessions and anticipated the 3 changes in the location of food availability during each session. Analyses based on Weber's law suggested that the rats restarted timing as they moved from 1 lever to the next. The advantages of this strategy, and its functional similarity to animals' use of landmarks during dead reckoning navigation, are explored.

Encoding the spatial location and the time at which significant biological events occur is thought to be a fundamental way in which memory is organized in animals. Some field data on gulls' foraging behavior suggests that time-place behavior may consist of a conditional discrimination. In this study gulls flew at sunrise to locations containing earth worms, but only after rainfall. The purpose of the present research was to attempt to demonstrate conditional time-place learning in the laboratory. Pigeons were trained to visit three sites successively in two different orders that were signaled by room and test chamber cues. The pigeons successfully learned the task, supporting the notion that time-place foraging behavior can be modulated by other environmental regularities.