Rats acquire a low-response-cost daily time-place task with differential amounts of food.

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.

The role of spatial and temporal information in learning interval time-place tasks.

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' performance on an interval time-place task: increasing sequence complexity.

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.

Interval time-place learning by rats: varying reinforcement contingencies.

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.

Spatial associative memory: a possible species difference in rats and pigeons.

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 30s 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.

Some pitfalls in measuring memory in animals.

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.

Rats have trouble associating all three parts of the time-place-event memory code.

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.

Unequal interval time-place learning.

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.

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.