Further evidence of joint time-place control of rats' behavior: results from an 'open hopper' test.

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.

Spatial working memory and hippocampal size across pregnancy in rats.

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.

Errors made by animals in memory paradigms are not always due to failure of memory.

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 are reluctant to use circadian timing in a 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.

Further evidence that rats use ordinal timing in a daily time-place learning task.

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.

Rats use an ordinal timer in a daily time-place learning task.

Rats received 2 daily sessions in a large clear chamber. A lever was mounted on each of the 4 chamber walls. For each rat, a different lever provided food during 0930 and 1530 sessions. The rats learned which lever would provide food at 0930 and 1530. Probe tests suggested that the rats learned to press 1 lever during their 1st session of each day and to then press a 2nd lever during their 2nd session of each day. We propose that this knowledge of the order of a set of events within a period of time constitutes ordinal timing. We contrast the temporal information provided by ordinal, phase, and interval timing and consider why multiple timing systems have evolved in animals.

Conditional time-place learning.

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.

Some characteristics of spatial associative memory in the pigeon, Columba livia.

Willson and Wilkie (1993) developed a novel procedure to assess pigeons' memory for the spatial location of food. Only one of four locations provided food each daily session. Each location consisted of an illuminated pecking key and grain feeder. Over different days different locations, randomly selected, provided food during a 16-min session. The pigeons tended to revisit the location at which food was found on the previous day thereby demonstrating memory for food-spatial location associations over 24 h. Three experiments were conducted to further investigate this phenomenon. In Experiment 1 the session duration was varied between 4 and 32 min. Longer sessions had no detectable effect on their ability to remember the rewarded location 24 h later, a result that suggests that only brief encounters with food at a particular location are necessary for recall. In Experiment 2 the necessity of an active search for the day's rewarded location was removed; a 5-min period in which only the rewarded key was lit preceded the regular 16-min session. Pecks to the lit key in this 5-min period produced grain on the standard schedule. This manipulation facilitated the pigeons' discovery of food but did not affect their ability to remember the rewarded location, suggesting that the process of search and discovery is not essential to the associative memory process. In Experiment 3, food was available during the complete session (non-depleting condition) or was available only during the first half of the session (depleting condition). No detectable differences in the birds' memory of yesterday's profitable location were found. This suggests that non-depletion of food is not a necessary condition for day-to-day recall of food location. Taken together these findings enlarge our understanding of the spatial associative memory process.

Field observations of time-place behaviour in scavenging birds.

Encoding the spatial location and the time at which significant biological events occur is thought to be a fundamental way in which one form of memory is organized in animals (Gallistel, 1990, The Organization of Learning. MIT Press, Cambridge, MA). If this is true, one would expect to find evidence of this process in a wide variety of animals and in a wide number of situations. We report field observations of scavenging birds at two outdoor locations at which people tend to congregate and eat food, primarily around midday. Scavenging birds appeared to anticipate this peak in food availability and arrived at these locations before the number of people was at a maximum; time of day, not the absolute number of people, was the best predictor of the number of birds at both sites. At a third location where food is not consumed this relationship was not observed. Taken together these observations support the notion that animals represent the spatial and temporal characteristics of biologically important events and use this knowledge to forage efficiently.

Discrimination of ovarian steroids by rats.

Rats' ability to discriminate their hormonal states was examined by observing the effects of ovarian steroids on state-dependent learning using a drug discrimination task. A rat's entry into the correct arm (left or right) of a Y-maze terminated mild foot shock. The arm designated as correct was alternated daily, but was consistently paired with a pretrial injection of hormone or vehicle. In Experiment 1, ovariectomized rats successfully discriminated pretreatment with 4.0 or 8.0 mg/kg progesterone vs. the oil vehicle but not 2.0 or 0.5 mg/kg progesterone vs. oil, or the daily alternation schedule alone (oil vs. oil). In Experiment 2a, ovariectomized rats correctly discriminated pretreatment with progesterone (4 mg/kg) vs. oil or dihydroprogesterone (4 mg/kg) vs. oil, and the results of Experiment 2b, appear consistent with the possibility that the rats discriminated pretreatment with progesterone vs. dihydroprogesterone. In Experiment 3a, ovariectomized rats discriminated on the basis of progesterone (4.0 mg/kg) vs. oil, estrogen (6.4 micrograms/kg estradiol benzoate) vs. oil, and estrogen vs. progesterone. In Experiment 3b, the rats were adrenalectomized, and the procedure from Experiment 3a repeated. The removal of the adrenal glands failed to abolish hormonal discriminations, suggesting that the effect is not adrenally mediated. The results of these studies show that rats can discriminate relatively low doses of ovarian steroids.

The spatial distribution of pigeons' target detection.

Pigeons were trained to detect briefly-presented targets that appeared on a flatscreen computer display. Pecks were detected by a touchscreen mounted on the display. Those that were directed at the targets produced grain reward whereas pecks at locations in which the target had not appeared did not produce reward. A "behavioral fixation" procedure was used to ensure that the pigeons were facing the display when the target was presented. In general, the probability of detecting a target was highest in the region surrounding the fixation point and decreased as the target appeared more peripherally, both horizontally and vertically. These results show that pigeons' ability to detect targets in a frontal plane is not uniform.

Properties of time-place learning by pigeons, Columba livia.

Pigeons received discrimination training in which food reinforcement for key pecking was conditional upon both spatial and temporal cues. In Experiment 1 food was available for periods of 15 min at each of four locations (pecking keys) during a 60-min trial. However, unlike the procedures used in a previous experiment (Wilkie and Willson, 1992, Experiment 2), food availability did not change over time from one location to the next in a simple monotonic (e.g. counterclockwise) manner. Despite making food available in a figure-eight pattern, pigeons' key pecking was still jointly controlled by the spatial and temporal cues. Experiment 2 sought evidence on the nature of the timing mechanism underlying this behavior. The results of manipulations such as turning all of the keys off, and removing and replacing the subjects, suggested that a stopwatch-like mechanism with properties of stop/restart and reset underlies pigeons' time-place learning, at least with the temporal parameters used in these experiments. This finding contrasts with others in the literature that suggests that a circadian mechanism controls birds visits to different spatial locations. It will be important in future research to determine the relations between the different timing systems involved in time-place learning by foragers.

Pigeons' landmark use as revealed in a 'feature-positive', digitized landscape, touchscreen paradigm.

Two pigeons were trained to discriminate between a S - (a digitized image of a grassy field presented on a computer monitor) and a S + (a digitized image of the same field containing a tree, a set of flowers, and a log). The location of the pecks to the images was recorded by a touchscreen. Both subjects quickly learned the discrimination and concentrated their pecks to particular 'landmarks', one pigeon pecking the flowers, the other the tree. This result suggests that the use of digitized images of real-world geographic locations may help us to understand how animals use visual landmarks in spatial navigation, and, in more general terms, how animals perceive and remember in their natural environments.

Time-place learning by pigeons, Columba livia.

In each of two experiments, 2 pigeons received discrimination training in which food reinforcement for key pecking was conditional upon both spatial and temporal cues. In Experiment 1, food was available for periods of 30 s at each of three locations (pecking keys) during trials that lasted 90 s. In Experiment 2, food was available for periods of 15 min at each of four locations (pecking keys) during a 60-min trial. In both experiments, pigeons' key pecking was jointly controlled by the spatial and temporal cues. These data, and other recent experiments, suggest that animals learn relationships between temporal and spatial cues that predict stable patterns of food availability.

Discrimination training facilitates pigeons' performance on one-trial-per-day delayed matching of key location.

Six pigeons were tested on a one-trial-per-day variant of delayed matching of key location. In one condition, a trial began with the illumination of a pair of quasi-randomly selected pecking keys in a large 10-key test box. Pigeons' pecks to one key (the sample) were reinforced with 8-second access to grain on a variable-interval 30-second schedule, whereas pecks to the other key (the distractor) had no scheduled consequences. In the second condition, the nonreinforced distractor was not presented. In both conditions, subjects were removed from the apparatus after 15 minutes and placed in a holding cage. Subjects were subsequently replaced in the box after a delay (retention interval) of 30 seconds and were reexposed to the illuminated sample and distractor keys for 1 minute. If a pigeon made more pecks to the sample during this interval, the distractor was extinguished and subsequent pecks to the sample were reinforced on the previous schedule for an additional 15 minutes. If, however, a pigeon made more pecks to the distractor, both keys were extinguished and the subject was returned to its home cage. For all subjects, matching-to-sample accuracy was higher in the first condition. In a second experiment, the retention interval was increased to 5, 15, and 30 minutes, and then to 1, 2, 4, 8, 12, and 24 hours. Most subjects remembered the correct key location for up to 4 hours, and in one case, up to 24 hours, demonstrating a spatial-memory proficiency far better than previously reported in this species on delayed matching tasks. The results are discussed in terms of the commonly held distinction between working and reference memory.

Further support for the "drift" model of pigeons' short-term memory for spatial location.

The Drift Model is a conception of animals' short-term memory process as manifested in tasks such as delayed matching to sample. The model has four main assumptions. First, an attention focus or pointer moves through memory space representing the information that must be remembered. Second, during sample presentation, the pointer migrates in the direction of memory space representing the sample. Third, during delays (i.e., retention intervals), the pointer drifts in a random walk manner through memory space. Fourth, during the choice phase, subjects choose the alternative in memory space closest to the pointer. The model successfully accounts for many aspects of rats' (Roitblat & Harley, 1988) and pigeons' (Wilkie & Kennedy, 1987) short-term memory for spatial location. In the present research two explicit predictions were derived from the model, tested using pigeons in a delayed matching of key location task, and confirmed.

Hamsters (Mesocricetus auratus ) use spatial memory in foraging for food to hoard.

We have collected evidence that a hoarding species of rodent, the Syrian golden hamster (Mesocricetus auratus), uses spatial memory in foraging for food to hoard. Before each trial, we baited the same four arms of a modified seven arm radial maze with sunflower seeds. During the trial we gave each hamster 15-min access to the maze and observed its behaviour. Typically their behaviour comprised two phases: Upon entering the maze the hamsters frequently explored the arms of the maze, not eating seeds nor storing seeds in their cheek pouches. This exploration was followed by food gathering. In doing this, the hamsters generally visited the baited arms in succession, placing all the seed that they found in an arm into their cheek pouches. While gathering food, the hamsters seldom revisited depleted arms, suggesting that they remembered the locations of depleted food sites.

Rats' short-term memory for brief electrical stimulation of the ventral tegmental area of the brain.

Short-term memory for brief electrical stimulation of rats' ventral tegmentum was assessed in a delayed conditional discrimination procedure in which trials began with a train of either low- or high-intensity stimulations. After a delay (i.e., retention interval) ranging from 0.01 to 4 sec, a lever was inserted, accompanied by a dim or a bright light. Lever-pressing was rewarded with food on low intensity-dim light and high intensity-bright light trials, but not on low-bright or high-dim trials. Discrimination ratios, based on relative responding on rewarded trials, indicated that subjects were able to remember the electrical stimulations, but that there was sometimes substantial forgetting after the 4-sec retention interval. The implications of these results for an understanding of the stimulus properties of electrical brain stimulation were discussed.

Rodents' (Rattus, Mesocricetus, and Meriones) use of learned caloric information in diet selection.

When given a choice between two mashes of equal caloric density but differing flavors, rats (Rattus norvegicus) show a robust preference for the flavor previously associated with a higher calorie food. This finding suggests that rats may identify food quality by sensory cues such as taste. Our initial attempt to show this effect in the golden Syrian hamster (Mesocricetus auratus) failed, apparently because of this species's tendency to store both high- and low-calorie mashes in their cheek pouches during conditioning trials. Initially we attempted to circumvent this seeming morphological constraint on learning by presenting low- and high-calorie mashes on alternate days. This procedure too failed to produce evidence of flavor-caloric learning, although this procedure produced robust learning in another rodent, the Mongolian gerbil (Meriones unguiculatus). Another method of preventing cheek pouching--concurrently presenting low- and high-calorie liquid diets--was more successful; then, hamsters showed clear evidence of flavor-caloric learning. Thus, although flavor-caloric learning is demonstrable in species of rodent besides the rat, the circumstances under which it occurs vary.

Effects of superior colliculus lesions on rats' orienting and detection of neglected visual cues.

Superior colliculus lesions generally result in a deficit in visual orienting described as sensory neglect. This observation was confirmed in this study: Rats with lesions did not orient to some stimuli that intact rats readily oriented to. However, rats with lesions did orient to stimuli that the intact rats treated as more salient. Also, when the less salient stimuli signaled aversive stimulation, the rats with lesions detected these stimuli. These findings suggest that superior colliculus lesions do not affect the detection of visual stimuli that have been neglected.