Episodic-like memory

Episodic-like memory was first demonstrated in the western scrub jay (Aphelocoma californica).

Recent research regarding mental time travel and episodic-like memory has focused on determining whether there are any non-human animals that demonstrate future planning and under what conditions they do so. One species that has frequently been considered is the western scrub jay (Aphelocoma californica), a member of the corvid family of birds native to western North America. These large-brained, long-lived, and highly social birds hide food caches for future consumption and rely on memory to recover their caches of hidden food at a later date, typically weeks if not months into the future.[8] They show an ability to form what-where-when memories characteristic of episodic memory as they remember the spatial location and contents of their caches as well as recalling which conspecifics were watching during caching.

Flexibility within episodic-like memory has been demonstrated within a study by Clayton et al. involving the caching of perishable and non-perishable foods.[2] The jays were allowed to cache perishable and non-perishable items but then discovered, in the interval between caching and recovery, that the perishable food type degraded more quickly than originally thought. They reasoned that, if the birds do use a flexible declarative memory system, they should be able to update their knowledge about the rate of perishability of the food and change their search behaviour at recovery accordingly, even though the episodic information about what they cached where and when was encoded before gaining the new knowledge about the decay rates. Results confirmed this reasoning demonstrating that these birds possess a flexible episodic like memory system where they can update their information after the time of encoding.

An experiment conducted by Dally et al. examined the importance of social living in scrub jays by testing whether storer birds remember the status of the observer bird who watched them during caching – adding a ‘who’ to the what-where-when memory framework.[8] They found that, as predicted, storer birds’ adjusted their behaviour during the initial caching period according to the rank of the observer bird. In the dominant observer bird condition, where they experienced the highest risk of cache theft, storers cached predominantly in the tray farthest away from the observer bird and recached the greatest proportion of items during the recovery period. In a second part of this study, they tested whether scrub jays remember which particular individual was present when they made specific caches. Birds cached in front of observer birds as they did the first part of this study, but then hours later were separated into three conditions where they either recovered their caches in private, in front of an observer bird that watched them cache initially, or in front of a new control bird. They found that the proportion of caches that were recached at recovery differed significantly between conditions and significantly more caches were recached during the observed condition relative to the control condition. This suggests that during the recovery stage, storer birds remember whether the observer bird watching them recover their cache was the same bird who watched them cache initially and engage in additional behaviours to prevent cache theft.

A study of the rufous hummingbird found they were able to learn and remember which flowers in an arrangement contained a nectar reward. Although visual cues such as the type and colour of flower increased how quickly the locations were learned, they weren't necessary for learning. Hummingbirds could remember that only the center flower contained a reward even in arrangements of identical flowers. Artificial flowers were created using small cardboard disks painted in unique colours, the center of which contained a syringe tip filled with a small amount of sucrose solution.[9] When spacing between the flowers was increased, hummingbirds still remembered the relative locations of the flowers in arrangement. When the arrangements of artificial flowers were moved, the hummingbirds remembered which flowers contained nectar, even when the new location of the arrangement placed an empty flower in the location previously occupied by a reward flower.[10]

Hummingbirds demonstrate the ability to recall where certain flowers were located and how recently they were visited.

Rufous hummingbirds are also able to adjust their foraging strategies based on when they've last visited flowers and how often the flower's nectar is renewed. Artificial flowers were refilled in either ten- or twenty-minute intervals upon being emptied. The hummingbirds were able to distinguish between the types of flower and adjust their foraging strategies accordingly. Over time the hummingbirds learned the schedule of renewal and visited the flowers renewed every ten minutes much more frequently than the flowers renewed every twenty minutes.[10] This implies planning on the part of the hummingbird in order to avoid redundant trips and avoid wasting energy. Similar cognitive abilities and foraging strategies were also observed in a study of the green-backed firecrown, another species of hummingbird.[11]

Pigeons have been shown to think back on past experience to generate positive future outcomes.

The pigeon has also been shown to exhibit qualities similar to episodic-like memory.[12] Pigeons respond to a stimulus shown before the presentation of food by thereafter pecking future examples of the stimulus. In the event that a stimulus is presented without food, pigeons will choose not to peck at future presentations of the stimulus. A study at the University of Kentucky aimed to determine whether pigeons could recall their previous actions with regard to certain hues presented either with or without food. The first phase of the experiment involved training the pigeons to peck in response to one stimulus (vertical lines) and refrain from pecking for at least four seconds in response to another stimulus (horizontal lines).[12] The presented stimuli were then followed by both a red and green key. Pecking the green key following a pecking stimulus (vertical lines) resulted in a food reward, as did pecking the red stimulus following a non-pecking stimulus (horizontal lines). This allowed the experimenters to effectively pose questions to the pigeons on their past actions. The pigeons were required to recall what the previous stimulus had been and how they had reacted in order to formulate a correct response and receive a reward.

This differs from other memory tasks where the aim was simply to determine whether a stimulus and response could be paired as a learned association and then testing the memory for that association. This experiment showed a clear use of episodic memory or a similar construct, pigeons were shown to think back on past experience to generate a positive future outcome.

Due to their similarities to humans, researchers have been interested in looking into the episodic memory abilities of non-human primates.[13] However, little uncritisized research has previously been done. For example, Schwartz performed an experiment with gorillas in a task requiring the animal to select the appropriate card that represented the food he had just eaten and who had given it to him.[14] While the gorilla appropriately identified the food items and trainer, it is unclear if he recalled the event or chose the answer most familiar to him. Menzel also showed evidence of episodic memory in apes, however, an alternative explanation is that the chimpanzees were displaying spatial semantic memory.[15] Furthermore, Hampton had mixed results when testing rhesus monkeys; while demonstrating memory for the location and type of food, they lacked sensitivity to when they acquired the knowledge.[16] Thus, more research was required for this type of memory in non-human primates.

Humans and primates may possess some of the same information encoding and storage mechanisms related to episodic memory.

Chimpanzees, orangutans, and bonobos were tested using an adapted design by Clayton and colleagues for experimenting with scrub jays.[17] After five minutes and again at one hour, the apes were presented with the choice of selecting hidden frozen juice, less-preferred grapes, or an empty platform. While the juice was the preferred item, it would melt before the hour. Subjects were both male and female. Food item placement was changed during multiple trials so that the study was not accidentally measuring familiarity. The primates rarely chose the empty platform, and after five minutes preferred the juice solution over the grape. After an hour, while a smaller number of primates chose the juice, the majority of apes still reached for melted juice.

The study also wanted to compare human and primate performance on the task to show episodic memory. Humans exhibit age-dependent performance with inverted U-shaped results, meaning ability increases in childhood, stabilizes for a few years and then descends as adulthood progresses. The similarities in findings found may indicate these primates and humans share some information encoding and storage mechanisms.[17] Future research may be done with a larger sample size and different experiments to replicate the inverted U-shape findings.

Rats demonstrate the ability to discriminate based on the what, where, and when components of episodic-like memory.

A study by Babb and Crystal (2005) provided evidence that rats also demonstrate the ability to discriminate based on what, where, and when.[18] In experiments using a radial arm maze, four of the eight arms of the maze contained food. The other arms were made inaccessible to the rats. Of the food containing corridors of the maze, three contained standard rat-chow pellets while one arm contained high value chocolate-flavoured pellets. This was the first phase of the experiment, defined as the forced-choice phase (some corridors were inaccessible). The second phase was defined as the free-choice phase (all corridors were now accessible to the rats). The period of time between each phase served as a discriminating cue. Some days the interval between phases would be short (30 minutes) other days the interval would be long (4 hours), but only one type of interval was tested each day. On days when a short interval was used, the previously inaccessible corridors were made accessible and were the only corridors to contain regular pellets and no chocolate pellets were refilled. On days using a long interval, pellets were refilled as on short interval days, but in addition, the chocolate pellets were refilled in the location they had originally been found. The rats were able to discriminate based on the length of interval before the test phase, with the phases following a long interval having the rats immediately search in the arm of the maze associated with the location of the high value (chocolate-flavoured) pellets.[18]

Research suggests that honey bees possess Circadian timed episodic-like memory.

Researchers in Australia found what they consider to be Circadian timed episodic-like memory in honey bees. In their study they examined foraging bees in three Y-mazes. Two mazes represented training and testing zones with different time placements. Maze C acted as the location for transfer tests. The bees were placed in Maze A in the afternoon hours of 2:30 to 5:30, whereas Maze B held bees in the morning hours of 9:30 to 12:30. All of the three mazes had two compartments, and in Mazes A and B, one held a sugar solution as a reward for making the positive decision. During training, the compartment containing the positive pattern was changed every thirty minutes. In Maze A, the positive (rewarded) pattern was a blue horizontal pattern, while the negative (non-rewarded) pattern was a blue vertical pattern. Additionally, the positive pattern for Maze B was a yellow vertical (rewarded) pattern, with a yellow horizontal pattern as a negative (non-rewarded) pattern. The three aspects of episodic-like memory in this experiment are the morning or afternoon times (when), either Maze A or B (where), and by using horizontal/vertical patterns (what).

In the first of four experiments, the colour cue was removed by using black patterns, but the shape cues remained the same. The scientists tested whether the bees would still choose the positive pattern; this decision would then be based on the what, where, and when components. Through the other three experiments, one of the cues was examined independently from the others.

They found that, on average, 96% of bees learned to forage at each maze at the appropriate time. The experimenters suggest the error rate can be accounted for by a foraging strategy, in which multiple feeding locations are visited at fixed times.[19] Only a small number of bees visited the incorrect compartment during these times, and usually by only briefly hovered outside of it, instead of entering it. With the addition of visual pattern in this test, the bees also showed 80-88% of the time to have learned which maze to enter at the correct time. With the removal of the colour cue in both of these tests, the results remained consistent. The bees then showed they had learnt these rules by applying them to the new context, Maze C, in experiment 2. In experiment 3, based on colour cue alone, having excluded the pattern and maze location cues, the forager bees could still make a correct decision. In the final experiment, the bees used only pattern orientation cues; the lowered performance showed how much more difficult this was than when the colour cue was still present.

The researchers were uncertain, however, if the honey bees have a sense of time governed by their circadian rhythm by connecting a specific memory to a certain time period in the 24-hour cycle, or if they can measure elapsed time between two events. The difference in this type of memory from other episodic-like memory in animals is the presence of circadian timing, since normally interval timing is displayed.

Randolf Menzel also provided evidence for episodic memory in honey bees by examining their learning of spatio-temporal tasks. The bees showed learning of serial positioning, turning serial patterns into episodes. The bees showed evidence of discrimination, thus at three out of four serial positions, stimuli were independently learned. Menzel suggests strong results may be found by further isolating the configural components. Such serial pattern configuration in mammals has been interpreted as indicative of mental representations of time and space.[20]